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McGRAW-HILL PUBLICATIONS IN THE
BOTANICAL SCIENCES
EDMUND W. SINNOTT, Consulting Editor

INTRODUCTION TO CYTOLOGY

Selected Titles From

McGRAW-HILL PUBLICATIONS IN THE
BOTANICAL SCIENCES

Edmund W. Sinnott, Consulting Editor

Babcock and Clausen — Genetics

Belling — The Use of the Microscope

Boysen Jensen- — Growth Hormones
in Plants

Braun-Blanquet and Fuller and Can-
ard— Plant Sociology

Curtis — The Translocation of Solutes
in Plants

Fames — Morphology of Vascular
Plants

Eames and MacDaniels — Plant
Anatomy

Fitzpatrick — The Lower Fungi

Gaumann and Dodge — Comparative
Morphology of Fungi

Hill — Economic Botany

Hill, Overholts, and Popp — Botany

Loomis and Shull — Methods in Plant
Physiology

Lutman — Microbiology

Maximov — Plant Physiology

Miller — Plant Physiology

Pool — Flowers and Plants

Seifriz — Protoplasm

Sharp — Cytology

Sinnott — Botany

Sinnott and Dunn — Genetics

Smith — Fresh-water Algae

Swingle — Systematic Botany

Weaver — Root Development of Field
Crops

Weaver and Bruner — Root Develop-
ment of Vegetable Crops

Weaver and Clements — Plant Ecology

Wodehouse — Pollen Grains

There are also the related series of McGraw-Hill Publications in the Zoologi-
cal Sciences, of which A. Franklin Shull is Consulting Editor, and in the
Agricultural Sciences, of which Leon J. Cole is Consulting Editor.

INTRODUCTION TO

CYTOLOGY

BY
LESTER W. SHARP

Cornell University

"The most important discoveries of the laws, methods
and progress of nature have nearly always sprung from
the examination of the smallest objects which she
contains, and from apparently the most insignificant
enquiries." — Lamarck, Philosophie Zoologigue.

Third Edition
Fourth Impression

McGRAW-HILL BOOK COMPANY, Inc.

NEW YORK AND LONDON
1934

Copyright, 1921, 1926, 1934, by the
McGraw-Hill Book Company, Inc.

PRINTED IN THE UNITED STATES OF AMERICA

All rights reserved. This book, or

parts thereof, may not be reproduced

in any form without permission of

the publishers.

THE MAPLE PRESS COMPANY, YORK, PA.

To the memory of my father
LESTER ALLEN SHARP

PREFACE TO THE THIRD EDITION

An unfortunate though inevitable result of advance in any field of
knowledge is the rapid obsolescence of textbooks. In cytology, the
years just past have witnessed the accumulation of a wealth of new
observations, including a number of significant discoveries calling for a
decided revision of certain concepts and statements which seemed
adequate when the second edition of this book was prepared. Many
of the questions troublesome at that time have received answers or
what is often fully as important, more precise formulation. New and
equally perplexing problems have arisen, but on the whole the cytological
picture, particularly those portions of interest to the geneticist, appear
notably clearer than they did eight years ago.

Next to the desire to bring the book into better accord with the
present state of the subject in both text and illustration, the chief thought
in preparing this edition has been that of improving its adaptability to
the needs of students with comparatively little experience in the special
field of cytology, without, however, making it an elementary treatise.
To this end much of the material has been rearranged, the treatment of
many points has been simplified, and certain border-line topics have been
omitted altogether. Most of the citations to literature have been
transferred from the body of the text to footnotes, where they are still
available to the advanced student but need not confuse the beginner.
Instructors will often find it advisable to omit or rearrange certain
sections of the book in their class work. Much of the special matter in
the opening chapters, for example, might w^ell be considered later in
courses. In accordance with repeated recommendations from users of
the book, most of the former bibliography has been retained in spite of
its length.

This edition, like the earlier ones, treats chiefly of the structural
and genetical aspects of cytology. An especially valuable complemental
work is J. Gray's A Textbook of Experimental Cytology, which deals at
length with the results of physical and chemical researches on the cell.
Among other recent general works of value to the student should be
mentioned Special Cytology, edited by E. V. Cowdry, K. Belaf's Die
Cytologischen Grundlagen der Vererhung, C. D. Darlington's Recent
Advances in Cytology, and Traite de Cytologic Vegetale by A. Guilliermond,
G. Mangenot, and L. Plantefol. Of special interest to readers of Japanese
are G. Yamaha's Saibo and Y. Sinoto's Japana Historio Citologia.

vii

viii PREFACE TO THE THIRD EDITION

The author takes pleasure in acknowledging his indebtedness to those
who have aided him in many ways during the course of the work. He is
particularly grateful to Dr. Barbara McClintock, Dr. L. F. Randolph,
Dr. Lillian Hollingshead Hill, Dr. Harriet Creighton, and Dr. Marcus
M. Rhoades for their valued criticisms of a number of the chapters and
for generous contributions of new material.

L. W. S.
Ithaca, New York,
November, 1933.

PREFACE TO THE FIRST EDITION

This book has been prepared for students of the biological sciences who
desire a means of becoming more readily acquainted with the literature
and problems of cytology. It does not pretend to be an exhaustive
treatise for the use of experienced cytologists, though it is hoped that to
them also some of its features may be of service.

For a number of years students of biology, especially those working
along botanical lines, have been faced with the task of searching through
a widely scattered literature for information on various cytological
subjects. It is the purpose of this book not to render the consultation of
that literature unnecessary, but only to make it easier; the student can
scarcely be too strongly urged to derive his information from original
sources wherever possible. The author does not presume to replace, but
rather aims to supplement. Professor Wilson's well-known book. The
Cell in Development and Inheritance, which, though written twenty years
ago and with the emphasis primarily on the zoological side, will remain
invaluable to all workers for many years to come. The more recent
works of Gurwitsch (Morphologie und Biologie der Zelle), Heidenhain
(Plasma und Zelle), and Buchner (Prakticum der Zellenlehre) are of
importance, especially to the zoologist.

The living cell, or protoplast, which represents an organized proto-
plasmic unit of structure and function, obviously cannot receive complete
description in structural terms. Until a comparatively recent period
cytological researches dealt primarily with cell structure, including
particularly the conspicuous changes undergone by this structure in
connection with the reproduction of the cell (cell-division) and of the
multicellular organism (maturation and fertilization). A gradual shifting
of emphasis has since led to the opening of fruitful fields in other direc-
tions, and the important results already achieved have shown with
increasing clearness the need for a closer acquaintance with the physi-
ological aspects of cell activity, not only in metabolism and growth, but
also in the reproductive phases of the life cycle. The present work,
though dealing mainly with the structural aspects of the subject, may aid
indirectly in fulfilling the above need by making the prerequisite data of
cell morphology more readily available.

Throughout the book, which in many of its chapters treats chiefly
of the plant cell, attention is focused upon the protoplast; the cell wall
is given only brief consideration, since it plays a relatively minor role in
the processes of particular interest to the cytologist at the present time.

ix

X PREFACE TO THE FIRST EDITION

Because of their fundamental importance in connection with the problems
confronting the geneticist, the phenomena of nuclear division, chromo-
some reduction, and fertilization are described with considerable fullness,
and their relation to the problems of heredity is taken up in five special
chapters. With regard to many of the subjects treated, it has not been
found possible to formulate final conclusions, since in many cases nothing
more than tentative general statements are warranted by the facts in
our possession. In some chapters little more than catalogs of conflicting
opinions can be given, but in such a form the state of certain questions
is not inaccurately represented. The student entering upon the field of
cytology will be impressed by the large number of special points which
remain undetermined and general questions which await adequate
answers. If he can look upon cytology as a developing science, and if
he has reached the stage at which he no longer demands categorical
answers to all his questions, this book will be of interest to him as much
for the problems it raises as for those it helps to solve. Not the least of
its functions is to indicate lines of research along which he can hope to
make contributions to the subject.

In compiling his materials the author has not hesitated to draw very
freely upon the writings of others. In many cases where direct quotation
is not made, the language of the originals has been closely followed in
order to lessen the likelihood of misrepresentation. His great debt to
Professor Wilson's book will be apparent to all those familiar with that
admirable work. The majority of the diagrams and a number of the
other figures are new. Most of the latter, however, have been redrawn
from works cited in the text, not only that the value of the book may be
enhanced by the presence of authoritative illustrations, but also that the
student may be encouraged to become more familiar with the original
papers. The general systematic positions of organisms indicated in the
text by their scientific names only may be ascertained by referring to
the generic names in the index.

The illustrations are largely the work of Miss Mildred Stratton, in
whose skill and spirit of cooperation the author has had invaluable
assistance. The criticisms of the text kindly given by Professor C. J.
Chamberlain of the University of Chicago and Professor R. A. Emerson
of Cornell University have been very highly appreciated. Acknowledg-
ments are also made to the author's other colleagues for their advice
and continued encouragement. Further criticisms looking toward the
improvement of future editions will be welcomed.

L. W. S.
Ithaca, New York,

September 8, 1920.

CONTENTS

Page
Preface to the Third Edition vii

Preface to the First Edition ix

CHAPTER I

Cells and Tissues 1

Description of the cell — Living and fixed cells — Development — Differentia-
tion— Correlation — Cell theory and organismal theory.

CHAPTER II

Protoplasm 25

Chemical nature — Physical nature — Colloidal state of matter — Colloidal
nature of protoplasm — Ectoplasm and plasma membrane — Vacuole mem-
brane— Ectoplast of Protista — Kinoplasm— Protoplasm and metaplasm —
Protoplasm and life.

CHAPTER III

The Nucleus 48

General features — Structure — Nucleolus — Functions.

CHAPTER IV

Plastids 61

Occurrence and general characters — Chromoplasts — Photosynthesis — Elaio-
plasts — Eyespot — Structure of chloroplast — Origin and multiplication —
Conclusions.

CHAPTER V

The Golgi Material 73

Occurrence and general characters — Behavior in cell-division — Role in
secretion — Comparison with plant cells.

CHAPTER VI

Chondriosomes 82

Occurrence and general characters — Physical and chemical nature — Origin
and multiplication — Function — Chondriosomes and plastids — Conclusion.

CHAPTER VII

Ergastic Substances 93

Vacuoles — Cell sap — Carbohydrates — Proteins — Fats and allied substances
— Crystals — Recapitulation: structure of the protoplast.

CHAPTER VIII

Somatic Cell-division 105

Outline of somatic mitosis — Cytokinesis — Cell-division in animals — Dura-
tion and periodicity of cell-division — Summary and conclusions.

xi

60918

xii • CONTENTS

CHAPTER IX P.,oE

The Morphology of the Chromosomes 114

Size and general form — Spindle-attachment region — Nucleolus-forming
region — Other specialized regions — The chromosome complement — Arrange-
ment of chromosomes in the mitotic figure — Chromosome complements in
related organisms.

CHAPTER X

The Structure of the Chromosomes 132

Chromonema theory — The mitotic cycle — Slender and small chromosomes —
Chromonemata in sporocytes — Alveolation theory — Chromomere theory —
Chromomeres in the chromonema — Chromosome structure and the gene
theory — Continuity of the chromosome.

CHAPTER XI

The Achromatic Figure 149

Anastral figures — Amphiastral figures — Mechanism of mitosis.

CHAPTER XII

Cytokinesis and the Cell Wall 165

Furrowing in plants — Furrowing in animals — Cytokinesis by cell-plates —
Cell wall^Composition of the cell wall — Ultramicroscopic structure of
wall — Walls of spores — Cell membranes of animals.

CHAPTER XIII

Atypical Mitosis and Other Nuclear Phenomena 183

Amitosis — Induced aberrations of mitosis — Karyosome nuclei — Blue-green
algse — Bacteria — Chromidia.

CHAPTER XIV

Gametogenesis and Sporogenesis 196

Alga) — Fungi — Bryophytes — Pteridophytes-^Gymnosperms — Angiosperms
— Oogenesis in animals — Spermatogenesis in animals — Structure of other
ciliated cells.

CHAPTER XV

Syngamy 226

Plants: Algae — Fungi — Bryophytes and Pteridophytes — Gymnosperms —
Angiosperms. Animals: Nucleus — Centrosome — Cytoplasm and chondrio-
somes — Conjugation and endomixis — Physiology of fertilization — Con-
clusion.

CHAPTER XVI

Meiosis 250

Stage of life cycle at which meiosis occurs — Preliminary sketch — Detailed
description — Disjunctional and equational division — The chiasma — The
synaptic reaction — Meiosis in lower organisms — Conclusion.

CHAPTER XVII

Chromosomes and Mendelian Heredity 284

Development and heredity — Role of the nucleus — Examples of Mendelian
heredity — Terminology — Cytological basis of Mendelian heredity — Linkage

CONTENTS " xiii

Page
and crossing-over — Assignment of linkage groups to chromosomes — Location
of genes in the chromosome — Chromatid exchange as the mechanism of
recombination — Mendelism in monoploid plants — The gene theory —
Summary.

CHAPTER XVIII

Fragmentation and Translocation 314

Fragmentation of chromosomes — Behavior of free fragments — Inversion —
Translocation — Bearing on the chromosome map — Discussion.

CHAPTER XIX

Reciprocal Translocation 327

Origin of the theory (Datura) — Reciprocal translocation in Zea — ffinothera.

CHAPTER XX

Heteroploidy 339

Terminology — Heteroploidy in related species — Chromosome numbers in
related genera— Heteroploidy within species and individuals — How differ-
ences in number arise — Autoheteroploidy and alloheteroploidy.

CHAPTER XXI

The Cytogenetics of Autoheteroploid Plants 350

Tetraploids and tetrasomics — Triploids and trisomies — Other heteroploids —
Monoploid sporophytes — Other features of autoheteroploids.

CHAPTER XXII

The Cytogenetics of Hybrids 359

Diploid hybrids with good synapsis and fertility — Partial asynapsis and its
results — Synapsis in relation to polyploidy in hybrids — Analysis of allo-
heteroploid types — Amphidiploid hybrids — Parental characters in polyploid
hybrids — Segregation of parental chromosome sets — A fertile tetraploid
obtained through a sterile triploid — Conclusions.

CHAPTER XXIII

Chromosomes and Sex 375

Sex-chromosomes in animals — Bryophytes — Algaj and Fungi — Angio-
sperms — Sex-linkage — Heteroploidy and sex — Modification of sex — Con-
clusion.

CHAPTER XXIV

Apomdcis and Related Phenomena 401

Plants: Apomixis — Parthenogenesis — Apogamy — Sporophytic budding —
Apospory — False hybrids — Pseudogamy — Androgenesis — M e r o g o n y —
Causes of apomixis. Animals: Parthenogenesis — Parthenogamy — False
hybrids — Gynogenesis — Androgenesis — Merogony — Parthenogenesis and
heteroploidy.

CHAPTER XXV

Cytoplasmic Heredity 414

Chlorophyll inheritance — Theories of chlorophyll inheritance — Mosses —
Other cases — Conclusions.

xiv CONTENTS

CHAPTER XXVI Page

Historical Sketch 422

Discovery of the cellular organization of plants and animals — Preformation
and epigenesis — Renewal of study of organic structure — Cell theory — Cell
multiplication — Protoplasm doctrine — Organismal theory — Syngamy and
embryogeny — Mitosis and meiosis — Cytology and heredity — The twentieth
century.

Bibliography 449

Index 533

INTRODUCTION TO CYTOLOGY

CHAPTER I

CELLS AND TISSUES

Every living organism, plant or animal, is a protoplasmic system
interacting with its environment. Although it is probable that the
protoplasm of every kind of living thing, even every individual, differs
physico-chemically from that of every other, it is nevertheless true that in
certain major features of its organization protoplasm tends to be strikingly
the same throughout almost the entire organic world. With the possible
exception of certain lowly types of life, protoplasm everywhere is differ-
entiated into two principal constituents, cytoplasm and nucleus. Fur-
thermore, in most plants and animals protoplasm is organized in the
form of cells, each cell consisting typically and essentially of a nucleus, a
mass of cytoplasm, and a limiting membrane.

Cytology derives its name from the cell: kvtos = hollow place (a cell).
"Cytology, the study of cells" is a convenient definition, but in certain
respects it is scarcely adequate. There are many tissues and many fairly
complex organisms which are really large masses of nucleated protoplasm
with actual cellular subdivisions partially or wholly absent, yet they
carry on the same vital activities and confront the biologist with nearly
all of the same fundamental problems as do the typically cellular forms.
Hence it seems better to say that cytology is that branch of biology which
deals directly with the structural and functional organization of proto-
plasm, usually in the form of cells, and with the relation of this organi-
zation to such phenomena as metabolism, ontogenetic differentiation,
heredity, and phylogeny.

Throughout most of its historical development cytology concerned
itself chiefly with the structural aspects of protoplasmic organization,
its principal tool being the microscope. Since the nature of light and
the structure of the human eye impose arbitrary limitations upon the
applicability of microscopical methods, structural cytology came to be
rather sharply set apart from the study of physiological function, in which
a different set of techniques had to be employed. The artificial character
of this distinction should be obvious. Every structure has its functional
meaning, while every physiological proce.ss involves a structural alteration
of some order in the protoplasmic system. Modern cytology is making

1

2 INTRODUCTION TO CYTOLOGY

increasing use of the methods and results of the physiologist, the physicist,
the chemist, the geneticist, and the taxonomist, as well as those of the
microscopist. The continued advance of this branch of biology will
depend largely upon the measure in which these various investigators
recognize the truly complementary nature of their tasks, and upon the
rigor with which their guiding theories are checked by sound observation.

Description of the Cell. — The term cell was introduced in the seven-
teenth century by Robert Hooke and other microscopists, who applied it
to the small cavities in the honeycomb-like structure which they dis-
covered in plant tissues. Today the term denotes primarily the proto-
plasmic "cell contents," to which, strangely enough, the early workers
attached little importance. The term protoplast, proposed by Hanstein
(1880), is more appropriate and has come into fairly general use, but
long usage and brevity have insured the permanence of the older term.
The structural features of ordinary cells will now be sketched in their
barest outlines by way of introduction to the detailed descriptions and
discussions to follow in subsequent chapters.

The three most constant constituents of the typical cell are the
cytoplasm, in which other cell organs and inclusions are imbedded, the
nucleus, bounded by its own membrane, and the plasma membrane differ-
entiated at the outer boundary of the cytoplasm.^ The cytoplasmic
portion of the cell may be referred to as the cytosome.

The nucleus consists of a ground mass of hyaline fluid known as
karyolymph ("nuclear sap"), an imbedded reticulum composed of kary-
otin, which is usually highly stainable, one or more true nucleoli, or
plasmosomes, and a limiting nuclear membrane. Frequently masses of
karyotin known as chromocenters are present at certain points in the
reticulum (see Figs. 23, 24, and 73, 30).

The cytoplasm, a more or less transparent, viscous fluid, may, with
its formed components and inclusions, occupy practically the entire
volume of the cell. This is generally true of animal cells. In most
plant cells a considerable amount of cell sap is present in one or more
vacuoles. Often it far exceeds the cytoplasm in volume, the cytoplasm
constituting a thin layer about it and lining the cell wall. In many cases
the cytoplasm forms a system of strands that often show active streaming.
Where it meets an enclosed vacuole it is limited by a vacuole membrane, or
tonoplast. Externally the cytoplasm is bounded by a specialized layer of
ultramicroscopic thinness, the plasma membrane. In some cells, for
example certain amcebse, a comparatively thick outer region known as the

1 According to an older usage only the extra-nuclear portion of the protoplast was
called "protoplasm," which was unfortunate because of the fact that the nucleus also
is composed of protoplasm, or living substance in the broader sense. It is now the
general custom to avoid this ambiguity by employing Strasburger's terms cytoplasm
and nucleoplasm (kanjoplasm, Flemming). The older usage has not, however, been
entirely superseded.

CELLS AND TISSUES 3

edoplast may be distinguished; in some cases the plasma membrane
appears to be the most superficial layer of the ectoplast (see Figs. 1, 48,
and 49).

In plant cells plastids of one or more types are nearly always present
in the cytoplasm. The most conspicuous among these are green chloro-
plasts, which are concerned in the fundamental process of carbohydrate
synthesis (see Figs. 25 to 29).

A characteristic constituent of animal cells is the Golgi material, which
may appear in the form of small bodies or more or less extensive networks

Fig. 1. — Living cells as they appear under dark-field illumination, a, cell from hair
of squash. The cytoplasm lines the cell and extends in strands through the vacuolar
matter; nucleus in lower center. (After Heidenhain, 1897.) b, cell from chick embryo
in tissue culture. The cell is adhering to the underside of a cover slip. Near the nucleus
are numerous fat globules; note also filamentous chondriosomes. (After Strangeways and
Canti, 1927.)

in the cytoplasm. It is therefore often called the "internal reticular
apparatus." It evidently plays a special role in secretion (see Figs. 35
and 37).

A centrosome is found in the majority of animal cells and in those of
certain lower plants. It is typically made up of a central granule, or
centriole, imbedded in a mass of hyaline or alveolar material known as the
centrosphere, but either of these elements may be present alone. During
stages of nuclear division the centrosome is surrounded by a conspicuous
system of radiating astral rays, collectively called the aster (see Figs. 85
and 86).

Chondriosomes have been demonstrated in the cytoplasm of nearly
all plant and animal, groups. These are minute bodies having the form

4 INTRODUCTION TO CYTOLOGY

of granules, rods, or threads and constitute a group of materials of uncer-
tain function (see Figs. 43 to 46).

Ergastic substances are accumulations of nutritive materials and other
products of metabolic activity. These non-protoplasmic substances,
which occur chiefly in the cytoplasm and vacuoles, may exist in the form
of visible granules, droplets, or crystals. Such substances may also occur
in the dissolved state.

The cell wall of plants, as at present understood, is usually regarded
not as a part of the cell proper, or protoplast, but rather as a secretion of
the latter. It is often absent, as in motile spores and gametes, which
have only delicate limiting membranes. The intercellular substance of
many animal tissues also bears a somewhat problematic relation to the
protoplast.

Even in such a brief description as this, one is struck by the general
similarity of plant and animal cells. This is obviously associated with
the fact that all organisms, be they plants or animals, must carry on
certain basic vital activities in common. Differences in cell structure
may be taken to indicate differences in the vital processes habitually
performed. The plastids, for instance, are to be viewed as structural
and functional modifications by the aid of which plants are able to
manufacture their own food out of simpler compounds derived from the
environment, an act which animals cannot accomplish. The prevalence
of large sap vacuoles in plant cells is also associated with peculiarities
in metabolism. The elaborate cell walls of plants furnish support for
large bodies, a problem which animals have solved in quite different
ways. These are probably the three most conspicuous structural differ-
ences between the cells of the two kingdoms. Other minor differences
will appear in subsequent chapters, but we shall continue to be impressed
by the remarkable cytological unity of both branches of the organic
world.

It is scarcely necessary to point out that the cell should not be thought
of as a static thing with a permanent physical structure. It is rather a
dynamic system in a constantly changing state of molecular flux, its
constitution at any given moment being dependent upon antecedent
states and upon environmental conditions. In the words of Harper
(1919), it is a colloidal system in w^hich the various processes have become
progressively localized in certain regions, with the resulting formation of
organs, which, with the increasing constancy of the processes involved,
have come to possess a permanence and individuality of their own. The
characteristic organization of the cell is a result of the differentiation of
protoplasm, and this organization is of such a nature that it plays in turn
an important part in determining the development of a higher degree of
differentiation. Its efficiency in this respect is indicated by its almost
universal occurrence in organisms of so many types.

CELLS AND TISSUES 5

Living and Fixed Cells. — The majority of cytological descriptions
have been based on material which has been prepared for observation by
complicated processes involving (1) fixation, whereby the cell structures
are rendered firm and capable of enduring the subsequent treatments
without undue distortion, (2) dehydration, (3) imbedding in paraffin, (4)
sectioning into thin slices, (5) staining with various dyes to bring out
contrasts, and (6) mounting in a medium, usually Canada balsam, having
a refractive index equal to that of the slide and cover-glass between which
the material is supported. Consequently cytologists have had to meet
the criticism that they are studying a series of artificial appearances
rather than the natural structures of cells. It is well known that the

#

C !>^:

Fig. 2. — Root-tip cells stained with iron alum-htematoxylin after fixation in various
aqueous solutions: o, ammonium and potassium bichromates, copper sulphate and pyridine;
b, chromic anhydride, butyric acid, and nickel hydroxide; c, formic acid, chromic anhydride^
and acetaldehyde; d, trichloracetic acid, formaldehyde, and nickel hydroxide, o, b, d
are from Zea; c from Allivm. Fluids with a pH below about 4.2 to 4.6 tend to give the " acid
fixation image" (c) desired in studies of chromosomes, while those with a higher pH tend
to give the "basic fixation image" (d) showing the chondriosomes. {Photographs con-
tributed by C. Zirkle.)

coagulative action of a fixing fluid may produce a visible structure not
previously present in the protoplasm, and that some fluids swell certain
cell components while others shrink them. Moreover, it is known that a
given fluid may preserve the nucleus well and the cytoplasm poorly, or
vice versa, and that the fixation images may differ characteristically
according to the pH and other chemical features of the fluids used (Fig.
2). 2 Hence careful cytologists are attempting to check their observations
on fixed and stained cells against living material as far as possible and are
constantly devising and refining methods for the study of untreated
protoplasm.

Nearly all of the cell components mentioned on the foregoing pages
may be observed to good advantage in living cells. For such study
various kinds of cells can be kept aUve for long periods if mounted in

2 See Yamaha (1926 et seq.) and Zirkle (1928a6, 1929a).

6 INTRODUCTION TO CYTOLOGY

Ringer's solution or paraffin oil, the streaming of the protoplasm often
continuing actively for hours or days. In the remarkable researches of
R. G. Harrison and others^ it has been shown that cells from various
tissues of vertebrate animals can be isolated and kept actively growing
and multiplying in culture dishes for a length of time often far exceeding
the normal life period of such tissues in the body. Under such conditions
the cells appear pale and colorless, but by careful adjustment of the
light the other components may be made to stand out with considerable
clearness. The cytoplasm usually appears as an optically homogeneous
fluid carrying various sorts of small inclusions which may show Brownian
movement if the viscosity of the cytoplasm is not too high. Chondrio-
somes appear as dull granules or threads somewhat difficult to make out
in many cells, while oil droplets stand out as highly refractive bodies.
Centrosomes and centrioles may often be seen, especially if identified by
surrounding astral rays. The nucleus may appear optically homogeneous
except for the nucleolus, which is usually seen without difficulty, or it
may present a finely mottled ("granular") appearance. In favorable
material the reticulate structure is evident. The cell sap of plant vac-
uoles appears as a clear space, with or without inclusions. When properly
illuminated in a dark field, many living cells are strikingly beautiful
objects, the chondriosomes and other small bodies appearing as glistening
specks in the pale protoplasm.

The visibility of certain components of living cells may be enhanced by
the use of dyes which enter the cell without killing it. Examples of such
"vital dyes" are neutral red and Janus green, which stain vacuoles and
chondriosomes respectively. The vital staining of the nucleus with
several dyes is also reported,^ but in several such cases it has been ques-
tioned whether or not the stained nuclei were actually uninjured and
wholly normal.

Particularly noteworthy are the results obtained by a number of
workers^ through the use of micromanipulative methods. Apparatus
and technique have been developed whereby it is possible to dissect,
inject, and otherwise operate upon living cells under very high powers of
the microscope. Many cells are highly tolerant of such treatment. A
microneedle may be pushed carefully into the cell and even into the
nucleus of a Tradescantia stamen hair without causing visible injury or
cessation of activity, but a lowering of the internal pressure due to escape
of material from the cell when the needle is withdrawn causes a series
of alterations from which the cell may later recover (Martens and Cham-
bers). In such ways it has been possible to learn much about the natural

' Carrel, Leo Loeb, Burrows, H. V. Wilson, W. H. and M. R. Lewis, Drew.
4 Kiister (19186, 1926), Gicklhorn (1927), Paltauf (1928), P. Dangeard (1923o).
« Kite (1913), Chambers (1914 et seq.), Seifriz (1918 et seq.), C. V. Taylor (1920
et seq.), Peterfi (1923), Martens and Chambers (1932).

CELLS AND TISSUES

physical and chemical states of protoplasm and its differentiations in
cells, as well as to correct many misconceptions due to inference from the
aspects presented by fixed material. Of great interest also is the recent
application of motion-picture photography to cytological problems.
Films taken slowly of cells in tissue cultures and then projected at high
speed have served to furnish information, especially with respect to time
relations, which it would be difficult or impossible to obtain by any other
means. Moreover, they have placed desirable emphasis on the concep-
tion of the cell as a dynamic system. As a consequence of the renewed
study of living cells, it has been possible to evaluate anew the results
obtained by the standard methods of fixation and staining and to improve
upon such procedures. Critical studies have been made upon cells

^tJ&s>#.

%

«r»-

^J

Fig. 3. — Spermatocytes of Stenobothrus (Chorthippus) lineatus: (1) living; (2) after
treatment with OsOi vapor and Flemming's fixing fluid; (3) after staining and mounting.
{After Belar, 19286.)

i

before, during, and after fixation and staining^ (Fig. 3) ; and as a result
it appears that, although the cytologist must be on his guard in inter-
preting the finer details even in his best fixed preparations, the general
picture presented in such material is on the whole strikingly true to
nature. Moreover, it is abundantly evident that no single set of methods
will suffice to solve all of cytology's problems.

Development. — In studying the development of any small, relatively
undifferentiated mass of nucleated protoplasm into a mature organism
and in interpreting the role of cells and tissues in this process, there are
certain general phenomena which may be considered before taking up the
more special data of cytology. These are growth, morphallaxis, differ-
entiation, and correlation.

By groxDth is meant primarily the synthesis of new protoplasm through
the activity of the old, and secondarily the increase in body size which
usually results. The synthetic processes involve an extensive interchange

« See Martens (19276c) and Belaf (1929a).

8

INTRODUCTION TO CYTOLOGY

of materials between nucleus and cytoplasm, so that a certain proportion
of nuclear and cytoplasmic substances (the " nucleoplasmic ratio") must
be maintained if these processes are to continue. The part which any
single spherical nucleus can play is strictly limited by the simple fact
that its surface, through which the interchanges occur, does not increase
at the same rate as does its volume during growth. The further growth
of the protoplasmic mass therefore requires a relative increase in the
nuclear surface. This is sometimes accomplished by a change in the
shape of the nucleus, but the almost universal method is by nuclear divi-
sion, whereby the nuclear surface is increased without a corresponding
change in volume. This permits further growth up to the point at which

the critical ratio is again reached,
whereupon the process is repeated.
The same principle is applicable
to the relation between the proto-
plasmic mass and its environment.
The size which a globular mass of
protoplasm can attain through an
increase in the actual amount of its
substance is limited by a critical ratio
between its volume and the amount
of surface through which interaction
with the external environment is
carried on. The maintenance of the
volume-surface ratio necessary to a
proper metabolic equilibrium in the
growing mass is secured in several
ways. The mass may simply divide
into two, thus increasing the surface
without immediate increase in vol-
ume, and incidentally multiplying
the number of individuals (Protozoa
and Protophyta). A second method is by change of shape. This is
well exemplified in coenocytic plants, such as Vaucheria (Fig. 4), Mucor,
and the myxomycetes, in which large masses of protoplasm expose an
extensive surface by assuming a flat, spreading form (myxomycetes) or
by developing filamentous branching bodies (coenocytic algae and
phycomycetes). At the same time the nucleoplasmic ratio is maintained
by repeated nuclear division, the numerous nuclei being either relatively
fixed in position (Caulerpa) or free to move about with the flowing
cytoplasm (Brijopsis, phycomycetes, myxomycetes).

The formation of partitions and the division of the nuclei show various
degrees of correlation in different organisms. The two processes may be
quite independent, in which case the compartments (cells) contain vary-

FiG. 4. — V, portion of ccenocytic body of
Vaucheria; nuclei dark and plastids in out-
line. C, portion of semi-ccenocytic body of
Cladophora.

CELLS AND TISSUES 9

ing numbers of nuclei (e.g., Cladophora; Fig. 4). In many cases, however,
they are so intimately related that they are like one process, and the
result is a regularly uninucleate condition of the cells. Here growth may
appear to be a matter of cell multiplication, but a consideration of proto-
plasmic masses not showing such a correlation between nuclear division
and cytoplasmic septation suggests that the regularly uninucleate cellular
condition is the result of a special refinement in mode of growth and
differentiation. The great importance of this refinement in connection
with the evolution of organisms is indicated by its prevalence. In certain
organisms the number and arrangement of the cells are constant in a
given organ or even in the whole body.^

By morphallaxis is meant the development of a particular form other-
wise than through synthesis or enlargement directly. The specific form
of the body is due in part to the fact that growth at certain periods is not
equal in all directions, but in addition to this the rearrangement of mate-
rials already present may play a prominent role. A striking illustration
of morphallaxis is afforded by small pieces of Hydra which under proper
conditions will, without further growth, remold themselves into complete,
though dwarfed, individuals.

As the young organism grows, it differentiates. Differentiation, in
the words of Conklin, is "transformation from a more general and
homogeneous to a more special and heterogeneous condition." It
involves the development of unlike functions and structures, and the
localization of these in different regions of the organism. Physiological
division of labor and morphological division of substance constitute one
inseparable process, and this process in its last analysis is the result of
physical and chemical changes in protoplasm caused by the combined
action of intrinsic and extrinsic factors. The next section will be devoted
to the subject of differentiation.

One of the most remarkable features of a living organism is the
perfect correlation which is normally maintained between the activities
of its many diverse organs; without such correlation development could
never occur at all. Differentiation and integration are, in fact, two
aspects of one thing, namely, organization (Conklin). It is to be empha-
sized that correlation is not something which comes into being as the
differentiation of functionally distinct regions occurs: the organism
behaves as a consistent, correlated whole from the beginning of its devel-
opment onward. The correlation existing between the activities of the
parts of the cell with which development begins gradually becomes the
more extensive correlation of the highly differentiated mature organism.
Correlation is retained from the first, although new means for its main-
tenance are elaborated. What these means are will be pointed out below.

^ See the review by Van Cleave (1932). For a review of the subject of cell form,
see Gray (1931).

10

INTRODUCTION TO CYTOLOGY

Mac.

Mic

Differentiation. — Differentiation occurs in uninucleate cells, multi-
nucleate Plasmodia, and multicellular masses. In the bodies of certain
Protozoa (Fig. 5) one sees within a single cell a very elaborate regional
differentiation in structure, certain functions being localized in definitely
constituted organs. There are distinct locomotor, digestive, and excre-
tory systems, as well as a "neuromotor apparatus"
which functions much as does the nervous system
of larger animals.^ These are probably the most
complex cells known. ^

Differentiation in multinucleate masses of proto-
plasm may be seen in the plasmodia of myxomy-
cetes, in the coenocytic algse and fungi, and in the
embryos of certain higher animals and plants. In
the myxomycete the protoplasm heaps up locally
and develops into a highly characteristic fruit body
with well-differentiated stalk, capsule wall, and sup-
porting capillitium filaments, but there is no sub-
division into cells until the spores are finally
delimited. In the coenocytic algae, such as Vaucheria
and Caulevpa, the body develops a definite form and
structure without cellular subdivisions. In Cau-
lerpa (Fig. 6) there are well-formed "roots,"
"stems," and "leaves," yet the whole vegetative
body is one continuous mass of cytoplasm with
thousands of nuclei scattered through it. The
nuclei may be relatively fixed in position, or they
may move about freely with the streaming cyto-
plasm. In a number of coenocytic plants, moreover, the spores and
gametes themselves are coenocytic ("coenogametes" of Mucor and
Albugo hliti; zoospores of Vaucheria).

8R. G. Sharp (1914), Yocum (1918), C. V. Taylor (1920), Rees (1921, 19226,
1931), McDonald (1922), Kofoid and Swezy (1922, 1923).

^ Certain writers, notably Dobell (1911a), hold that the protozoan body is "non-
cellular" rather than "unicellular," and restrict the term "cell" to the integral parts
into which a "multicellular" organism is subdivided. Whatever may be thought of
the practicability of this use of terms, its theoretical implications are worthy of
attention. Although agreeing with Dobell that the protozoan body and the ordinary
tissue cell are not homologous, we have chosen to use "cell" more loosely as a term
of convenience for both of them, as well as for other units for which morphological
equivalence is not claimed.

It is also frequently urged that "organelle" rather than "organ" should be used
for intracellular differentiations such as nuclei, plastids, and the neuromotor apparatus,
and that the latter term should be applied only to multicellular structures. We have
used "organ" in the more general sense in order to emphasize the fact that in all
cases the structures indicated are regional differentiations of protoplasm associated
with certain functions, to which the presence or absence of cell partitions is a sub-
ordinate feature. "Organelle" is, however, a useful term.

Fig. 5. — Diplodinium
ecaudatum. M, mouth;
A'', neuromotor appara-
tus; Mic, micronucleus;
Mac, macronucleus;
C.V., one of the con-
tractile vacuoles; A, anal
canal; C, contractile re-
gion; S, skeletal plates.
{After R.G. Sharp, 1914.)

CELLS AND TISSUES

11

The bodies of such organisms may be surprisingly elaborate, but the
degree of complexity which they attain is nevertheless limited. The
functional differentiation of regions in continuous large masses of proto-
plasm, which shows itself in visible structural differentiations, may be
considerable; but the degree of differentiation reached by the higher
classes of plants and animals seems to have been very largely conditioned
by the development of partitions between the various centers of activity

Fig. 6. — A, Caulerpa macrodisca, a ccenocytic plant,
showing supporting trabeculse.

B, section of leaf of Caulerpa prolifera,
iAfter Oltmanns.)

(nuclei) and functionally differentiating regions, the regions thus set
apart then becoming more fully specialized than would have been possible
in a continuous aqueous colloidal medium (see R. S. Lillie, 1923). The
protoplasmic body thus attains a multicellular organization.

Differentiation in multicellular masses is well exemplified in the
growing points of vascular plants (Fig. 7). In the stem tip and root tip
there are actively growing regions known as meristems, in which the cells
are in a relatively undifferentiated ''meristematic" or "embryonic"
condition.'" In mahy plants there is another extensive region of such

1" For an extensive account of meristems, see Schiiepp (1926).

12

INTRODUCTION TO CYTOLOGY

cells in the cambium. As a rule, meristematic cells contain no conspic-
uous ergastic inclusions aside from vacuoles and are separated by very
delicate walls with no intercellular spaces. As growth proceeds in such
tissues, every nuclear division is accompanied by a division of the cyto-
plasm; hence growth results in the multiplication of the uninucleate cells.
In regions farther from the point of greatest meristematic activity the
cells gradually become visibly diversified in structure in connection with

their increasing specialization in func-
tion. Throughout the active life of the
plant the homogeneous meristematic cell
mass thus continues to grow distally
and differentiate proximally into tissues
with very diverse histological characters
(see Eames and MacDaniels, 1925).

Fig. 7. — Longitudinal and transverse sections of apical meristem in root of Pteris,
showing triangular pyramidal apical cell. The segments cut from the distal face of the
cell go to form the root cap, while those from the three lateral faces develop into the tissues
of the root proper. In seed plants the meristematic activity does not center in a single
distinguishable cell. {After Hof, 1898.)

Most of the visible characters which ordinarily serve to distinguish
the various kinds of differentiated cells of the vascular plant are found
in the cell wall rather than in the protoplast itself. Thus, besides meri-
stematic and slightly modified parenchymatous cells, there are many
other types, such as tracheids, vessels, wood fibers, phloem fibers, and
sieve tubes (Fig. 8), all of which are characterized by the peculiar ways in
which their walls become modified through secondary and tertiary thick-
enings and by the form and arrangement assumed by the pits (see p. 175).
The protoplasts may finally disappear completely from wood cells,
leaving a tissue or framework composed of lifeless cell walls. All func-
tional differences are accompanied by chemical or physical differences of
some sort in the protoplasm, but it is mainly in the non-protoplasmic

CELLS AND TISSUES

13

elements (including the wall) rather than in any conspicuous structural
changes in the protoplasm itself that cell differentiation is rendered
visible in the case of plants. Apart "from differences in shape, amount of
vacuolar material, accumulated food, and other products of differentia-
tion, protoplasts performing widely different functions may appear much
alike.

Structural differentiation in connection with division of labor is very
striking in the protoplasm of animal cells," which are destitute of such
■walls as plant cells possess. The muscle cell shows fine longitudinal

((if

VMS'
V

1 )

J

i

B

Fig. 8. — Differentiated cells from vascular plants. A, wood fiber with thickened wall.
B, C, portions of tracheids with spiral and annular thickenings. D, pitted tracheid.
E, portion of sieve tube with adjacent companion cells. F, face view of sieve plate shown
in section in E.

fibrils, which are in some way concerned with the cell's power of contrac-
tility. In certain muscles these fibrils show transverse membranes
at regular intervals, and these so correspond in adjacent fibrils that the
muscle has a transversely striped appearance.

The nerve cell (Fig. 9) typically possesses a single unbranched pro-
longation (axon) and one or more others (dendrites) which often become
very elaborately branched, especially in the ganglion cells of the spinal
cord and brain. In fixed preparations the cytoplasm of the nerve cell
contains fine "neurofibrils"^^ and also granules of chromatic "Nissl
substance."

^1 For detailed descriptions of the cytological features of animal cells of many
types, see Special Cytology, ed. by Cowdry (1932); see also Heidenhain (1907, 1911).

12 It has been reported that in healthy living cells the neurofibrils cannot be
detected and probably represent coagulation artifacts (Matsumoto, 1920; Lewis and
Lewis, 1924; de Mouhn, 1923), but other investigators (Cowdry, 1914, 1928; Bozler,
1927; Boeke, 1926; Parker, 1929a6) are convinced that they correspond to real
differentiations in the cell.

14

INTRODUCTION TO CYTOLOGY

Cells specialized in connection with motility, such as spermatozoa
and the cells of certain epithelial tissues, show complex structural modi-
fications not only in the flagella, cilia, and cirri which they bear but
also in the other cell organs with which the activities of these motile
structures are closely connected (Figs. 134, 136, 137). Secretory cells
are often distinguishable by the accumulations of secretion products in
their cytoplasm, or by the peculiar form assumed by their nuclei (Fig. 22).

In connective tissues (Fig. 10) the protoplasm is subdivided into cells
with various degrees of distinctness depending on the relative amount
of supporting substance they produce during their differentiation.

. "^^^3r%:^

E

mmm

p piiiiliiii

Fig. 9. — Nerve and muscle cells of animals. A, diagram of a typical neuron: a, axis
cylinder process, or axon, ending in arborescent system; d, dendrites. B, cell from human
spinal cord. {A and B after Obersteiner and Hill.) C, nerve cell from eye. {After Len-
hossek.) D, nerve cell from earthworm. {After Kowalski.) E, young voluntary muscle
cell. F, portion of mature voluntary muscle cell, showing striations. G, involuntary
muscle cell from intestine. {E-G after Piersol.)

Cartilage and bone cells are likewise imbedded in such substances, which
are here produced in relatively enormous amounts and later form the main
supporting framework of the body. Blood, which is sometimes spoken of
as a "fluid tissue," consists of a plasma carrying cells of a variety of
types.

Differentiation in a multicellular mass involves the gradual setting
apart of special regions with modified structural and functional charac-
ters as in the body of a protozoon, but with the important difference that
these regions include many cells, each of which retains in some degree the
fundamental type of protoplasmic organization (nucleus, cytoplasm,
semipermeable membranes) possessed by the cell which began the
development of the differentiating mass. One therefore expects a greater
capacity for independent action in these cellular components of the body
than in the subcellular components of the protozoan body. This expec-

CELLS AND TISSUES

15

tation is fulfilled in the results of experiments which have shown that
many tissues and cells of higher organisms may, if given structural
independence and a proper environment, continue to live or even in
many cases to grow into a complete new body. The ability of such an

/ E

Fig. 10. — A, reticular connective tissue from lymph gland of cat. {After Heidenhain.)
B, young heart muscle of dog embryo, showing myofibrils developing, but no subdivision
into cells. C, later stage of same. {B and C after Godlewski.) D, development of cells in
Plasmodium by vacuole formation in human embryonic epithelium. {After M archand.)
E, development of cartilage tissue from Plasmodium in Lophius. {After Studnicka.)

isolated part to reconstitute a whole depends upon the measure in which
it has retained what is fundamental in the physico-chemical constitution
of protoplasts through the period of its differentiation.

Correlation. — No such degree of differentiation and specialization
of tissues as we see in organisms could be attained, and no such complex
mechanism could continue to act as a unit or individual, were it not for

16 INTRODUCTION TO CYTOLOGY

adequate means of keeping the activities of the various parts fully
coordinated. Among the means by which this correlation of the parts
is maintained, we may consider protoplasmic continuity, the differentia-
tion of specialized tracts, hormones, and physiological gradients.

The delicate intercellular strands in the tissues of multicellular plants
have been described in a large number of papers. ^^ Two general types
of connection are usually distinguished. In the red algse and certain
other thallophytes adjacent cells are connected at one relatively large
region where membrane materials are deposited. The question of actual
protoplasmic continuity through this region is at present a debated one
(Jungers, 1933). Large protoplasmic strands are found between the egg
and surrounding cells in cycads and in certain other tissues, but these
seem to be due either to the enlargement of smaller pores present at an
early stage or to actual solution of the intervening wall. Strands of the
second general type, which are known as plasmodesms (Fig. 11), are of
exceedingly small diameter, special methods being required for their
demonstration. They may be distributed rather uniformly over the wall,
or they may be aggregated in small groups, which are often located in
pits or thin spots; frequently they are branched.

Very little is accurately known regarding the origin and development
of plasmodesms. It can scarcely be doubted that the pores through
which they pass are often present from the time the cell partitions are
first formed, no wall substance being deposited at these points. There
is also considerable evidence in support of the view that plasmodesms
are secondarily developed structures. Strasburger (1901) stated that
extensions from adjacent cells come into contact as the intervening wall
begins to thicken but do not form continuous strands. The fact that
in separating cells the break occurs through the thickened median portion
of the strands lends support to this view (Hume, 1913). That the
strands are actually continuous was emphasized by Meyer (1896 et seq.),
who held that they are due both to retention and to new formation. He
observed a secondary formation of connections in Volvox and in fungus
hypha? which came in contact.

Light on this question has been sought in parasites and graft hybrids,
where cells of different species come together. Kienitz-Gerloff, Kuhla,

1^ Among these may be mentioned the works of Wille (1883) and Borzi (1886)
on the Cyanophycese; Kohl (1891), E. Overton (1889), and Meyer (1896) on the
Chlorophyceae; Hick (1885) and Doubt (1928) on the Fucacese; Hick (1883), Massee
(1884), Rosenvinge (1888), and Mangenot (1926) on Florideje; Kohl (1897) on mosses;
and, on vascuhir plants, those of Tangl (1879), Russow (1882), Strasburger (1882,
1901a), Goroschankin (1883), Terletski (1884), Wortmann (1887, 1889), Haberlandt
(1890), Kienitz-Gerloff (1891), Jonsson (1892), Kuhla (1900), Poirault (1893),
Gardiner (1884, 1897, 1900), Hill (1900, 1901), Gardiner and Hill (1901), Kohl
(1900, 1902), and Quisumbing (1925). For general accounts of protoplasmic connec-
tions, see Davis (1905a), Meyer (1920), Lundeg&rdh (1922), and Jungers (1930).

CELLS AND TISSUES

17

and Strasburger found no plasmodesms between the cells of Viscnm and
Cuscuta and their hosts, but in the case of graft hybrids both Buder (1911)
and Hume (1913) report their presence in the walls separating cells which
are supposed to be genetically unrelated. This seems to show that con-
nections may arise secondarily, although uncertainty regarding the exact
behavior of the protoplasts in the wounded region leaves an element of
doubt. They arise secondarily in the abutting walls of tyloses, according
to Molisch (1888).

At present the probabilities are in favor of the view that intercellular
strands are both primary and secondary in origin, some of them repre-
senting regions in w^hich the continuity of the protoplasm has never been
broken and others being subsequently developed through the intervening

Fig. 11. — Endosperm of
Diospyros, showing plasmo-
desms traversing the thick-
ened cell walls. {After Qui-
sumbing, 1925.)

" W ,

fl)

%

■in^

■mk

:-C?

:>: V ■

.-::;.)

6r- „ __ „ _ -

Fig. 12. — Protoplasmic con-
tinuity in human mesoderm
tissue. (After Maurer.)

0-j ,

afsc^

cell membranes. The very fact that a given area of cell wall becomes
enormously extended during the growth of the tissues indicates that
many of the pores seen at maturity must have been formed anew. It
is also to be remembered that at the time when pore formation would
necessarily occur the cell membranes are very thin and semifluid and
would offer little resistance to dissolution or penetration by the proto-
plasts. Hence the fact that cells may glide or roll over one another
during the early stages of development does not prove the impossibility
of protoplasmic continuity between them. The exceeding fineness of
many known plasmodesms, moreover, indicates that failure to find such
connections in certain tissues does not necessarily prove their absence.
On the other hand, proof that plasmodesms are continuous through the
entire wall is not so complete as desired. Jungers (1930) has recently
called into question the evidence for the view that plasmodesms in

18 INTRODUCTION TO CYTOLOGY

endosperm, sieve tubes, and thickened parenchyma are actually proto-
plasmic in nature. Their resistance to potassium hypochlorite and their
arrangement in growing walls suggest to him that they are rather struc-
tural constituents of the wall itself.

Protoplasmic connections have been rather widely described in
animals, and are best known in epithelial, muscle, and connective tissues
(Fig. 12). In connective tissue they may be broad cytoplasmic exten-
sions, giving the tissue the character of a protoplasmic network (Fig. 10),
or they may be very fine threads. As in plants, they are the result
either of an incomplete division or of a fusion of cell outgrowths. The
fact that cells in animals are mostly divided by a process of furrowing
indicates that connections, if present, must be for the most part second-
arily developed. In his study of living tissues Chambers (1924) finds
in the majority of cases no direct evidence of protoplasmic bridges and
is inclined to agree with certain other workers in interpreting many
reported connections as either fixation artifacts or fibrous differentiations
in the intercellular substance, rather than actual protoplasmic strands.
Such strands are clearly present, however, in squamous epithelium
(Chambers and Renyi, 1925). Some investigators, as will be pointed
out in a subsequent chapter, regard the intercellular substance itself
as living matter of a special kind. The establishment of protoplasmic
connections between blastomeres has been described. ^^

The chief significance of protoplasmic connections of all types prob-
ably lies in their coordinating function. That plasmodesms serve to
transmit stimuli from one cell to another is indicated by their presence
in tissues of plant parts known to be particularly responsive to external
stimuli. 1^ The effects of mechanical injury appear to be transmitted
through epithelial tissue by way of such intercellular bridges according
to Chambers and Renyi (1925). Their extensive development in storage
tissues, such as the endosperm of seeds (Tangl, 1879; Gardiner, 1897),
also suggests that they are in part responsible for the readiness with
which nutritive materials are translocated in such specialized tissues.

The protoplasm of the entire individual is more or less continuous
from the beginning of the ontogeny onward. It should not be thought,
however, that without such connections there can be no correlation.
Mere contact is sufficient for the passage of electrical stimuli, which,
as will be indicated below, are recognized as important factors in the
development and operation of the body. Cells separated by delicate
colloidal membranes with no actual protoplasmic continuity are still
able to interact and influence each other's behavior so that the entire

" G. F. Andrews (1897), E. A. Andrews (1898), Shearer (1906), Whong (1931).

'* The leaves of Mimosa (Gardiner, 1884) and Dionoea (Gardiner, 1884; Macfarlane,
1892); the stamens of Berheris (Gardiner, 1884); the sensitive labellum of the orchid
Masdevallia muscosa (Ohver, 1888).

CELLS AND TISSUES 19

group tends to act as a unit. Thus without protoplasmic continuity
the cells may still have a physiological continuity; it is the possession
of both that conditions the coordinated action of most tissues. In
any case the field of force which pervades the whole organism and which
shapes its development is not interrupted by cell partitions (Thompson,
1917).

The differentiation of specialized tracts with a correlating function
is exemplified not only in the nervous system of higher animals but also
in the neuromotor apparatus of certain Protozoa. It has been found
that after the delicate strands leading to the several groups of locomotor
organelles in Euplotes are cut, the action of the groups is no longer
properly coordinated (C. V. Taylor, 1920, 1929). It has been contended
that the vascular bundle regions of higher plants serve to conduct
correlating stimuli, but the evidence for this is as yet inconclusive.

In the vertebrates correlation is maintained in part through the agency
of hormones. These are chemical substances which are elaborated in the
endocrine glands and carried by the blood or lymph to the various parts of
the body, where they exercise profound effects upon growth and other
activities of the organs and tissues. The discovery of these endocrine
secretions and the application of knowledge concerning them to the treat-
ment of certain human disorders constitute one of the most significant
developments in modern medical biology. ^^ The question of the possible
role of hormones in plants is still a disputed one, although Went (1931)
and others have adduced evidence indicating the presence of one, called
"auxin," in growing points, while Haberlandt (1921 et seq.) attributes
the healing of wounds to a hormone.

One of the most important contributions to our understanding of
correlation is the conception of physiological gradients developed by
Child (1911 et seq.) and his associates. It has been shown in a number
of animals and plants that along each of the axes of symmetry there
exists a physiological gradient (also called "metabolic gradient" and
"axial gradient"), the rate of the physiological processes being highest
at one end of the axis and diminishing progressively toward the other
end. The anterior end of a planarian, for example, exceeds the posterior
end in its rate of oxygen consumption and carbon dioxide output and
in its susceptibility to poisons. Furthermore, the portions having a
higher rate exercise a "dominating" influence over the development of
those portions having a lower rate, with the result that the individual
maintains a definite physiological correlation of anterior and posterior
parts. Similarly in individuals with more than one axis of symmetry
there may be a corresponding dorsal-ventral, as well as an axial-marginal,
correlation. The gradient arises in the first place, according to Child,
as a response to differential factors in the environment; and, although

^^ For a convenient account of hormones and their effects, see Guyer (1931).

20 INTRODUCTION TO CYTOLOGY

the types of organs developed depend upon the hereditary constitution
of the organism, their arrangement and mutual behavior are due in large
measure to the gradient. This is indicated by the fact that experimental
alterations in the metabolic rate along the axis are followed by the
expected abnormalities in structural development.

As to the means by which different regions along an axis influence one
another, Child (1915, p. 224) adduces evidence in support of the theory
that the fundamental relations of polarity "depend primarily upon
impulses or changes of some sort transmitted from the dominant region,
rather than upon the transportation of chemical substances." Very
significant in this connection is the fact that there is a definite relation
between physiological gradients and electrical polarity. The dominant
and less active regions are respectively the negative and positive poles
of the living system. Where the current enters the system from the
exterior (negative pole), anabolic processes are promoted through
increased oxidation; and where it leaves (positive pole), catabolic proc-
esses are furthered." Alterations in electrical polarity are accompanied
by alterations in the mode of growth. ^^ Thus, in the opinion of Lillie
(1923), "bioelectric currents exert a controlling and coordinating influence
in normal growth processes as well as in normal stimulation."

The Cell Theory and the Organismal Theory. — Although not of the
first importance to the student beginning work in cytology, the following
discussion is added because of its theoretical interest.

The fact that the body of a higher organism comprises a vast number
of specialized parts, the cells, led many years ago to the formulation of
two general theories which differed in their interpretation of the relation
existing between the two individualities : the organism as a whole and the
cell. These theories are known as the cell theory and the organismal
theory.

The cell theory set forth a century ago by Dutrochet, Schleiden, and
Schwann exerted a dominating influence upon biology throughout the
nineteenth century (see Chapter XXVI). The principal propositions
involved in the theory are summarized by Heidenhain (1907, p. 29)
essentially as follows: All living substance is concentrated in cells; the
cells of the body are all individuals of the same morphological rank;
the tissue cell is morphologically and physiologically an elementary
individual, the unit of structure and function; the body is an aggregate
of cells, which are its "building stones"; the action of the body is the sum
of the many special actions performed by collaborating cells of many
kinds. According to this theory, therefore, the cell is the fundamentally
important individual — the "primary agent of organization." In
ontogeny the multiplying elementary organisms, or cells, cooperate to

17 Hering (1888), Mathews (1903), R. S. Lillie (1919, 1922, 1923).

18 Bose (1918), Ingvar (1920), Lund (1921). See also Beutner (1933).

CELLS AND TISSUES 21

build up an individual of a higher order, the multicellular organism.
Such an organism is thus a "cell state," or "cell republic," secondarily-
formed by the aggregation of a vast number of elementary individuals.

The phylogenetic aspect of the cell theory developed when it was
discovered that many minute organisms are single uninucleated masses
of protoplasm much like the constituent cells of the multicellular forms.
It was concluded that such "unicellular elementary organisms" have
in the course of time formed loose colonies, either by direct aggregation
or by an acquired failure to separate after a period of multiplication;
and that the individual units have become increasingly interdependent
and knit together until individuals of a higher grade, multicellular
organisms, have resulted. As a consequence of this interpretation,
the individual protozoon has been homologized with a single cell of the
human body. The dominance of the cell theory, moreover, has resulted
in the tendency to describe everything of a biological nature so far as
possible in terms of cells.

It has always been very difficult to make any plausible interpretation
of plasmodial or coenocytic organisms in terms of the cell theory. Such
organisms are multinucleate and non-septate masses of protoplasm,
which nevertheless build up bodies of definite form and with a consider-
able degree of differentiation. The nuclei are centers of action whose
reactions influence the cytoplasm to different distances, especially in
those forms in which their position is being constantly changed by
protoplasmic streaming. Some have taken the standpoint that in such
coenocytic bodies each nucleus with the portion of the cytoplasm it
influences "represents" a cell, while others hold that the entire multi-
nucleate body is one huge cell. Both of these interpretations contain
elements of truth, but they also appear like attempts to save a theory
based on a limited group of observations.

The early dissatisfaction with the conception of the cell as the primary
and universal agent of organization led to the formulation of the organ-
ismal theory, in which the emphasis was placed on the living mass as a
whole rather than on the constituent cells. ^^ According to this general
interpretation, ontogenesis is a function primarily of the organism as a
whole and consists in the growth and progressive internal differentiation
of a single protoplasmic individual, this differentiation often, but not
always, involving the septation of the living mass into subordinate
semiindependent parts, the cells. Since the septation is rarely complete,
all parts remain in connection and the whole continues to act as a unit.
Hence development is not primarily the establishment of an association
of multiplying elementary units to form a new whole but rather the

1' For a list of biologists who developed and supported this theory, see p. 436.
See also Whitman (1893), Sedgwick (1894), Dobell (1911a), Ritter (1919\ Ritter
and Bailey (1928), and Russell (1930).

22 INTRODUCTION TO CYTOLOGY

resolution of one persistent whole into newly formed metabolic units:
it should be thought of not as primarily a multiplication and cooperation
of cells but rather as the differentiation of growing protoplasm.

The real unity is that of the entire organism and, as long as its cells remain in
continuity, they are to be regarded not as morphological individuals but as
specialized centers of action into which the living body resolves itself and by
means of which the physiological division of labor is effected (Wilson, 1893).

The phylogenetic implication of the organismal theory is that if
multicellular organisms have arisen from unicellular forms, the process
may have been the same as that seen in ontogeny: the differentiation
and subdivision of a continuous growing mass of nucleated protoplasm
into a system of uninucleate cells. If the septation coincided with
nuclear division from the first, there was a direct transition to forms with
several cells. If the two processes did not so coincide, ccenocytic or
"plasmodial" types arose, some of which persisted as our ccenocytic
organisms while others developed internal walls and became our multi-
cellular forms. The ability of isolated tissue cells to live independently
does not prove that independent cells have combined to form the multi-
cellular body but only that such parts can still carry on essential proto-
plasmic functions. The phenomenon could as well be taken to prove the
derived nature of Protista. The body is not an aggregation of elementary
organisms, but a single organism which has evolved a multicellular structure.
The cell colonies in certain green algae-" and the remarkable polyp colonies
in the Siphonophora (see J. S. Huxley, 1912) indicate the dependence of
the part upon the whole even in a group formed by aggregation, and they
show the possibility of an evolution by the combination of individuals;
but it is not at all clear that they afford the key to the evolution of organ-
isms in general. The protozoon is more properly compared with the whole
man ; both are organisms which have differentiated a series of specialized
internal regions or organs, the one without cellular subdivision or increase
in size and the other with them.

Some of the cytological facts underlying the organismal theory may be
briefly cited as follows.

Many algse and other organisms, as already noted, develop bodies of
considerable size and with definitely differentiated form and structure
without any cellular subdivision of the multinucleate protoplasm. In
some of these {e.g., Bryopsis; Noll, 1903) the tips of the plant grow steadily
forward as wholes, in spite of the fact that the cytoplasm and the nuclei
it carries are constantly being changed by protoplasmic streaming.
Interpreting the entire plant as a huge cell accomplishing the development
is here equivalent to admission that it is the whole which dominates the
"centers of activity" about the nuclei.

2" Bock (1926) describes plasmodesms in Pandorina, Eudorina, and Gonium.

CELLS AND TISSUES 23

The same general result may be achieved with or without cell-forma-
tion, as in the bodies of Vaucheria, Cladophora, and Stigeoclonium, which
show essentially the same degree of elaboration although the first is
ccenocytic, the second semicoenocytic, and the third strictly cellular.
Eggs of Chcelopterus have been observed to differentiate into swimming
larvae even when the usual cytoplasmic cleavages are suppressed by add-
ing some KCl to the sea water (F. R. Lillie, 1902, 1906). It has been
shown in a number of cases that alterations in the position of successive
cleavage furrows do not disturb the normal course of development and
differentiation. In the frog, for example, "normal development does not
depend upon a specific number and succession of cleavages in definite
positions but rather upon an egg pattern which may be cut up by the
cleavage furrows in various ways without destroying the pattern or the
normal results of development" (Conklin, 1924). Spemann (1918 et
seq.) has shown that in very young amphibian embryos groups of cells can
be cut out and reversed in position or transplanted into other regions,
whereupon they develop as parts of the organs normally differentiating in
those regions and not as those of the regions from which they came.
Thus, as F. R. Lillie (1902) concluded for Chcetopterus, "the process of
cell-division, as such, is necessary neither to growth, differentiation, nor
the earliest correlations; but it is accessory, in Metazoa, to all three as a
localizing factor, often from the earliest stages. "

It was to the same conclusion that W. Hofmeister, Sachs, de Bary, and
other botanists were led many years ago through detailed studies of cell-
formation in the growing regions of plants. They found the growth of the
organ as a whole to be the primary matter, the position of the cell walls
within it being secondarily determined by the physical forces acting within
the growing mass. "The formation of new cells in the vegetative point is
accordingly a function of the general growth, not its cause" (Hofmeister,
1867). This view has been upheld by many researches on the mechanics
of growth and form (see Thompson, 1917) and by the recent studies of
Sinnott (1930) on the relation of the dimensions of cells to the size and
form of the organ they constitute.

Many organisms which are cellular throughout the greater portion of
the life cycle pass through a ccenocytic phase, often at a critical stage in
the cycle, and in this phase as elsewhere growth and differentiation con-
tinue. In the young embryos of Agathis (Fig. 13) and other gymnosperms
the characteristic mode of development is indicated by the positions
taken up by the nuclei during the ccenocytic stage, the position of the
subsequently formed cell partitions being determined by differentiations
occurring in this stage. Similarly, there are among animals cases in
which the embryo first passes through a free-nucleate stage, subdivision
into cells occurring after differentiation, particularly that of the germ
region, is well on its way. That differentiation in such cases is a function
of the protoplasmic mass as a whole is indicated by the fact that any

24

INTRODUCTION TO CYTOLOGY

nuclei which happen to enter the germinal region become germinal nuclei,
the rest becoming somatic nuclei (Huettner, 1923; on Drosophila). In
many such eggs the cleavage is at first only superficial, the walls forming
without special reference to the nuclei or their division, and the resulting
compartments remaining for a time open into the common underlying
mass of protoplasm. Many of the special tissues of the animal body may
begin their development as plasmodial masses in which cellular differentia-
tion occurs later. In some tissues the non-cellular condition may remain
until maturity, as in certain "syncytial" types of connective tissue. The
internal structures characterizing many tissue cells, such as neurofibrils
and elastic fibrils, may arise before the subdivision into cells (see Rohde,
1908, 1923).

D

Fig. 13. — Early stages in the embryogeny of Agathis australis. A, ccenocytic stage.
B, 32-nucleate stage with cytoplasmic suspensor cap differentiated. C, proembryo sub-
divided into cells. Three regions distinguishable: suspensor initials above, embryo
proper in middle, and embryonic cap below. D, later stage; cap well developed and
suspensor elongating. {After Eames, 1913.)

All of this is not to be interpreted as a denial of the importance of
cells in multicellar organisms but only as a recognition of the fact that the
principle of functional protoplasmic differentiation is more general and
fundamental than that of cells as units (Heidenhain, 1907). Although
we thus look upon cellular organization as initially a result of differentia-
tion, it is true that it has, in turn, conditioned differentiation of a higher
degree. The presence of cell partitions allows a more effective segregation
of functionally specialized regions and a fuller play to those important
physico-chemical processes which depend on surfaces and thin films for
their action. Furthermore, it permits the development of larger plant
bodies by furnishing an ideal basis for the more effective operation of
turgor and for the deposition of supporting materials. The evolution of
higher organisms has unquestionably been very largely conditioned by the
multicellular state, but we should think of such organisms primarily as
highly differentiated protoplasmic individuals rather than cell republics.

CHAPTER II

PROTOPLASM

In spite of the enormous amount of work which has been done upon
protoplasm during a period of many years, our knowledge of its constitu-
tion and behavior must still be regarded as very superficial. Some have
inclined to the view that a given kind of protoplasm is a single complex
chemical compound, but at present it seems more probable that it
represents a somewhat looser combination of substances, many of which
are themselves very elaborate in composition. It furthermore seems
probable that these substances differ from those which may exist apart
from protoplasm, not so much in their fundamental chemical nature
as in the degree of their complexity, their energy content or reactivity
(Mathews, 1924), and especially in their mutual organization. Proto-
plasm is made up of proteins, fats, salts, water, carbohydrates, and other
compounds, but it is not a mere mixture of these materials: it is an intri-
cately organized system of substances of many types, and only by virtue of
this specific physico-chemical organization does it serve as the material
substratum for those peculiar orderly activities characterizing the
organism, namely, synthetic metabolism, irritability, reproduction,
and adaptive response. Living protoplasm should always be thought of
as a system in dynamic equilibrium; it is continuously maintaining itself
through a balance of constructive and destructive processes. The "abil-
ity to transform environmental material into its own specifically organized
and active substance is the distinctive criterion of living as distinguished
from non-living matter" (R. S. Lillie, 1923).

The Chemical Nature of Protoplasm.^ — The operation of any system,
living or lifeless, depends upon the materials of which it is made up (its
chemical composition), the arrangement of these materials (its physical
organization), and the set of surrounding conditions under which it acts
(its environment).

The chemical composition of protoplasm has been determined
approximately in a number of instances. For this purpose the plasmodia

1 See on this subject A. Zimmermann (1896), Hammarsten (1909), Zacharias
(1910), Czapek (1913, 1920), Wells (1914), Bayliss (1915), Mathews (1916, 1924),
Palladin (1923), Meyer (1920), T. B. Robertson (1920), B. Moore (1921), R. W.
Thatcher (1921), Walter (1921), Pratje (1920), Tischler (1921-1922, Chap. II),
Lundeg&rdh (1922, Pt. I, Chap. XI, B), Grafe (1922, Chap. IV), Onslow (1923),
Trier (1924), Heilbrunn (1928), Gortner (1929), and Kiesel (1930).

25

26 INTRODUCTION TO CYTOLOGY

of myxomycetes^ and the spermatozoa of fish have been most frequently
employed, the former because of the large mass of protoplasm readily
available, and the latter because they yield large amounts of nuclear
material in a fairly pure state. By the use of stains Unna and others
have been able to determine the position in the cell occupied by certain
organic constituents. Microchemical methods have been employed
to some extent in the study of the inorganic constituents, but they are in
need of further development. The results of Kiesel's analysis of the
myxomycete Reticularia lyco'perdon are as follows:

Per Cent Per Cent

Dry Weight Dry Weight

Proteins 29.07 Lecithin 4.67

Oil 17.85 Cholesterol 0.58

Glycogen 15 . 24 Nitrogen extractives 12

Other non-reducing soluble carbo- Nucleic acid 3 . 68

hydrates 5 . 32 Lecithoproteins 1.2

Reducing carbohydrates 2 . 74 Unknown 5 . 87

Polysaccharides 1 . 78

The protein matter of protoplasm exists in relatively complex forms.
"The chief mass of the protein substances of the cells does not consist of
proteids in the ordinary sense, but consists of more complex phosphorized
bodies. ..." (Hammarsten). Such "phosphorized bodies" are the
nucleo-proteins, which are "probably the most important constituents of
the cell, both in quantity and in relation to cell activity" (Wells). A long
series of chemical investigations^ has shown that these nucleo-proteins
are essentially combinations of nucleic acid with proteins.

The nucleus, as a rule, contains little or no uncombined carbohydrate,
fat, or salt, but is characterized rather by the abundance of a substance
called "nuclein, " isolated in 1871 by Miescher, who gave it the formula
C22H49N9P3022. It was shown by Altmann (1889) that nuclein, like
other nucleo-proteins, is a combination of two substances: nucleic acid
and a simpler form of protein, the two existing in chemical combination
much like an ordinary salt. Nucleic acid, which is, in turn, a com-
bination of phosphoric acid with certain carbohydrates and bases, seems
to be very much the same in all types of protoplasm. It is well known in
two general forms, differing chiefly in the carbohydrate constituent of the
molecule; in one form this is a pentose and in the other a hexose. The
former is known to occur in yeast, wheat, and certain animals,
while the latter has been found in thymus and lymph glands, blood cor-
puscles, and spermatozoa. The strong afl^inity of nucleic acid for organic
bases is responsible for the staining reactions of the chromatic nuclear
substance: a fixed and stained chromosome is a salt of nucleic acid with a

2 Reinke and Rodewald (1881) and Lepeschkin (1923) on Fuligo varians (J<Jlhalium
septicum); Kiesel (1925. 1927) on Reticularia and Lycogala.

^ By Miescher, Hoppe-Seyler, Reinke, Kossel, Lilienfeld, and later workers.

PROTOPLASM 27

basic dye. The basic constituent of this substance in a Hving nucleus
may be a very complex protein, a simpler and more basic histon (blood,
thymus, echinoderm sperm), or a still simpler and more strongly basic
protamine (fish sperm). The following scheme will help to make clear
the relationships of these substances:

Phosphoric acid

Nucleic acid
Nucleo-proteins
"Nuclein"
"Chromatin"

Pentoses or hexoses
Purin bases
Pyrimidins
Etc.
Protein base: protamine, histon, or other protein

In the cytoplasm, in contrast to the nucleus, the proportion of protein
constituents is relatively high. The cytoplasm normally has no
"nuclein, " but it is rich in nucleo-albumins, albumins, globulins, and
peptones; these, unlike nuclein, contain little or no phosphorus. Accord-
ing to Hammarsten, "the globulins and albumins are to be considered as
nutritive materials for the cell or as destructive products in the chemical
transformation of the protoplasm." Volutin, a compound which resists
strong acids and shows an affinity for basic dyes,^ is frequently present
in the form of globules in the cytoplasm, notably in lower organisms.
It is usually regarded as a reserve substance. The importance of proteins
in protoplasmic activity is partly due to their amphoteric properties;
they may act either as acids or as bases under proper conditions. In
general, most of them act during life as acids.

The fatty constituents of protoplasm comprise the true fats and a
number of more complex derivatives containing nitrogen and phosphorus,
such as the phospholipides (phosphatides). Among the fatty substances
which appear to have a peculiar importance in the organism are choles-
terol, ergosterol, and lecithin. Under the influence of certain light rays
ergosterol may be transformed into vitamin D.^ The staining reactions
of fixed cytoplasm apparently depend not only upon its chemical com-
position, but also upon the degree of physical dispersion induced by the
reagents used (see Yamaha, 1932).

The carbohydrates found in protoplasm are chiefly pentoses (plants)
and hexoses (animals), which are, as a rule, combined with proteins and
with lipides. Glycogen exists free in many tissues and serves as a source
of energy. The important role played by pentoses and pentosans in the
activity of the plant cell has been strongly emphasized; in fact, proto-
plasm has been called "an intermeshed pentosan-protein colloid.""

^Reichenow (1909), van Herwerden (1917), Doflein (1918).
^ See Gortner (1929, Chaps. XXXI-XXXII, XXXV).
«Spoehr (1917, 1919), MacDougal (1920).

28 INTRODUCTION TO CYTOLOGY

Inorganic salts are present in considerable variety, as shown by the
presence of the following elements in the ash of Fuligo protoplasm:
chlorine, sulphur, phosphorus, potassium, magnesium, sodium, calcium,
and iron.

Enzymes, or organic catalysts, are of great importance in protoplasm
because of their power of initiating and altering the rate of reactions.
Their chemical nature is a matter of considerable dispute. Urease,
isolated from jack-bean meal, is a globulin,^ and there is evidence that a
number of other enzymes also are proteins. The high specificity
characterizing the action of enzymes indicates the importance of their
chemical composition, and it is also ev-ident that such action depends
largely upon the peculiar energy relations existing at the surfaces they
occupy or present.^

The amount of water in protoplasm varies greatly under different con-
ditions, but usually it is present in large proportions. It makes up from
85 to 95 per cent of the weight of actively streaming protoplasm such as is
seen in Tradescantia, and in actively functioning cells it rarely drops
below 70 per cent. In dry spores, however, it may be reduced to 10 or 15
per cent, the protoplasm then becoming very viscous. The body of a
jellyfish may consist of more than 99 per cent by weight of water. The
approximate composition of the human body is as follows: water, 65
per cent; protein, 15 per cent; fat, 14 per cent; salts, 5 per cent; other
organic compounds, 1 per cent. A considerable portion of the water in
the cell or body is physically "bound" in the colloidal structure of the
protoplasm and must be considered an integral part of the living system.

No single substance is of greater significance in the life of the organism
than water. In the words of Henderson (1913):

. . . the physiologist has found that water is invariably the principal con-
stituent of living organisms. Water is ingested in greater amounts than all
other substances combined, and it is no less the chief excretion. It is the vehicle
of the principal foods and excretion products, for most of these are dissolved as
they enter or leave the body [across the wall of the intestine and across the
epithelia of kidnej^s, lungs, and sweat glands]. Indeed, as clearer ideas of the
physico-chemical organization of protoplasm have developed, it has become
evident that the organism itself is essentially an aqueous solution in which are
spread out colloidal substances of great complexity [Bechhold, 1912]. As a
result of these conditions there is hardly a physiological process in which water
is not of fundamental importance.

It is not only by virtue of its great solvent power that water is so
effective in promoting chemical interaction. Its exceptional ionizing
power is especially noteworthy in this connection, while its high surface
tension has a notable influence on reactions involving adsorption. There

' Sumner (1926), Sumner and Hand (1928).
8 See Gortner (1929; Chap. XXXV).

PROTOPLASM 29

is also evidence that water is necessary to that most fundamental of vital
processes, oxidation. The importance of these and other characteristics
of water is discussed at length by Henderson in his inquiry into the
biological significance of the properties of water.

Another highly important chemical feature of protoplasm is its
hydrogen-ion concentration. Through the use of color indicators and
the microinjection method Chambers and his associates^ have determined
the pH of a number of animal cells with considerable accuracy. They
find the nucleus to be slightly alkaline (pH about 7.5 to 7.6) and the
cytoplasm slightly acid (pH about 6.7 to 6.9).^° Injury causes the cyto-
plasm to become much more acid (pH 5.2 to 5.5). If the pH remains
altered, the cell dies. The experiments show the protoplasm to be well
"buffered," or protected against sudden or radical alterations in pH, by
certain substances in solution. The principal buffers in organisms are
carbonates, bicarbonates, and phosphates. It is a very significant fact
that the vital reactions occur in a medium near the point of neutrality, and
that protoplasm has a means of preserving its pH at the proper level under
a considerable range of environmental conditions.

The pH values for plant protoplasm are less well known, since the
analyses have included considerable amounts of cell sap, which in mature
cells is usually decidedly acid in reaction. As a result, the published
values^^ in nearly all cases fall well on the acid side of neutrality. More-
over, in determinations made on expressed saps an increase of acidity due
to injury is suspected.

Active acidity, due to the concentration of free hydrogen ions, is to
be distinguished from potential acidity, which is determined by the quan-
tity of hydrogen ions which can be made to combine with a base. The
nucleus, although slightly alkaline to indicators, has a large amount of
undissociated nucleic acid which reacts strongly with basic dyes in the
usual staining procedures; hence the common statement that the nucleus
reacts as an acid. In general the cytoplasm has a high potential alka-
linity and a slight active acidity.

Protoplasm, because of the many combinations possible among its
numerous constituents, is a substance which may exist in a vast number of
different forms. When it is further recalled that many of the constituents

» Chambers (1928, 1930(7, 1932), Chambers and Pollack (1927), Chambers,
Pollack and Hiller (1927), Chambers, Pollack and Cohen (1929), Reznikoff and
Pollack (1928), Pollack (1928), Chambers and Cameron (1932), Chambers and Kerr
(1932).

^^ The reactions of solutions ranging from 0. 1 normal in terms of hydrogen ions
to lO"!* normal are expressed in 14 steps from /jH 1 to jiH 14. The neutral point is
at pH 7; a solution with a lower p^ is acid, while one with a higher pH is alkaline.
The scale is a logarithmic one, a decrease of 1 in /jH corresponding to a tenfold increase
in hydrogen-ion concentration. See Gortner (1929, p. 92).

" Eichhorn (1927) and Small (1929) review the data for plant tissues. See the
papers of Pfeiffer (1930, 1931, 1932) on the isoelectric point.

30 INTRODUCTION TO CYTOLOGY

exhibit singly the phenomenon of isomerism, this number is seen to be
incalculable. For example, it was shown by Miescher that an albumin
molecule with 40 carbon atoms could have about 1,000,000,000 isomers,
and some albumins probably have more than 700 carbon atoms. Albu-
min, moreover, is only one of many complex substances present in proto-
plasm. Hence, the statement that all living cells are composed of the
same substance, protoplasm, is true only in a general sense. Although
they are made up of the same categories of substances existing in the
same general type of organization, the protoplasms of different organisms
vary widely in the relative amounts of these leading constituents. For
example, the fats and lipides are relatively more abundant in the proto-
plasm of animals than in that of plants. The carbohydrate-protein
ratio also shows notable differences in the two kingdoms, carbohydrates
being relatively more abundant in plant protoplasm. ^^ Qualitative
differences are no less significant. The carbohydrates, which in plants
are chiefly pentoses and in animals chiefly hexoses, may be cited. Analo-
gous differences also exist between the smaller plant and animal groups,
and with these differences in chemical constitution are associated many
characteristic diversities in metabolic activity. Thus it is not simply
with protoplasm, but with protoplasms, that the working biologist has to
deal.

Special emphasis has been placed by Kossel, E. T. Reichert, and a
number of other writers upon the relation of this great diversity in the
constitution of protoplasms to the amazing variety observed among
living organisms. Reichert and Brown (1909) have shown that each
animal species examined has its own characteristic type of haemoglobin,
and that relationships may be indicated by degrees of similarity in the
crystals of this substance. The same situation is found in the case of
starch in plants (Reichert, 1913, 1919). That the specificity of organisms
is largely a matter of protein diversity is strongly indicated by the
phenomena of immunology. ^^ At the same time the importance of
structural diversity must not be forgotten.

In concluding this section, the general significance of the results of
analyses of protoplasm by chemical methods should be considered. It
cannot be maintained that anything like an adequate chemical picture of
living protoplasm has been obtained. As A. Meyer (1920) and others
have pointed out, such analyses include ergastic reserves and by-products,
which differ in amount and kind at different stages of the metabolic
cycle. Furthermore, in such a complex and delicately balanced system
as protoplasm the analytical methods employed can scarcely fail to induce

^^ E.g., compare the analyses of Sabellaria eggs (Faure-Fremiet, 1921) and Zea
pollen (Andersen and Kulp, 1922, 1923).

" See Reichert (1914) and R. S. Lillie (1923; Chap. Ill and literature there cited),
also the discussion by G. Reed (1923).

PROTOPLASM 31

reactions which result in the formation of compounds not present during
life. In spite of their shortcomings, however, chemical analyses do yield
valuable information concerning the types of substance present in proto-
plasm and the relative proportions in which they may occur. Such
information, inadequate as it may be, is obviously prerequisite to any
understanding of protoplasmic activity.

The chief point to be borne in mind is that chemical analyses do not
reveal a most significant characteristic of protoplasm, namely, its peculiar
organization. Just as in the case of any other operating system, such as a
watch, the activities of protoplasm can be understood only if the struc-
tural relations of the materials composing it are known. It is now
abundantly clear that the essential synthetic chemical reactions of proto-
plasm depend upon an essential type of structure present only during life
(see R. S. Lillie, 1923, 1924).

The Physical Nature of Protoplasm. ^^ — Under the ordinary micro-
scope living cytoplasm appears as a colorless, optically homogeneous
fluid, called hyaloplasm, in which there are usually imbedded granules and
globules of varying size, shape, and number. It is commonly observed
to be in a state of active streaming, notably in highly vacuolate cells
of plants. In the leaf cells of Elodea, for instance, the cytoplasm is in
almost continuous rotation, while the stamen hairs of Tradescantia afford
a beautiful example of a more complex type of circulation. Various
theories, involving electricity, contractility, surface tension, imbibition,
and other phenomena have been propounded to account for such proto-
plasmic movement. ^^ The specific gravity of protoplasm is very slightly
above that of water.

Noteworthy among the general physical characteristics of living
protoplasm are its elasticity and viscosity. These are properties which
it is difficult to estimate quantitatively. Much has been learned about
them through the use of microdissection apparatus, ^"^ the centrifuge, ^'^ and
electromagnets acting on inserted iron or nickel particles. ^^ The viscosity
varies greatly in different tissues, in different portions or organs of a
cell, and at different stages of cell-division and differentiation. In
general, it seems that animal protoplasm is on the average more viscous
than that of plants. In nerve cells and non-dividing epithelial cells no
Brownian movement is visible, even with dark-field illumination, but in
plant cells, as well as in eggs and many tissue-culture cells of animals,

1^ See Chambers (1924), Lundegardh (1922, Pt. I, Chap. XI; Pt. II, Chaps. I-III),
Meyer (1921), Schaeffer (1920), Harper (1919), Wilson (1923, 1926), Heilbrunn
(1927, 1928), Seifriz (1929a). Weber (1926a) and Spek (1926) give bibliographies.

>s Meyer (1921), Beikirch (1925), S. Nichols (1925), Fitting (1927), Spek (1926),
Umrath (1930).

" Chambers, Seifriz, C. V. Taylor.

" Lyon, Heilbrunn, Weber, W. Zimmermann.

'* Heilbronn, Freundhch, Seifriz.

32 INTRODUCTION TO CYTOLOGY

it may readily be observed (see Chambers, 1924). Seifriz (1924a) states
that the viscosity of protoplasm is on the average about like that of
glycerine and seldom below that of machine oil. According to Heilbrunn
(1926c), the viscosity of the granule-free cytoplasm of the Arbacia egg
is 0.02 and that of the Cumingia egg 0.04 (water = 0.01). With the
granules included the values are 2 or 3 times as high as this. Myxomy-
cete protoplasm is found to be 15 or 20 times as viscous as water (Heil-
bronn, 1922). The internal protoplasm of Paramoecium is said to be
8,000 times as viscous as water (Fetter, 1926), although this may be due
in part to fibrillar structures present. The effects of a variety of agencies
on viscosity have been ascertained.^^ The viscosity changes occurring
during meiosis, syngamy, and cell-division will be referred to in a later
chapter.

As already stated, cytoplasm nearly always contains visible globules
and other particles. These represent vacuolar material, chondriosomes,
and more or less transitory nutritive substances of various types. Some
cells show no such elements or only chondriosomes, but this condition is
rather exceptional. The smallest of the other visible granules, the
"microsomes," are almost universally present, according to Chambers
(1917, 1924). In the echinoderm egg there are, in addition, many larger
"macrosomes" (called "alveolar spheres" by Wilson, 1899), which
measure 3 or 4^ in diameter and seem to represent nutritive matter.
Other bodies, such as fat and oil globules, are also present. All of these
may be so abundant that the ground substance, or hyaloplasm, is almost
invisible. Likewise, in plants especially, minute vacuoles may be so
numerous that the protoplasm has an alveolar or foamy appearance.
Fibrillar differentiations may further complicate the picture. It will be
readily recognized that the optical appearance of a given sample of
protoplasm depends very largely upon the kinds of inclusions present,
their size and arrangement, and the degree to which they are crowded
together.

A fact which is both striking and very significant is that cytoplasm
may be deprived of all the above inclusions without losing the power of
carrying on certain of its characteristic activities. Hyaline pseudopodia
amputated from granular amoebae are irritable and move in a typical
amoeboid manner. Centrifuged sea-urchin eggs can be cut into two por-
tions, one with all the visible granules (except oil globules) and the other
with none, after which both portions may be inseminated and undergo
cleavage (see Chambers, 1924). This means that the visible inclusions,
although they should be regarded as a part of the living system to the
degree in which they are active in protoplasmic reactions (see p. 46),
are not an indispensable part of that system; and that "it is in the appar-

J9 Heilbrunn (1920c, 1924, 1925/, 1929a&), Heilbnmn and Young (1930), Weber
(1922, 1923, 1927), Scarth (1924), and others.

PROTOPLASM 33

ently structureless hyaloplasm that the real problem of cytoplasmic
organization lies" (Wilson, 1923).

With the aid of a Spierer objective, which has a portion of the rear
surface of the front lens silvered, Seifriz (1931) has been able to see in
the hyaloplasm of onion cells a structure not hitherto reported. In the
optically empty ground substance ("cryptoplasm") there are dispersed
innumerable droplets of a grayish substance ("phaneroplasm"). The
cytoplasm thus has a finely mottled appearance. As the cytoplasm
streams, the phaneroplasm takes the form of parallel rods or continuous
strands 0.3 to OAfx thick and 0.2 to 0.3/i apart. It is the cryptoplasm
which appears to be the actively streaming component.

The Colloidal State of Matter. — It is evident that many phenomena
in protoplasm are in some way dependent upon its ultramicroscopic
structure. It is here that cytology has received a notable contribution
from the field of physical chemistry in the form of facts and hypotheses
concerning the colloidal state of matter.-'^

Matter is said to be in the colloidal state when it is subdivided into
ultramicroscopic particles. Matter in which the particles are large
enough to be microscopically visible may show some of the properties of
colloids, but such properties are exhibited most characteristically when
the size of the particles lies between 0.1/x and Im/x. Such particles, or
"micelles," are generally groups of molecules, although it seems that they
may sometimes be single large molecules {e.g., in egg albumin). Although
they cannot be seen with the ordinary microscope, which reaches the
limit of its power with particles between 0.2ju and O.lix in diameter, their
presence may be indicated by the Tyndall phenomenon or by the ultra-
microscope, under which they appear as bright points against a dark
field. Wolfgang Ostwald (1917) gives the following table of diameters:

Red blood corpuscle 7,500mM ( =7.5;u)

Staphylococcus 800

Particles in fine mastic suspension 500-1,000

Casein particles in milk 130-170

Colloidal gold particles 2-15

Molecule of soluble starch 5

Molecule of hsemoglobin 2.5

Molecule of grape sugar 0.7

Molecule of hydrogen 0.1

The colloidal substance is, of course, enveloped in some other medium

(gas, liquid, or solid), the two together constituting what may be termed

a colloidal system. The subdivided substance is known as the "disperse

phase," and the enveloping medium as the "dispersions medium."

2° See Bancroft (1921), Bayliss (1915, 1923), Bechhold (1919), Czapek (19116),
Hatschek (1916), Lundeg&rdh (1922; Pt. I, Chap. XI), Meyer (1920; Chap. IV),
T. B. Robertson (1920), Lepeschkin (1924), Svedberg (1928), Freundlich (1928),
Gortner (1929), and Gray (1931). .

34

INTRODUCTION TO CYTOLOGY

Each of the physically homogeneous constituents, or phases, may be
chemically complex; an aqueous phase, for example, may contain salts
and other compounds in solution. The different chemical substances,
including the solvent, which make up a phase, are called components.
Furthermore, more than two phases may be present; there may be
"polyphase systems"; but it will be sufficient for our purpose to deal only
with those having two phases.

Colloidal systems differ widely in general properties according to the
liquid, solid, or gaseous nature of the phases. The following list of
familiar substances will help to give a picture of colloidal structure,
although some of them, because of the large size of their particles, are
only large-scale models of such structure.

Liquid in liquid: mayonnaise
Solid in liquid: muddy water
Gas in liquid: foam
Liquid in solid: pearl

Solid in solid: true ruby glass
Gas in solid: bread
Liquid in gas: fog
Solid in gas: smoke

It is with the liquid colloidal systems that biology is chiefly concerned.
Typically these are uncrystallizable, considerably more viscous than
water, readily coagulable, only slightly or not at all osmotic, and poor as
electrical conductors. In all of these features they differ markedly
from true molecular solutions. It was formerly customary to classify
them as "suspensoids," in which the suspended matter is solid, and
"emulsoids," in which it is supposedly liquid. More adequate is the
classification into lyophobic and lyophilic systems. A lijophohic system
is one in which neither phase will dissolve in the other, whereas in a
lyophilic system the disperse phase and the dispersions medium are
more or less soluble one in the other (Martin Fischer). Gelatin in water
is a lyophilic system; gelatin in alcohol is a lyophobic system. It is
uncertain to what extent the dispersions medium actually dissolves in the
micelles in the solvation of a lyophilic colloid (as when gelatin swells in
water, a case of hydration) or only becomes closely "bound" in layers
about them (Gortner, 1929, p. 212.)

Colloidal systems are referred to as sols if they flow readily and as
gels if they do not. Gels include jellies (true gels) formed by lyophilic
colloids, and coagula formed by precipitation in lyophobic ones. A sol
may be made to become a gel {gelation) or a gel to become a sol {peptiza-
tion) under certain conditions. In many cases such alterations are
reversible. What structural change occurs during gelation is not well
known, but there is evidence which indicates that an agglomeration or a
partial coalescence of the suspended particles occurs, with the resulting
formation of a reticulum or a spongework of threads. The consistency
of a colloidal system obviously may vary according to the relative volumes
of its phases, the closeness with which the dispersed particles are packed

PROTOPLASM

35

in the dispersions medium (Fig. 14), and the measure in which the dis-
persions medium is bound by the micelles.

The stability of a liquid colloidal system with a solid disperse
phase depends largely upon the similar electric charge carried by the
suspended particles. The addition of an electrolyte neutralizing the
charges brings about a precipitation of the particles. In a liquid-in-

4

>.p'

N^

-.-'/v

Fig. 14. — Diagram to show the various appearances observable in a two-phase colloidal
emulsion. A, suspended droplets well separated, giving an alveolar appearance. B,
droplets crowded, giving continuous phase a reticular appearance. C, D, aspects due to a
proportionally smaller amount of the originally continuous phase and a coalescence of the
droplets, both phases becoming continuous.

Fig. 15. — Photograph of an
oil-water emulsion. {After Seifriz,
1930a.)

Fig. 16. — A torn Fticus
egg. Compare with Fig.
15. (After Seifriz, 1930o.)

liquid system the matter is more complicated. A relatively coarse
oil-water emulsion will serve to illustrate some of the principal facts.
When olive oil and water are beaten up together, the oil forms droplets
suspended in the water. If the mixture is allowed to stand, the two
constituents quickly separate. If, however, one includes in the original
mixture a third substance having a certain effect upon surface tension (an
"emulsifier," or "stabilizer"), the resulting emulsion is stable, since the
emulsifier enters the interface between the oil and the water and prevents
the coalescence of the droplets (Fig. 15). Mayonnaise dressing is an

36

INTRODUCTION TO CYTOLOGY

emulsion of oil in an aqueous medium (vinegar) with egg protein as an
emulsifier. Milk also is stabilized largely by proteins. When water-
soluble sodium oleate is formed as the emulsifier in an olive oil-water
mixture by adding NaCl, the oil disperses in the water; this occurs even if
the water constitutes only 1 per cent of the whole, the water forming a
series of thin films separating the large oil droplets. When oil-soluble
calcium oleate is formed by including CaCU, the water disperses in the
oil. By employing both sodium and calcium salts, varying their ratio,
the important change known as phase reversal may be produced at will
in either direction (Fig. 17). At a certain critical ratio there is a very
delicate balance between the two conditions, and it is a biologically
significant fact that the ratio at which colloidal proteins and lipides form

A

Fig. 17. — Diagram illustrating phase reversal in a colloidal emulsion. A, aqueous
phase. B, oil or other non-aqueous phase. C, interfacial film formed by emulsifying
agent. {After Clowes, 1916.)

such balanced emulsions is about the same as that in which the two classes
of salts occur in both blood and sea water.

In many colloidal systems the finely divided substance is in the form
of filaments or thin films rather than globules or small granules. Further-
more, these may extend throughout the mass as a network or platework,
neither phase being wholly discontinuous. The structure of such an
"interlacing system" is illustrated on a large scale by bread or a rubber
bath sponge. What is essential to all types of systems is the enormous
extent of the interface, and to obtain this condition it is therefore only
necessary to make at least one dimension of the dispersed matter small.
It can readily be calculated that a cube of matter 1 centimeter in each
dimension and exposing 6 square centimeters of surface would expose 60
square centimeters if cut into 1-millimeter cubes, 6 square meters if cut
into 1-/X cubes, and 6,000 square meters if cut into l-m^u cubes.

The Colloidal Nature of Protoplasm. — The work of the past few years
has made it abundantly clear that protoplasm is a colloidal system. This
is manifest in its general physical properties. Its viscosity, surface-
tension phenomena, power of adsorption, and high electrical resistance

PROTOPLASM 37

are like those of other known colloids. Its semipermeable properties are
typically those of colloidal systems; a semipermeable region is probably
present wherever protoplasm comes in contact with other substances,
such as water. Protoplasm shows most strikingly its colloidal character
in the alterations of physical state, involving imperfectly understood
structural changes, which it undergoes as a result of variations in external
conditions and internal reactions. Local temporary alterations of this
nature are known to accompany a number of important life processes.
Protoplasm, like many organic and inorganic colloids, is irreversibly
coagulated by too high temperatures and a variety of chemical substances.
The "fixation" of protoplasm by the reagents employed in cytological
technique is primarily the transformation of a lyophilic system into an
irreversible lyophobic coagulum.

Protoplasm is colloidal, but the question of the particular type or
types of colloidal structure it possesses is one to which no satisfactory
answer can yet be given. The most widely prevalent theory is that the
emulsion type of structure, often visible with the microscope, is continu-
ous with an ultramicroscopic colloidal structure of the same sort, with
discontinuous phases of lipides, proteins, and other liquid and solid sub-
stances suspended in an aqueous medium. It has been thought by some
that high electrical resistance indicates a discontinuity of the water phase
(M. Fischer, 1923), some non-conducting material constituting the medium
of dispersion. The suddenness of many permeability changes has been
thought to favor the view that protoplasm has an emulsion structure, at
least in plasma membranes (Clowes, 1916). R. S. Lillie (1923) sees
further evidence in a variety of phenomena, including the autolytic action
of injured cells wherein enzyme and substrate are allowed to interact by
the breakdown of films normally separating them.

The view that the submicroscopic colloidal constitution of protoplasm
is primarily like that of an emulsion has been brought into question by
Seifriz (1924a6, 1926a6c, 19295). He points out that living protoplasm,
although it may show such a structure within the power of the micro-
scope (Fig. 16), differs markedly from emulsions in its noticeable degree of
elasticity, its power of imbibition, and its characteristic behavior in form-
ing a granular irreversible coagulum at death. Comparisons wdth certain
inorganic systems suggest that it has a structure in which the units are
arranged in linear chains which may form a three-dimensional network or
"brush heap."

It is not to be concluded that investigators insist that all protoplasm
must have this or that particular type of colloidal structure. It is
probable that the minute structure varies within wide limits in different
tissues and in different regions of any differentiated mass of protoplasm.
It may be that emulsions, interlacing systems, and molecular bridgeworks
all actually exist and pass one into another according to general and local

38 INTRODUCTION TO CYTOLOGY

conditions. Only future research will permit an evaluation of the many
conflicting views on this subject. Of special interest will be the results
of studies to determine to what extent protoplasm may possess a micellar
structure comparable to that of many of its products (p. 179). The point
to be borne in mind at present is that the structure in any event is indis-
putably colloidal, and that our attempts to explain protoplasmic behavior
must be based on this fundamental fact. We shall proceed, then, with
the general conception of protoplasm as a complex system of many sub-
stances dispersed in the form of granules, globules, filaments, networks,
and plates, which thus expose an enormous area of reacting surface in
proportion to their volume. The system includes an extensive series of
thin films in the interfaces between the continuous and dispersed phases,
between the differentiated protoplasmic regions or organs, and around the
mass as a whole.

Some of the activities of protoplasm which seem clearly to be condi-
tioned by its polyphase, film-partitioned organization may now be briefly
enumerated. ^^

A great many chemical substances coexist in protoplasm without inter-
acting until certain conditions prevail, whereupon interaction occurs
suddenly and extensively. This is thought often to involve films separat-
ing the different phases of the system. Under appropriate circumstances
the properties of these films are rapidly altered, allowing the substances
on either side to interact, and the volume and the velocity of the reaction
are due in large measure to the enormous area of reacting surface. The
films separating various regions within a protoplasmic mass permit the
localization of very diverse types of chemical activity within a small space
and the consequent differentiation of organs in which these activities are
then more efficiently carried on. A particularly important case of the
control of reactions through changes in colloidal films is seen in general
and local alterations in the permeability of the plasma membrane bound-
ing any unit mass of protoplasm, a matter to be discussed in the next
section.

The effect of colloidal structure upon processes involving adsorption
is noteworthy. Substances are peculiarly subject to chemical change
when adsorbed at surfaces because of the special energy conditions present
there. Adsorption is frequently a necessary preliminary to chemical
reaction. In protoplasm there exists an ideal structural basis for such
"adsorption catalysis"; in fact, it seems that "the determination and con-
trol of chemical reactions by adsorption are universal in living proto-
plasm" (R. S. Lillie, 1923). It seems clear that a part of the catalytic
activity of enzymes is due to their colloidal state; indeed, it appears that
respiration itself is a surface reaction conditioned in this way (Warburg;
see, further, Beutner, 1933). These facts suggest why it is that certain

" See Bayliss (1923) and R. S. Lillie (1923).

PROTOPLASM 39

reactions, such as rapid oxidation, ordinarily occurring only at high tem-
peratures, may take place at relatively low temperatures in the organism.

Finally, in the film-partitioned structure of protoplasm there is a
basis for further electrical phenomena, a subject fully discussed by Lillie.
Electric currents have been shown to accompany a variety of vital
processes and to have a fundamentally important bearing upon problems
pertaining to the reception and conduction of stimuli, automatic or reflex
activity, muscular contraction, the movement of plant parts, correlation,
polarity, growth, and other biological phenomena. "They .appear, in
fact, to be as essential a feature of protoplasmic action as the consumption
of oxygen or the evolution of CO2. "

Ectoplasm and the Plasma Membrane. — It has long been known
that there is at the normal surface of any mass of
protoplasm a layer whose physical properties differ
somewhat from those of the substance within the
mass. Sometimes such a differentiation can be
easily seen: in amoebse and myxomycetes a layer of
hyaline ectoplasm surrounds the granular endoplasm
within (Fig. 18) . Frequently the boundary between
these two is not at all sharp, and it seems evident
that they may be readily converted one into the
other. Among Protista, as will be shown farther
on, the edoplast is often elaborately differentiated
and may be accompanied by additional envelopes. pj^ is.— An amceba,

There is a large body of evidence for the view showingectopiasm.endo-

,•■ , 1- 1 xi • 7 1 plasm, and contractile

that an exceedingly thin plasma membrane, or vacuole.
plasmalemma, is always present at the surface of

the protoplast, whether any special ectoplasmic layer can be directly
observed or not. In case such a layer is present, the plasma membrane
represents its external surface film. Much has been learned about the
plasma membranes of amoebae and other cells by observing the behavior
of particles adhering to it (Schaeffer, 1920) and by the use of the micro-
manipulator.-^ In myxomycetes Seifriz finds the outer membrane to be
distinctly more elastic and tenacious than the hyaline substance imme-
diately beneath. Although it is very thin, it is a definite morphological
structure which may be removed after death with dissecting needles.
Moreover, it is capable of constant repair. Such a capacity to form a
surface membrane immiscible with water, provided the injury has not
been too sudden and extensive, seems to be generally present in healthy
protoplasm. The development of the membrane is in many respects like
that of the formation of superficial films by other colloidal systems,
although in the case of protoplasm certain metabolic syntheses seem to be

"Kite (1913), Chambers (1917 et seq.), Seifriz (1918, 1921), Chambers and
Hofler (1931), Plowe (1931a).

40 INTRODUCTION TO CYTOLOGY

involved. In the Arhacia egg there is a reaction of calcium with a sub-
stance visible in the cytoplasm, according to Heilbrunn (1928, 1930a).

Because of the very different surface conditions prevailing in tissue
cells, the differentiations can scarcely be expected to be wholly the same
as in "naked" masses of protoplasm. Nevertheless, there is reason to
believe that here, too, specialized osmotic membranes are responsible for
certain physiological phenomena, notably selective permeability, as was
claimed long ago by Pfeffer (1890). Plowe (1931a6) has been able to
show both by microdissection and by permeability studies that the plasma
membrane in the familiar cell of the onion-bulb scale is a real structure.
That surface membranes have properties not present in the endoplasm is
shown by the fact that certain substances, eosin for example, to which the
membrane is impermeable, will diffuse readily through the endoplasm if
artificially injected through the membrane (Chambers). Such semi-
permeable membranes (membranes permeable to solvent but not to
solute) are also present about nuclei and sap vacuoles (see below). All
such membranes of the protoplast appear to be lyophilic gels. In the
case of a vacuolate cell, the permeability of the whole is determined by the
permeabilities of all the regions traversed — plasma membrane, endoplasm
and vacuole membrane — but it is due chiefly to the membranes.

Because of the great importance of the cell membrane in physiology
many studies have been made with the hope of determining its exact
physico-chemical constitution.-^ One of the most influential theories has
been that developed by E. Overton (1895 et seq.), who concluded that the
membrane is composed primarily of lipides. This theory was founded
chiefly on the high correlation found to exist between the lipide solubility
of many organic compounds, notably dyes, and their ability to pass
through cell membranes. IMoreover, lipides would be expected to
accumulate at free surfaces, and their presence would help to explain the
immiscibility of the membrane with water. This theory has been much
criticized, not only because it has been thought not to account satis-
factorily for the high permeability of the membrane to water, but also
on the basis of further studies on permeability and leaching.-^

The probable importance of proteins in the cell membrane has been
emphasized by a number of investigators, ^^ partly because of the colloidal
nature of these substances and the readiness with which they form pre-

2^ For discussions and literature pertaining to the constitution and physiological
behavior of plasma membranes, see Schaeffer (1920), Bayliss (1921), LundegSrdh
(1922), Hober (1922), R. S. Lillie (1923), Chambers (1924), Jacobs (1924), Stiles
(1924), Weber (19266), Gellhorn (1929), Steward (1929), Gray (1931), and
Beutner (1933).

2^Ruhhmd (1908 et seq.), Hober (1909, 1922), Steward (1928a6, 1929), Bailey
and Zirkle (1931). See, further. Gray (1931).

26 Pfeffer (1900), Ramsden (1904), Osterhout (1911), Loeb (1911), T. B. Robertson
(1908), Lepeschkin (1910, 1911).

PROTOPLASM 41

cipitation membranes. The high permeabihty of such membranes to
strong electrolytes is, however, against the assumption that they can be
primarily responsible for the selective properties of the living cell's
surface (Gray) ; moreover, protein membranes do not exhibit the neces-
sary osmotic properties.

As a result of such difficulties, physiologists have been forced to the
conclusion that the membrane is characterized by a peculiar physical
and chemical complexity. That both lipide and protein constituents are
present is strongly indicated, but what other constituents may accompany
them, and how they are all physically arranged, is not at all clear.
According to Gortner (1929), it is possible to picture the membrane pro-
visionally as consisting of a "protein gel, probably in the form of a fibrillar
structure with fats, soaps, and lipides immeshed in the protein network.
The transfer of lipide-soluble materials would be through the fat-soap-
lipide portion of the structure, whereas the passage of water and such
water-soluble materials as actually do pass in and out of the cells would be
through the hydrated filaments of the protein network."

Various conjectures have been made regarding the possible alterations
in the structure of the colloidal cell membrane as it undergoes observed
changes in permeability. Clowes (1916, 1918), who studied the relation
existing between balanced antagonistic salts and phase reversal in olive
oil-water emulsions, believed that similar reversals of lipide and aqueous
phases might account for permeability changes in cell membranes, the sub-
stance originally forming a continuous path becoming discontinuous, and
vice versa. Many membranes maintain their normal state of semipermea-
bility only when the ratio of such antagonistic salts is held constant within
narrow limits. Since colloidal systems are known in which the two phases
differ chiefly in the relative proportion of water they contain, it has
also been suggested that changes in permeability may be due to redis-
tributions of water between such phases in the membrane (Lloyd, 1915;
Free, 1918). Such changes would affect the size of dispersed droplets and
the closeness with which they are packed and hence the action of the
membrane as a whole. Such a hypothesis is thought to account more
readily for very gradual changes in permeability than does the reversal
hypothesis. Both gradual and sudden changes occur, and it is highly
probable that they involve structural alterations of more than one type.

In his discussion of this general subject Gray (1931) lays emphasis
upon the fact that "the living cell is bounded by a surface or a membrane
which is capable of generating energy or of transforming energy which is
supplied to it in an appropriate form, " and upon the further fact that no
inanimate system known at present has the electrical properties mani-
fested by the cell membrane. "In other words the plasma membrane is
part of a dynamic system whose machinery is of a type not yet demon-
strated outside the living cell." It remains true, however, that the

42

INTRODUCTION TO CYTOLOGY

results obtained with artificial systems, if rightly construed, cannot fail to
contribute to our understanding of cell membranes and their action (see
Beutner, 1933).

Vacuole Membranes. — The character of the tonoplast, or membrane
bounding the ordinary sap vacuole, has been the subject of many investi-
gations. In 1885 de Vries found that the large central vacuoles of Allium
and Spirogyra could be isolated by placing the cells in hypertonic solutions
of a potassium salt, and that the semipermeability of their membranes was
retained in a measure for some time. Such observations on onion cells
have been repeated and extended by Chambers and Hofler (1931), who
have isolated the vacuole with a micromanipulator. They find the
tonoplast membrane-*^ to be "a highly cohesive and extensible fluid film
of unappreciable thickness." It resembles the plasma membrane in being
immiscible with water when normal, in not wetting a clean glass micro-

Fig. 19. — Discharge of the contractile vacuole (Vi) and the accompanying behavior of
subsidiary groups of vacuoles (gr. Vi, gr. Vs) in Euplotes. p.p., papilla pulsatoria. mac.
macronucleus. {After C. V. Taylor, 1923.)

needle, and in being wetted by oil and chloroform. A further resemblance
is seen in the failure of acid dyes to pass through either membrane when
injected into the cytoplasm (Plo^ve, 19316).

The osmotic properties of vacuoles are important not only in connec-
tion with metabolic processes but also in supporting many plant struc-
tures through turgor. It is also by virtue of osmotic action that vacuoles
may function in subdividing large masses of protoplasm in the sporangia
of certain fungi (p. 165), in pollen tube formation (Woycicki, 1926), and
doubtless in many other processes.

The contractile vacuoles of certain lower animals and plants have
similar limiting membranes. Such vacuoles periodically absorb water
and solutes from the protoplast and then expel them to the exterior. In
some cases, as in Paramcecium trichium (Wenrich, 1926), there is evidence
that the membrane is a permanent structure which contracts rhythmically
to expel fluid received from subsidiary vacuoles. In fixed material the
membrane shows a characteristic fibrous structure. In Euplotes, C. V.
Taylor (1923a) finds that the primary contractile vacuole, which is

2^ Chambers and Hofler extend the term "tonoplast" to the vacuole as a whole
with its membrane. De Vries applied it to the membrane alone. See also Plowe
(1931o).

PROTOPLASM 43

accompanied by two adjacent series of smaller vacuoles, discharges its
contents through a definitely localized but temporary ectoplasmic pore,
whereupon it disappears completely. Its place is then taken by another
formed by the union of secondary adjacent vacuoles (Fig. 19). These
latter vacuoles arise in turn from still smaller ones, which seem either to
be derived ultimately from vacuoles containing granules that dissolve,
or to arise de novo as fluid centers causing the protoplasm to form a
membrane by gelation. These observations have an interesting bearing
on the problem of the origin of ordinary sap vacuoles (p. 94) In amoebse
the membrane of the contractile vacuole appears to be formed anew
periodically by gelation (Day, 1927) and shows certain resemblances to
the plasma membrane in its permeability (Morita and Chambers, 1929).

Contractile vacuoles have usually been regarded as excretory organs,
but there is evidence that they are mainly concerned in the regulation of
hydrostatic pressure. ^^ In Spirogyra, Lloyd (1925, 1928a6) has shown
that the action of contractile vacuoles is concerned in the movement of
the gametes at the time of conjugation.

The Ectoplast of Protista. — The ectoplast shows its most elaborate
structural differentiations in Protista, where it clearly has several func-
tions— protective, motor, excretory, and sensory (see Minchin, 1912,
Chapter V). In many forms there is a relatively tough outer envelope,
or "pellicle," in addition to the more fluid hyaline ectoplasm. The
origin and the degree of development of this envelope, however, are not
the same in all cases. Commonly, it seems to arise as a modification
of the outer region of the ectoplast. In Amoeba proteus, Mast (1926) finds
the internal protoplasm ("plasmasol") to be surrounded by a fairly rigid
granular layer ("plasmagel") and this in turn by a tough "plasmalemma"
about 0.25m thick. The "periplast" of flagellates seems to represent the
entire ectoplast modified. In still other forms the resistant envelope is
formed indirectly by secretion.

Among the ectoplasmic structures with a motor function the simplest
are the pseudopodia; in the larger ones there is a core of endoplasm, but
the more delicate "filose" ones consist entirely of ectoplasm. Minute
suspended particles can be detected in hyaline pseudopodia by the use of
dark-field illumination, their Brownian movement affording an index of
the fluidity of the ectoplasm (Bayliss, 1920). The cilia on the velum in
certain molluscan larvae have the form of thin blades, and each of these
is composed of a number of long plates (Fig. 20, C). In Spirillum long
contractile filaments are separable, but in Chromatium they are firmly
united (Metzner, 1920). Cilia, which are short and numerous and show
rhythmic pulsation, ^^ cirri, which are formed of tufts of cilia, memhranellce,

"" See Calkins (1926); also Weatherby (1927) and Day (1930).
^* For discussions of the structure and mechanics of flagella and cilia, see Heiden-
hain (1911), Lundeg&rdh (1922), Metzner (1920), Gray (1928), and Petersen (1929).

44

INTRODUCTION TO CYTOLOGY

representing fused rows of cilia, and undulating membranes, which are
mainly sheet-like extensions of the ectoplasm (Fig. 20, A), are all essen-
tially ectoplasmic organs. In Blepharisma, Chambers and Dawson find
that when touched with a needle the undulating membrane breaks up
into cilia, which may reunite. A further motor differentiation is seen in
the minute contractile fibrils known as myonemes (Fig. 20, B), which are
analogous to a system of muscle fibers. In ciliated forms they run
beneath the rows of cilia.

Contractile or pulsating vacuoles sometimes appear to originate in the
ectoplasm, although they may later lie much deeper. In certain cases
definite actively protective organs, the trichocysts, are differentiated in the
ectoplasm. A sensory function may be performed by the "eyespot, "

A B CDS F

Fig. 20. — Types of motile apparatus. A, Trypanosoma tincce, showing undulating
membrane. B, Trypanosoma percw, showing myonemes. C, velar cilia of ^olis. D,
Uroglena volvox. E, Phacus pyrum. F, Hamatococcus pluvialis. {A and B after Minchin;
C after G. Carter (1926) ; D F after J. B. Petersen, 1929.)

which in some cases appears to be ectoplasmic in origin (see p. 67), and
also by flagella and cilia, which are often receptors of tactile stimuli.

Kinoplasm. — In his descriptions of the plant protoplast Strasburger
(1892, 1897a, 1898) made a distinction between the nutritive alveolar
trophoplasm and a specialized active kinoplasm, the latter constituting
the plasma membrane, fibrils of the mitotic figure, centrosomes, and the
contractile substance of cilia and allied structures. -^ Although the theo-
retical aspects of such a distinction were overemphasized by certain
writers, the terms have remained useful for descriptive purposes.

The importance of kinoplasm has been emphasized anew by Lloyd

and Scarth^" in studies of living cells of Spirogyra, Symphoricarpos,

Tradescantia, and Elodea. According to these workers, the kinoplasm

2^ Allied to this were conceptions involving archoplaam and ergastoplasm (see
Wilson, 1925, p. 723).

3" Scarth (1927), Scarth and Lloyd (1927), Lloyd (1926), Lloyd and Scarth (1926).

PROTOPLASM 45

not only constitutes differentiated films about the cell, the nucleus and
the plastids, but may also develop filamentous prolongations extending
from these films into the cytoplasm and from the tonoplast into the
vacuole. In extreme cases it may form a spongy framework throughout
the cytoplasm and a "medusoid" growth over the surface of the vacuole.
It appears to be the kinoplasm that is responsible for protoplasmic stream-
ing; it flows through the relatively stationary trophoplasm, carrying with
it the plastids and chondriosomes.^^ There appears to be an inverse
relationship between the abundance of chondriosomes and differentiated
kinoplasm; moreover, the active kinoplasm does not stain, but as it
metamorphoses into the tonoplast it colors faintly with Janus green.
These and other facts suggest that lecithin enters into the composition
of the kinoplasm and that the chondriosomes may represent a substance
used in its elaboration.

Lloyd has shown that the contractile vacuole of the Spirogyra gamete
(see p. 228) arises by a swelling of kinoplasmic globules in the cytoplasm.
The cleavage of the protoplasm of many sporangia to form spores is also
regarded as an activity of extending kinoplasm. Such observations raise
a number of important cytological problems and emphasize the need for
further work along this line.

Protoplasm and Metaplasm. — Because of the place they occupy in
cytological discussions we may outline several classifications of the sub-
stances composing organisms which certain writers have found useful.

J. Hanstein (1868):

1. Protoplasm: the living substance.

2. Metaplasm: non-living substances in or on protoplasm.
M. Heidenhain (1902, 1907):

1. Protoplasm: the principal form of living substance.

2. Metaplasm: a less active form of living substance, formed by a process of
differentiation in protoplasm in connection with special functions, and capable of
growth, response to certain stimuli, and fui'ther differentiation. It is represented
chiefly by the intercellular substance of animals; also by certain other structures,
such as elastic and connective tissue fibrils.

3. Non-living substances.
E. Rohde (1908, 1923):

1. Protoplasm: the principal form of living substance.

2. Metaplasm: a less active form of living substance; essentially the same as
Heidenhain's metaplasm but including also contractile and nerve fibers, which
Heidenham regarded as protoplasmic. Metaplasm, according to Rohde, cannot again
become protoplasm and does not continue from generation to generation.

3. Non-living substances.
A. Meyer (1896, 1920):

1. Protoplasm: the principal form of living substance.

2. Alloplasm.: a less active form of living substance, essentially the same as the
metaplasm of Heidenhain and Rohde. Cilia, flagella, and cytoplasmic fibrils are

'alloplasmatic organs." Organs of this class arise by direct transformation of all

^1 Seifriz's cryptoplasm and phaneroplasm (p. 33) would both be included in the
kinoplasm.

46 INTRODUCTION TO CYTOLOGY

or part of a protoplasmatic organ, usually the cytoplasm. They may dissolve but
do not become protoplasm again.

3. Ergastic subdances: non-living substances arising anew in or on the protoplast;
these correspond to the metaplasm of Hanstein. The intercellular substance, regarded
as living by Heidenhain, is held to be ergastic by Meyer.

Protoplasm and Life. — Huxley, in his famous essay of 1868, very
aptly termed protoplasm "the physical basis of life." Since the true
significance of protoplasm was first recognized, many suggestions have
been ventured regarding the nature of the relation existing between life
and its physical basis. The modern conception of protoplasm as a living
system was preceded by a number of speculative "micromeric theories,"
or "atomic theories of biology," according to which the principle of life
was held to reside in ultimate vital particles.^- Such fundamental
particles were supposed to be for the most part of ultramicroscopic size,
capable of growth and reproduction by division, and associated like
members of a vast colony in protoplasm. Attempts were also made to
account for the activities of protoplasm on the basis of the known chemical
reactions of certain of its constituents, notably the proteins. It is not
surprising that the peculiar properties of these compounds, which are
certainly very significant, should have led to the belief that life is primarily
a series of changes in special labile protein molecules, or "biogens"
(Verworn).

The fundamental fallacy involved in all such speculation lies in
attributing the properties of a system to some one of its constituent ele-
ments and consequently in attempting to draw a sharp line between
"living" and "lifeless" components. Sachs (1892, 1895) and many others
have urged that the various elements should be referred to as active and
passive rather than living and lifeless. It cannot be emphasized too
strongly that protoplasm is a living system of components which by them-
selves are non-living — a system composed of all the substances that are
participating in essential protoplasmic reactions at a given moment (cf.
Wilson, 1923).

The various constituents of protoplasm share in all degrees in deter-
mining the activity of the system of which they are integral parts. It is
probable that protoplasm always contains visible or invisible materials
which might be removed without terminating the life processes. This
does not prove, however, that these materials had no share in the processes
while they were a part of the system, but shows only that the system which
remains after their removal still has an organization permitting it to con-
tinue in the living state. It is an altered system and operates in a some-
what altered manner. Furthermore, the same chemical compound may

'2 For summaries of these theories, see Delage (1903), Heidenhain (1907), Kellogg
(1907), and Meyer (1920). Some regard the gene theory as a modern development of
the same kind.

PROTOPLASM 47

be active at one moment and relatively inactive at another, depending
upon its physical state {e.g., whether in solution or not) and the presence
of other substances with which to react. It is not a certain chemical
composition, but activity, that marks a substance as a part of the living
system. The system remaining after the supposed removal of all dis-
pensable materials would comprise many classes of substances, some of
which, notably water, carbon, and proteins, are probably essential in all
forms of protoplasm because of their peculiar properties. The fact that
these forms of protoplasm are almost innumerable suggests that the com-
ponents of the fundamental system must vary quantitatively, qualita-
tively, and in their type of structural organization within considerable
limits.

In any case it should be evident, in spite of the special importance of
certain forms of matter, that it is not this or that component but the
organized system as a W'hole which lives. Steel is not a time-keeping
material, but it may be an important constituent of a time-keeping
system, such as a watch. Proteins are not living compounds, but they are
important constituents of living systems. That which is distinctively
biological inheres not merely in the several components but in their
unique integration and the consequent peculiar action of the organized
system as a whole. The action of the whole can be said to be a sum of the
action of the parts only when it is remembered that the parts act as they
do because of their position in the whole. Hence a true conception of
the organism can be approached only when analysis into physico-chemical
components is followed by resynthesis into a biological whole. ^^

We may go a step farther and point out that the organism is not to be
sharply set apart from the environment. The two are so inseparably
interlocked that they must be conceived as a single integrated system
whose orderly operation is necessary to life.^^ Thus life is largely a rela-
tion or adjustment between the properties of the organism and those of
the environment (Brooks, 1889), or, as Herbert Spencer put it, a "con-
tinuous adjustment of internal relations to external relations. "

"See J. A. Thomson (1920), C. Lloyd Morgan (1923), Jennings (1927), Russell
(1930), and Gray (1931).

'^ For discussions of this point, see Jennings (1924), Sharp (1925), and Carrel
(1931).

CHAPTER III

THE NUCLEUS

It is now a century since the nucleus was first recognized as a normal
and characteristic element of cells, and half a century since a new era in
cytology was ushered in by a series of researches revealing the remarkable
behavior of the nucleus during the critical stages of the life cycle.
Because of the peculiarly intimate relation which this behavior has been
shown to bear to many outstanding biological problems, including that
of Mendelian heredity, it is largely in nuclear phenomena that cytological
interest has continued to center up to the present day. The most striking
of these phenomena form the subjects of several subsequent chapters; at
this point the nucleus will be considered only as it appears in the "meta-
bolic" condition, i.e., when not undergoing division.^

General Features of Nuclei. — Whether or not one should say that all
protoplasm or all cells are nucleated depends upon what is meant by the
term "nucleus." If the chromatic substance, no matter whether dis-
tributed throughout the cell in the form of small particles or aggregated
in a well-defined organ, be regarded as constituting a nucleus, then it
follows that all complete plant and animal cells normally have nuclei.
If, however, the term be employed only with reference to a distinctly
delimited organ, we must regard those Protista with only scattered
chromatic material as devoid of nuclei, although they may contain
matter which performs at least certain nutritive functions of a nucleus.
The question of the presence of nuclei in bacteria is discussed in Chapter
XIII. In nearly all known organisms there are nuclei with roughly the
same general type of organization, which indicates that the functional
and structural differentiation of protoplasm into cytoplasm and nucleus
doubtless occurred at a very early period in the history of the organic
kingdoms.

The number of nuclei present in any mass of protoplasm depends
largely upon the bulk of the mass, since within limits a certain ratio of
nuclear surface to cytoplasmic volume must be maintained for the
proper action of the whole system. A small mass with but one or a very
few nuclei may grow into an extensive canocytic body with thousands of

1 For an exhaustive review of the Uterature on plant nuclei, see Tischler (1921-
1922, especially Chaps. I-IV). Von Neuenstein (1914) gives a systematic account
of alga nuclei; for recent literature, see Smith (1933). Agar's (1920) book on cytology
is chiefly an account of the structure and behavior of the metazoan nucleus.

48

THE NUCLEUS 49

nuclei produced by repeated division, as in the Siphonales and Phycomy-
cetes. In such a body a few partitions may be formed, giving cells with
varying numbers of nuclei, as in Cladophora (Fig. 4, C). Again, the
subdivision into cells may be very closely correlated with the division of
the nuclei so that every cell has one nucleus; this is the condition in the
majority of organisms. Frequently, cells with two or more nuclei occur
regularly in certain tissues of plants with uninucleate cells elsewhere
throughout the body, as in the internodal cells of Characese, tapetal cells,
and a number of other instances in vascular plants.^ A peculiar con-
dition is found in the red blood corpuscles of mammals. These cells
are originally nucleated, and the later enucleate condition is usually
attributed to an actual loss or degeneration of the nucleus. In amphib-
ians the enucleate erythrocyte ("erythroplastid") arises by the division of
a nucleated cell without an accompanying nuclear division.^ Enucleate
leucocytic elements are also known. The nuclei of a protoplast, whether
many or one, are called the nucleome by Dangeard.

In certain infusoria two unlike nuclei are present: a small micro-
nucleus and a much larger macronucleus (Fig. 5). This is usually the
condition in Paramoecmm caudatum, but races with no micronucleus are
known."* Some species may have more than one micronucleus: in P.
woodruffi there are usually three or four, although the number varies
from none to eight (Wenrich, 1928a). The micronucleus divides mitoti-
cally and the macronucleus is usually said to divide amitotically, but at
least in some cases the story is evidently less simple than this (Mac-
Dougall, 1925). The macronucleus appears to be primarily a special
nutritive organ, showing decided alterations under changing environ-
mental conditions (Stolte, 1922). At certain intervals it is absorbed
completely and replaced by a new one derived by a process of division
from the micronucleus. C. V. Taylor (1923a), working with Euplotes,
observed that individuals from which the micronuclei had been arti-
ficially removed underwent only one or two more fissions and died in a
few days.

The position of the nucleus is determined largely by physical causes,
such as surface tension, the position of the vacuoles, and the relative
density of the cytoplasm in different portions of the cell. In a non-
vacuolate cell it ordinarily occupies the center of the cytoplasmic mass.
In a cell with vacuoles it is imbedded in the cytoplasm even when the
latter is reduced to a thin parietal layer; it never lies free in the vacuole.
Its position is also related to the functions of the cell ; generally speaking,

- Arber (1920). A historical review of known cases is given by Beer and Arber
(1920). See also Tischler (1921-1922, pp. 212if.)
3 Beyer (1921), Emmel (1924, 1925).
^Landis (1920), Woodruflf (1921).

50

INTRODUCTION TO CYTOLOGY

Fig. 21. — Position of
nuclei in differentiating
cells. A, thickening of
inner wall of epidermal
cell of Scopolia. B, origin
of root hairs in Pisum.
{After Haberlandt.)

it lies in the region characterized by the most active metabohsm.^ For
example, in young, growing root hairs and pollen tubes it is commonly
found a short distance from the elongating tip. Wendel (1918) observed
that the root hairs of Sinapis alba seedlings grow first at the apex, then at
the base, and sometimes at the apex once more, and that the position of
the nucleus changes accordingly. In thickening epidermal cells (Fig. 21)
it frequently, though not always, lies near the wall upon which the thick-
ening material is being deposited.

In form the nucleus is typically spherical or ellipsoidal, its shape,
like its position, being determined by a number of physical factors.

Under comparatively uniform condi-
tions, as where a small nucleus lies in
a relatively large amount of non-
vacuolate cytoplasm, a spherical shape
is ordinarily assumed. Exceptions are
often seen in cells with specialized func-
tions. In the cells of the spinning glands
of Pieris and Vanessa (butterflies) the
physiological conditions lead to the as-
sumption of very irregular forms w^here-
by the nuclear surface is considerably
increased (Fig. 22). Analogous changes
occur in Lilium bulb cells (Goldstein,
1928). Nuclei seem rather commonly to
undergo amoeboid changes in shape, such
active movement being directly observa-
ble in the nucleus of the living cycad spermatozoid. In the long, narrow
cells of vascular bundles the nuclei, which are not free to grow in all
directions, come to be correspondingly elongated. In Stentor and
Spirostomum the nucleus has the form of a string of beads (Fig. 22, B).^
Nuclei show a wide variation in size, ranging in plants from extremely
minute nuclei like those of Mucor, 1/x or less in diameter, to the relatively
gigantic nucleus of the Dioon egg, with a diameter of 600;u. A similar
range is seen in animal nuclei. Although the nuclei of the fungi are
characterized by small size, most of them being less than 5jLt in diameter,
they may grow to be very large at certain stages. The primary nucleus
of Synchytrium, for instance, reaches a diameter of over 60/x. The major-
ity of nuclei, however, fall between 5 and 25ju. In spite of the wide range
in the size of nuclei of different organisms, it is generally uniform in a

^ This relation of position to function was emphasized in the works of Haberlandt
(1887) and Gerassimow (1890, 1899, 1901).

8 A discussion of the various factors influencing nuclear shape is given by Champy
and Carleton (1921). Tischler (1921-1922) and Goldstein (1928) describe many
unusual forms of nuclei. Tischler gives a long list of measuraments of plant nuclei.

THE NUCLEUS

51

given tissue, though it may vary considerably with the physiological
activity (Maige, 1923).

The ratio of the volume of the nucleus to that of the cytoplasm in a
ceU is called the " nucleoplasmic ratio," or " karyoplasmic ratio." Many
years ago it was held by Sachs and Strasburger that the size of a meri-
stematic plant cell maintains a very definite relation to the size of the
nucleus, owing to a supposed limitation of the sphere of influence of the
nucleus. This latter conception has been emphasized anew by Winkler,
and parallel views have been expressed by several zoologists.'^ In the
case of certain terminal meristems of plants such a rule may well hold

r.i-y--

■*■■ I jftv '•*^^ ■■

Fig. 22. — Peculiar nuclei. A, portion of nucleus from spinning gland of Vanessa
urticw. {After Korschelt, 1896.) B, Spirostomum ambiguum, with moniliform nucleus.
{After Stein.) C, nucleus from salivary gland of Chironomus; the chromatic material
is in a convoluted thread which ends in two nucleoli. {After Balhiani, 1881. See also
van Herwerden, 1910, 1911; Aherdes, 1912; Faussek, 1913; Tamer, 1921.) D, Chwnia
teres, with chromatic granules scattered throughout the body. {After Gruber, 1885.)
E, lobed nucleus from yellowing lily leaf. {After Goldstein, 1928.)

true within limits, but the condition reported by Bailey (1920) in the
lateral meristem (cambium) shows clearly that it cannot have universal
application. The cambial initials may vary enormously in size with no
corresponding variation in the size of their nuclei; two such initials, one
of them having many hundreds of times the volume of the other, may
possess nuclei of approximately equal size. Tischler (1924, 19256)
connects the ratio in pollen with the process of germination. The
nucleoplasmic ratio has figured prominently in discussions of the problem
of senescence and differentiation.^

In a given kind of cell there is a relation between the size of the nucleus
and the number of chromosomes. In 1895 Boveri showed that the size

7 Sachs (1892, 1893, 1895), Strasburger (1893), and Winkler (1916) on plant cells;
DoUey (1913) on nerve cells; Hegner (1919) on Arcella; Hegner and Wu (1921) on
Opalina; Dolley (1925) on pancreatic cells.

» R. Hertwig (1889, 1903, 1904, 1908), Minot (1891, 1908, 1913), Conklin (1912),
Child (1915), Popoff (1907), Marcus (1908), Howard (1910), Howard and Schultz
(1910). See Wilson (1925, p. 236); also Faure-Fremiet (1925).

52 INTRODUCTION TO CYTOLOGY

of the nuclei in merogonic echinoderm larvae is dependent upon the num-
ber of chromosomes each contains. In a more extended study (1905) he
demonstrated that it is the surface of the nucleus that is proportional
to the chromosome number, and also that the size of the cell is propor-
tional to both. Gates (19096), however, adduced evidence to show that
this rule is by no means universal. This question has been investigated
in connection with studies on polyploid plants with the general result
that, although in the majority of cases a rise in the chromosome number of
a species is seen to be accompanied by an increase in nuclear and cell
size, there are cases in which such a change in related types seems to have
been accompanied rather by a decrease in the size of the chromosomes.
This indicates that it is volume of karyotin, and not mere number of
chromosomes, that is of importance in this connection (see Tischler,
1921-1922, pp. 588^.).

With respect to the physical nature of the nucleus as a whole, studies
with the micromanipulator have shown^ that it ordinarily consists, at
least in part, of an elastic gel having a higher viscosity than that of the
cytoplasm, often being so firm that it can be handled without injury by
the instrument. This obviously would be impossible were the nucleus
merely a watery droplet or vesicle in the cytoplasm. The germinal
vesicle (nucleus) of certain animal eggs Chambers finds to be a sol droplet
with a gel membrane; when pinched in two by the instrument the two
halves will reunite if they come in contact.

Studies on the electrical properties of cells have shown that the
nucleus is apparently negative to the cytoplasm. Free nuclei and the
heads of spermatozoa, which are composed almost entirely of nuclear
material, pass to the anode in an isotonic cane-sugar solution; whereas,
cells rich in cytoplasm, such as large leucocytes, pass to the cathode. ^°
The difference in electrical potential ,on the two sides of the nuclear
membrane may be of considerable significance in the vital processes.

The chemical nature of the nucleus has been touched upon in the
preceding chapter (p. 26). The exact nature and distribution of the
various constituents are not well known, but recent researches'^ seem to
show that the reticulum contains both nucleo-protein and lipide, the
latter being in part combined with protein, while the karyolymph con-
tains lipides but no nucleo-protein. The most nearly specific test so
far devised for the chromatic nucleo-protein ("chromatin") of nuclei
is the Feulgen reaction, in which the production of a purplish color in
decolorized basic fuchsin indicates the presence of thymonucleic acid.'^

8 Kite (1913), Chambers (1914, 1917, 1921), Seifriz (1926c).
i« R. S. Lillie (1903), Hardy (1913).

11 Nemec (1909, 1910), Hansteen-Cranner (1919), Grafe (1925), Grafe and Magis-
tris (1926), Wermel (1927), Gutstein (1927), Shinke and Shigenaga (1933).

12 Feulgen and Rossenbeck (1924), Feulgen (1926). See also McClung's Micro-
scopical Technique and Margolena (1932).

THE NUCLEUS 53

The limitations of this method are not altogether clear, but it has already-
proved valuable in distinguishing chromosomal matter from other sub-
stances which stain like it with certain dyes. Most investigators have
found that vital dyes do not stain the nucleus as long as it is living and
healthy, but P. Dangeard (1923a) reports that nuclei in certain cells with
a somewhat retarded activity may be so stained with neutral red and
methyl violet. Successful results are reported by several other workers. ^^

Structure of the Nucleus. — The typical nucleus is bounded by
a nuclear membrane. The reality of this membrane has often been
questioned, but researches on living cells^^ leave no doubt that it is a
definite structure. It is usually very thin; it has even been suggested
that it may sometimes be but a single layer of molecules. In most cells
under the micromanipulator it appears, however, to be thicker, remaining
intact when the nucleus is pushed and pulled about or removed from the
cytoplasm, and crumpling into folds when fluid is withdrawn from the
nucleus with a pipette. Its origin with respect to the regions which it
separates is obscure. The suggestion has been made that it is double,
having distinct nuclear and cytoplasmic components. ^^

The larger portion of the volume of most nuclei is composed of a
highly transparent ground substance known as karyolymph, or "nuclear
sap." This usually appears optically homogeneous, with a few" dispersed
particles at most. The results of microdissection and the Brownian
movement of suspended particles show that it may be in either the sol
or the gel state. In old cells vacuole-like masses may appear within it
(Kisser, 1922).

Associated with the karyolymph is another substance which appears
in most preparations as a more or less continuous network of threads, the
reticulum. The naturalness of this structure has also been a subject of
debate. Many living nuclei, notably in animals, appear perfectly
homogeneous (excepting the nucleolus) or at most very finely granular,
a reticulum appearing gradually as the nuclei are injured experimentally
or allowed to become moribund. ^^ The coarseness and the uniformity
of the reticulum often vary considerably with the fixing agent employed ;
moreover, the coagulation of colloidal substances very commonly involves
the formation of fibrous and reticulate structures. It has accordingly
been inferred that the thready reticulum has no real existence in the
normal living state but represents an artifact brought about by altera-
tions in the nuclear colloids.

i^Kuster (19186, 1926), Gicklhorn (1927), Paltauf (1928), Albach (1928). The
reactions of plant and animal cells to vital dyes are compared by Benoist et al. (1929).

^* Kite, Chambers, C. V. Taylor, Gross, Nemec.

i^Scarth (1927), Klingstedt (1928).

"Lewis and Lewis (1924), Chambers (1924), Schaede (1925, 1930), Strugger
(1930).

54

INTRODUCTION TO CYTOLOGY

Opposed to the general validity of the foregoing interpretation are
the results obtained by a number of investigators^^ who have seen threads
or a reticulum in apparently healthy nuclei under carefully controlled
conditions of observation (Fig. 23). Martens, for example, working with
the plumose stigmas of Arrhenatherum, stamen hairs of Tradescantia, and
certain other tissues, watched the action of fixing fluids upon living nuclei

and found that the reticulate structure visible in
healthy nuclei before fixation remained unchanged,
except for a slight swelling of the threads and
increased visibility due to alterations in refractive
index. The same details appeared in material fixed
for longer periods and stained with iron alum-
hsematoxylin. These results, taken together with
analogous findings of Chambers (1924, 1925) on the
prophases in animal spermatocytes, indicate that the
reticulum appearing in a well-fixed nucleus fairly
represents a delicate thready structure actually
present during life and rendered more distinctly
visible by fixation. It is doubtless true that no fixer
gives a wholly perfect rendition of all details of the
living structure and that many fluids produce very
great alterations, but it now seems evident that the
reticulum cannot be explained away as merely a crea-
^g^ tion of technical procedures.

The reticulum is composed of threads. On the

crooked chromonem- ^ • i- • ^ j_ ^ x i • r^\ j. -v -j.

ata. {Photograph ftir- basis of evidence to be presented m Chapter X, it
nished by H. Teiezyn- may be Said that thcsc threads occur in a charac-
teristic number and are derived each from the
filamentous constituent (chromonema) of a chromosome. They appear to
be connected laterally by fine strands {anastomoses) about whose origin
and nature very little can be confidently affirmed (see p. 135). Since the
main threads tend to be crooked and not appreciably thicker than their
connecting strands, it is difficult or impossible to recognize them as indi-
viduals in the fully developed reticulum. They are characteristically
chromatic: they usually stain well, particularly with certain basic dyes
(basichromatism) and so offer a strong contrast with the achromatic
karyolymph. In some nuclei the threads are rather evenly basichromatic
throughout, the reticulum appearing as a system of uniform strands with
only slight swellings here and there, especially at the nodes. In other
cases the chromaticity may be more pronounced in the swellings, the
other regions of the threads being relatively colorless or even oxychro-

i^Lundegardh (1912a), Kite (1913), de Litardiere (19216), Martens (1924, 1927a6c,
19296), Scarth (1927), Belaf (19296, 1930), Guilliermond (1930o), Telezynski (1930),
Belling (1933).

Fig. 23. — Living nu
cleus in Tradescantia
stamen hair moun
in paraffin oil. Note

THE NUCLEUS 55

matic (stainable with acid dyes). In such cases the appearance of the
reticulum suggests a framework of one substance supporting differently
stained particles of another substance

The interpretation of the above appearances has long been a major
cytological problem, and no acceptable conclusion has yet been reached
with regard to many points. The view was long ago put forward that the
reticulum comprises two distinct elements: a supporting framework
composed of relatively achromatic linin upon or in which are carried
''granules" of a second, highly stainable substance, chromatin. The
chromatin granules were held to be composed of " oxychromatin " or
"basichromatin" according to their varying ratio of nucleic acid and
protein. '^^ Thus the "chromatin" may be highly basichromatic (strongly
acid) during nuclear division, but only weakly so or even oxychromatic
(basic in reaction) in the metabolic nucleus where it is in a different
functional state with its nucleic acid presumably combined with basic
substances. At all stages it reacts positively to the Feulgen test (p. 52).
Physical factors, such as degree of dispersion, as well as the order in
which stains are applied, may also affect the results obtained in
preparations.^^

The evidence for such a structural distinctness of chromatin and
achromatic supporting material in the reticulum has been questioned by
many workers. 2° It has been suggested that if there are two elements,
chromatin and linin, they are not so distinct morphologically as the
earlier workers supposed, the chromatin existing rather as a thin fluid
impregnating the linin substratum. The chromatic lumps are often not
sharply set off from the rest of the thread but taper off gradually. In
such cases it has been found that purposes of cytological description are
well served by the conception of a reticulum composed of a single com-
plex substance which stains variously in different regions and at different
stages of the nuclear cycle according to the size of the strands, their
physico-chemical state, and the technical procedure employed. This
one substance is loosely spoken of as chromatin, but because of the long
application of this term to a supposedly distinct component of the retic-
ulum it is advisable to use Lundegardh's (1910) term karyotiji for the
reticular substance as a whole. Only future research can decide whether
karyotin ("chromatin" in the wide sense) is a true chemical compound

1* Heidenhain (1890, 1907). As used by many writers, the term "oxychromatin"
includes the Hnin, "chromatin" denoting only the "basichromatin." Heidenhain
later called the chromatin granules "chromioles," a term introduced by Eisen (1899).
See the discussions by Wilson (1925) and Stieve (1921). Oes (1908, 1910) and
Nemec (1909, 1910) reported that the two kinds of chromatin differ in solubility.

" A. Fischer (1899), Hardy (1899).

2° Gregoire and Wygaerts (1903), Gregoire (1906), Sypkens (1904), Martins-
Mano (1904), Lundegkrdh (1910, 1912), Malte (1910), Sharp (1913, 1920a), de
Litardiere (19216), McClung (1924).

56

INTRODUCTION TO CYTOLOGY

or a looser combination of two or more constituents, only one of which is
"chromatin" (in the narrow sense).

In nuclei with more sharply differentiated chromatic lumps and
achromatic connecting strands the conception of two substances in the
reticulum may seem more attractive. Studies on the chromosomal
threads (chromonemata) during nuclear division have shown that the
lumps {chromomeres) may be located in definite positions in the threads,

which in such a case have characteristic structural
patterns (Fig. 79). Certain of the large lumps have
been identified in the reticulum, and it is inferred
that the small ones may also persist in some measure.
Hence such chromomeres can scarcely be chance
accumulations of chromatic matter; they are definite
differentiations which there is much reason to believe
are associated in some way with certain functional
activities. They might be regarded as local swellings
of the karyotin (one-substance theory) or as regions
where "chromatin" is produced in characteristic
amounts (two-substance theory). It may be that
we shall come to look upon "chromatin" not as a
substance existing primarily as definite units but
rather as one whose presence indicates activities in

^^^

I

Fig.

B

24.-

Kuhn, 1929a.) B, nu-
cleus of Impatiens in
prophase, showing eu-
chromocenters at spin-
dle-attachment regions
of developing chromo-
somes. (After Gregoire,
1932.)

cieus of Phaseoius with other localized units or regions in the nuclear threads.

chromocenters. (After

The above uncertainties do not prevent us from
carrying forward the conception of the reticulum as
a system of chromosomal threads connected by fine
strands, or from speaking of the reticular substance
in general as karyotin. As will be made evident
in later chapters, the nucleus may be regarded as a
group of closely associated chromosomes performing their metabolic
functions together.

In many nuclei there are at certain stages one or more conspicuous
masses of karyotin at several points in the reticulum (Fig. 24). Of
the many terms applied to these the most suitable seems to be chromo-
centers.^^ After certain stains (iron alum-hiematoxylin) they may at
times closely resemble true nucleoli, but the distinctness of the two was
long ago demonstrated with other stains (Rosen, 1892). In some
cases it has been shown that they represent definite chromosomal regions
which remain condensed and highly chromatic ("heteropyknotic")

21 Baccarini (1908). They have been variously known as net knots (Flemming,
1882), karyosonies (Ogata, 1883), pseudonucleoli (Rosen, 1892), Nebennucleoli (Zacha-
rias, 1895), and chromatin nucleoli. Karyosome is a widely adopted term, but the
fact that it has been applied to other quite different elements has made the substitu-
tion of another term advisable.

TllE NUCLEUS 57

instead of forming portions of the reticulum. ^^ These euchromocenters
appear to correspond in part to the "prochromosomes" which many
writers have pointed out as regions at which prophasic chromosome con-
densation begins. In other cases chromatic accumulations may arise
secondarily in the metabolic nucleus and disappear without showing any
direct connection with chromosome development (Kuhn, 1929a).

The Nucleolus. — Nearly all metabolic nuclei contain one or more
trae nucleoli, or plasmosomes.^^ In a young nucleus just formed by divi-
sion there are often several small nucleoli which may unite to form two
or one as the nucleus becomes fully developed. In the living nucleus
the nucleolus appears as a dull, viscous droplet, usually round but
frequently irregular in shape. Centrifuging-^ and the position it natu-
rally assumes in certain eggs-^ show it to be heavier than the rest of the
nuclear matter. It may be homogeneous throughout, or it may contain
vacuole-like masses and occasionally small granules.-'' Chemically,
it is composed mainly of proteins and lipides.-^ It commonly shows an
affinity for acid dyes, but in some procedures it takes the basic ones.
Of greater interest is the fact that its chromaticity undergoes marked
alterations during the nuclear division cycle, as will be pointed out in later
chapters. Such alterations are thought to indicate interactions of some
sort with the reticulum, with which the nucleolus is in contact at one or
more points. The broad, clear zone often seen about the nucleolus in
fixed material is, as a general rule, an artifact due to a contraction of the
reticulum.

The functions of the nucleolus are obscure, but there is obviously
some relation between its behavior and the cycle of alterations undergone
by the other nuclear constituents. This topic is to be discussed in Chap-
ter IX. It should, however, be pointed out here that the nucleolar
matter arising in the young nucleus develops principally in close associa-
tion with definitely localized regions of particular chromosomes, a fact
which has only recently come to light (p. 118). The nucleolus or nucleoli
tend to remain attached to such chromosomes and consequently to the
metabolic reticulum which the latter form. As the reticulum again

22 Strasburger (1904c), Miyake (1905a), Rosenberg (19076, 1909ac), Overton
(1905, 1909), Laibach (1907), Heitz (1929a), Gregoire (1932). These are called
euchromocenters (true chromocenters) by Gregoire.

23 por general accounts of the nucleolus and reviews of the literature pertaining
to it, see Montgomery (1899), Wager (1904), Walker and Tozer (1909), M. Jorgensen
(1913a), A. Meyer (1917a, 1920), Tischler (1921-1922), Ludford (1922a), and Guillier-
mond and Mangenot (1928).

2* Mottier (1899), F. M. Andrews (1902), E. W. Schmidt (1914), Nemec (1929/),
Shimamura (1929).

25 Gray (19276) on Echinus, Wakayama (1929) on Pinus.

26 Digby (1910), Reed (1914), Kuwada (1919), Carleton (1920), Saguchi (19206).
2^ Zacharias (1885), A. Meyer (1920), Unna and Fein (1921), Fels (1926), Shinke

and Shigenaga (1933).

58 INTRODUCTION TO CYTOLOGY

develops condensed chromosomes, the nucleolar matter diminishes in
amount and commonly disappears completely. This long ago suggested
that it is with the chromosomal changes especially that the nucleolus is
concerned.-^ Kossel suggested that the albuminous nucleolar material
arises as one of the products formed when complex albumin-rich com-
pounds are spht to form albumin-poor "chromatin."

Less evident are certain other functions which have been ascribed to
the nucleolus. It has often been regarded as a reserve material utilized
in some unknown manner by the protoplast.^^ To Strasburger (1895) its
behavior suggested a connection with the development of the achromatic
structures at the time of nuclear division (Chapter XI). Others have
made observations suggesting a role in secretion^" or yolk formation^^ in
animals. The evidence in a number of such cases has been adversely
criticized. ^-

The Functions of the Nucleus. — Many years ago Claude Bernard
(1878) suggested that the nucleus is necessary for synthetic metabolism.
Since that time various investigators^^ have sought to test this hypothesis
by experiments on plant cells artifically deprived of their nuclei by means
of plasmolysis, centrifuging, direct section, cooling, or anesthesia. It
was observed that in these cells such activities as the formation of
cellulose membranes, assimilation, the utilization of reserves, growth, and
the division of plastids ceased at once or continued for only a short time.
The general conclusions were that these activities depend upon the pres-
ence of specific substances (building materials, enzymes, etc.) in the
cytoplasm, that such substances are elaborated with the cooperation of
the nucleus, and that the occurrence or non-occurrence of the activities
in question in enucleated masses of cytoplasm depends upon the presence
or absence of these substances at the time of the experiment.

Analogous results have been obtained in certain experiments on
amoebae,^'* which can be cut into nucleate and enucleate pieces. The

28 Flemming (1882), Strasburger (1884), F. M. Andrews (1901), Rhumbler (1893),
R. Hertwig (1898), Lubosch (1902), Farmer (1907), Sheppard (1909), Maziarski
(1910), Reed (1914), Schiirhoff (1918), Digby (1919), de Litardiere (19216), Ludford
(1922a), Cleland (1922, 1924), Lenoir (1923), Martens (1922), Van Camp (1924),
Latter (1926, 1932), Gates and Latter (1927), Zirkle (19286, 1931).

29 M. Jorgensen (1913a), A. Meyer (1917, 1920), and many others.

s« Macallum (1891), Maziarski (1911), Nakahara (1917, 1918a), Saguchi (1920),
Kinney (1926), Beams and Wu (1929).

31 Macallum (1912), Lubosch (1902), Rohde (1903), Ludford (1921, 1922a),
Koch (1925), Gardiner (1927), Nath and Mehta (1929), Nath and Mohan (1929).

32 M. Jorgensen (1913a), A. Meyer (1917, 1920), de Winiwarter (1925).
33KIebs (1887, 1888), Haberlandt (1887, 1919, 1921), Gerassimow (1890 et seq.),

Townsend (1897), Palla (1889, 1890, 1906), Acqua (1891, 1910), van Wissehngh
(1909), BobiUoff-Preisser (1917), Heitz (1922). See Tischler (1921-1922; pp. 142-
147).

3" Stole (1910), Lynch (1919), Phelps (1926), Becker (1926).

THE NUCLEUS 59

enucleate pieces may move, respire, and respond to certain stimuli —
activities which depend upon catabolic processes; but they do not undergo
regeneration, growth through the formation of new albuminous material,
or division — activities which involve organic synthesis.

Among the many reactions involved in metabolism the most impor-
tant, according to modern physiology, is oxidation, for the energy utilized
by the organism is derived immediately from the union of protoplasm or
of its inclusions with oxygen. A relation between the nucleus and oxida-
tion and reduction has therefore been sought.

Following the experiments of Spitzer (1897), who observed that
nucleo-proteins extracted from certain animal tissues have the same
oxidizing power as the tissues themselves, it was suggested by Loeb
(1899) that the nucleus is the center of oxidation in the cell. Loeb
pointed out that this would explain the inability of enucleated cell-
fragments to undergo regeneration. This conclusion was supported by
R. S. Lillie (1903, 1913), who showed that rapid oxidation occurs both
at the surface of the cell and at the surface of the nucleus. Osterhout
(1917) found that "injury produces in the leaf-cells of the Indian Pipe
(Monotropa uniflora) a darkening which is due to oxidation. The oxida-
tion is much more rapid in the nucleus than in the cytoplasm and the
facts indicate that this is also the case with the oxidation of the uninjured
cell." Other investigators^^ have opposed the oxidation theory. Fur-
ther evidence in its support is brought forward by Chambers (1923a).
In healthy cells (amoebae, ciliated cells, echinoderm eggs) Janus green
does not enter the nucleus, but as the cells become moribund the dye
enters and colors the reticulum red. This probably means that the nor-
mal resistance to the penetration of the dye is lost, whereupon the reduc-
ing ability of the nucleus becomes manifest in the change of Janus green to
diethylsafranin. This reducing power is lost at death.

In interpreting the results of such experiments, particularly those
in which the cell is enucleated by mechanical means, it has not always
been sufficiently borne in mind that some of the effects upon metabolism
may be due to the injury itself rather than to any sort of normal activity
in the parts which remain. It is therefore very difficult to obtain by
such direct means unequivocal evidence regarding the precise manner in
which the nucleus functions during the normal life of the cell. Even
when the results of enucleation seem clearly to indicate a dependence
of certain functions on the nucleus, they do not limit to the nucleus
the performance of those functions. Removal of the cytoplasm would
also cause a cessation of such activities. Each function, though it
may be peculiarly subject to the differential influence of some one
organ, is, in reality, an act of the protoplasmic system as a whole. The
nucleus may be said "to control" an activity only in the sense that

s^Lynch (1919) on Amoeba, Wherry (1913), W. Schiiltze (1913), Reed (1915).

60 INTRODUCTION TO CYTOLOGY

it contains something necessary to the performance of that activity,
much as a chemical stockroom "controls" the activities carried on in the
laboratory.

In a mature organism metabolic activity maintains the individual in
the living condition. In a young and developing one it also results in
growth and the differentiation of structural and functional characters.
The manner in which the various constituents of the protoplast partici-
pate in metabolism and hence affect the course of development is studied
by observing the effects of altering this or that constituent. In the case
of the nucleus it has been found that differences in its constitution are
associated with particularly clear-cut differences in certain of the char-
acters developed. This leads to the subject of the role of the nucleus
in development and heredity, which is to occupy our attention in later
chapters of the book.

CHAPTER IV

PLASTIDS

The most conspicuous cytoplasmic differentiations in plants are
plastids. They may be looked upon as regions of the protoplast which
have become structurally specialized mainly in connection with carbohy-
drate synthesis and transformation; hence they serve to call attention to
one of the most profound metabolic differences between plants and ani-
mals. The total plastid outfit of the protoplast has been called the
plastidome by Dangeard."^

Occurrence and General Characters. — Plastids are of almost universal
occurrence in the tissues of plants, where they are found in one form or
another in all groups with the possible exception of bacteria, blue-green
algae, myxomycetes, and certain fungi. Within a single cell there may
regularly be but one plastid, as in many algae, Aiithoceros, and the meri-
stematic cells of Selaginella; or two, as in Zygnema; or a higher number,
as in the green tissues of most higher plants. They lie imbedded in the
cytoplasm and are often closely associated with the nucleus; they are
never found normally in the vacuole. The positions which they assume
within the cell are frequently related in a definite manner to certain
external conditions, as in palisade and stomatal cells of green leaves. ^

Although they may vary considerably in size, Mobius (1920) found
that 75 per cent of the plastids in 215 species of plants he examined
had a long diameter lying between 4 and 6^. The size may be affected
by temperature (0. Hartmann, 1919a). It seems that in some cases there
is a relation between the size of the plastids and that of the cells in
which they lie (Gates, 1923). Eyster (1929) observed characteristic
size differences in certain genetic strains of maize.

Plastids are usually classified on the basis of the colors of their con-
tained pigments. The arbitrary nature of such a classification is
apparent when it is realized that two plastids of the same color, or with
no color whatever, may be performing very different functions by virtue
of unlike substances not visible to the eye; and, further, that the same
plastid may be colorless, green, and yellow or red at different stages in its
history. A separation on the basis of color is, however, very convenient
and usually does correspond to functional diversity. This is shown by

1 For general accounts of plastids, see A. Meyer (18836), Schimper (1883, 1885),
Senn (1908), and Schvirhoff (1924).

2 Schimper (1885), Senn (1908), Haberlandt (1918), Weber (1925a).

61

62

INTRODUCTION TO CYTOLOGY

the interesting fact that the thallophyte groups with different predominat-
ing pigments are characterized by different principal products of metaboHc
activity. In the higher plants and the grass-green algse this product is
usually starch, in the yellow-green algse and diatoms it is oil, in the brown
algse it is pentosan, in the red algae (Floridese) it is Floridean starch, and
in the blue-green algae it is glycogen.

Leucoplasts. — All colorless plastids, regardless of their size, function,
or relation to other types of plastids, are known as leucoplasts (Fig. 25).
They are found commonly in meristematic tissue and may be retained

<ij(

e

^0

tV

©

f#

9

'^±<3

0O

.e

a

4 dO^^

\v-

V

g

^

"J.

\

\

O'

h

Fig. 25. — Leucoplasts in root cells, a-e, Yicia Faba; f, g, Pisum sativum; h, Hyacinthus
orientalis. The smaller bodies in b are chondriosomes. The light material in the enlarging
leucoplasts is starch. {After Bowen, 1929a.)

in some kinds of differentiated cells, such as the glandular hairs of
Pelargonium. The leucoplast in Orchis is of a very fluid consistency,
undergoing amoeboid changes of shape and multiplying by irregular
fission (Kiister, 1911). In Polytoma uvella it forms a reticulum or series
of bands (Volkonsky, 1930). Many smaller leucoplasts represent juvenile
stages in the development of plastids of more highly differentiated types,
for under certain conditions they develop into the larger and more special-
ized leucoplasts known as amyloplasts (Fig. 28, C) and into the various
kinds of chromoplasts mentioned below.

Chromoplasts. — Chromoplasts are plastids bearing one or more
pigments. They are frequently called "chromatophores, " but, since this

PLASTIDS

63

term has been used with special reference to the plastids of algae and also
for certain pigmented cells in animals, chromoplast is preferable as a gen-
eral term for all colored plastids.^

Of all chromoplasts the most familiar is the chloroplasl, whose color
is due to the presence of the green pigment chlorophyll. Chloroplasts
are usually spherical, ovoid, or discoid in shape, but many bizarre forms
are known particularly among the green algse. For example, in (Edo-

s

O H 1 J K L

Fig. 26. — Various types of plastids. A, CEdogonium, showing pyrenoids and stroma
starch. B, Leptonema fasciculatum. C, PilayeUa varia. D, Rhodochorton floridulum.
E, F, Euastrum dubium, front and side views. G-L, Hyalofheca mucosa, showing division of
plastid and pyrenoid with its surrounding starch masses. {From the works of Schmitz,
Reinke, Kuckuck, and Carter.)

gonium the plastid has the form of an irregular net, while in Spirogyra it is

a coiled ribbon and in desmids a series of radiating plates (Figs. 26, 27).

The plastid of Anthoceros is spindle shaped and becomes chainlike in

elongated columella cells (Scherrer, 1914). Chromoplasts are often

sharply angular, owing in part to the presence of crystals.

It has been reported for several algae that the chlorophyll is diffused

throughout the cytoplasm, not being confined to definite plastids. In

the case of Hydrodictyon, however, Lowe and Lloyd (1928) have shown

that chloroplasts can be detected by the use of light lying in the region of

the absorption bands of chlorophyll.

^A more common practice is to limit the term "chromoplast" to plastids with
colors other than green, the chloroplast ("autoplast," Meyer) being placed in a class
by itself. For accounts of chromoplasts in this sense, see Rothert (1912) and A. Meyer
(1926),

64

INTRODUCTION TO CYTOLOGY

The most important of all plastid pigments is chlorophyll, because of
its peculiar relation to the elaboration of carbohydrates by chloroplasts.
Chlorophyll ordinarily develops in the plastid only in the presence of light;
apparent exceptions are found in certain woods and the embryo and endo-
sperm of certain seeds. Other conditions necessary for the development
of chlorophyll are a favorable temperature and the presence of iron,
oxygen, and certain carbohydrates. Most young seedlings grown in the
absence of light show a pale yellowish color. When such
"etiolated" plants are placed in the light, the plastids
become green, apparently through an alteration of "chloro-
phyllogen" to chlorophyll. There is a close chemical
relationship between chlorophyll and the haemoglobin of
animal blood.

With chlorophyll are usually associated one or both of
the yellow carotinoid pigments carotin and xanthophyll.
The exact mutual relation of the several pigments in the
chloroplast is uncertain, some investigators thinking it
probable that a single green compound decomposes readily
into "chlorophyll a," "chlorophyll 6," and other products
when subjected to analysis (Lubimenko). In the algae
Cell of Spiro- Other pigments, notably brown phycophsein and fuco-
gyra, with spiral xanthin, red phycoerythrin, and blue phycocyanin.
The nucleus is occur in addition to chlorophyll, though in the case of the
suspended in the blue-green algsB there is some question concerning the
by a series of limitation of pigments to plastids (Chapter XIII). Red
cytoplasmic and yellow pigments may develop either in the leucoplasts
meet the pe- directly or in chloroplasts as the chlorophyll disintegrates
rip herai cyto- (Meyer). In tomatoes the red lycopin, an isomer of
the pyrenotds! carotin, appears in the chloroplasts as the fruit ripens.
{After Couch, The colors of flower petals are in some cases due to plastid

1 Q*^ 1 /i ^

pigments. In Nasturtium, for example, the yellow color
is in chromoplasts, but red pigment in the same flower is held in solu-
tion in the cell sap.*

Photosynthesis. — Of all chromoplasts the chloroplasts stand first in
importance, for by virtue of their chlorophyll they are able, in the pres-
ence of light, to recombine the elements of carbon dioxide and water in
such a way as to form certain carbohydrates, oxygen being given off as a
by-product. In this process the energy of sunlight is fixed, while in
respiration this energy is again released for use by the organism. Repre-

^ For accounts of plastid pigments, see the works of Palladin (1923), Onslow (1923),
R. W. Thatcher (1921), Beauverie (1919), Willstatter and Stoll (1913), Jorgensen and
Stiles (1917), Haas and Hill (1928), Rigg (1924), Oltmanns (1923), Palmer (1922),
Fulton (1922), Lloyd (1924), Mobius (1927), and Gortner (1929). The distribution
of carotin is discussed in an earlier paper by Tammes (1900).

PLASTIDS

65

senting the energy involved in terms of calories, the reactions may be
written as follows (Gortner) :

Photosynthesis: 6CO2 + 6H2O + 677.2 calories = CeHiaOe + 6O2.
Respiration: CeHiaOe + 6O2 = 6CO2 + 6H2O + 677.2 calories.

The carbohydrate first elaborated is presumably in solution and there-
fore invisible. In many plants this product either accumulates in the
dissolved state or is removed from the chloroplasts as
fast as it is formed. Very commonly, however, there
is a temporary excess, which is deposited as minute
granules of starch in the chloroplasts. This "assimila-
tion starch" is therefore the first visible product of
photosynthesis in most green plants; in some species
the product is evidently an oil. As Meyer originally
showed, the starch is actually synthesized within the
body of the chloroplast (Fig. 28, A). It is later trans-
formed through the agency of enzymes into some solu-
ble compound, usually a sugar, in which form it may
be carried to growing regions where, after further
changes, it is built into the structure of the plant, or it
may pass to storage organs where it is transformed
into "reserve" or "storage" starch. This deposition
of reserve starch is brought about through the agency
of amyloplasts, which are leucoplasts capable of chang- piastids. A, dividing

1111,1 ■ J. • 1 u chloroplasts of Fu7i-

mg already elaborated organic materials, such as ^^^^ ^j^j^ ^^^^^^ ^^

glucose, into starch (Fig. 28, C). assimilation starch.

The statement made by Schimper (1880) and s^^XLTpiZtZTyg-
Meyer (1883, 1895) that starch is always formed by nema, with several
piastids still holds good in its essential feature: so far abo^^ a &e^ntrai^pyre-
as is certainly known, no primary product of photo- noid. (After Bour-
synthesis is formed in the cytoplasm apart from plas- copLt^ UmyiSpiitt)'
tids. The granules of "Floridean starch" in the red in tuber of Phajus
algse lie in the cytoplasm, but they begin to form at g7a'il'''^^f' reserve
the surface of the plastid as flat plates which become starch. {After Stras-
cup shaped or conical, with their flattened sides "'"^^''-^
remaining in contact with the plastid as long as they continue to grow.^
It is, however, reported that they are formed some distance away from
the piastids in some species (Mangenot, 1923a). If such is actually the
case, it is highly probable that they arise through the transformation of
a non-visible product (sugar?) of the photosynthetic activity of the pias-
tids, and are not immediately built up from water and carbon dioxide. A
similar interpretation may be placed upon corresponding appearances
reported in higher plants.

^Henckel (1901\ Kylin (1913).

Fig. 28.— Forma-
tion of starch by

66 INTRODUCTION TO CYTOLOGY

Elaioplasts. — Special plastids concerned in the elaboration of oil are
known in a number of angiosperms'' (Fig. 29). Kiister and Harper have
shown in the case of Ornithogalum that the plastid can be recognized
before oil appears in it, and that the abundant oil which is present later
may be extruded on its surface when the tissue is prepared for observa-
tion. Woycicki has observed the fusion of small elaioplasts containing
fat droplets to form a large "oleosome" with a central fat drop. In old
cells the oleosomes degenerate. Since oil may also occur as droplets
directly in the cytoplasm, Harper suggests that much of the current
difference of opinion regarding elaioplasts may be due to
the fact that among these bodies there may be transitional
forms between oily ergastic accumulations not causing
any cytoplasmic differentiation and definite cytoplasmic
organs in which the production of the oil is localized.
Some reported "elaioplasts" seem to be only groups of
disorganizing plastids with their products.
Eiaioplast " with '^^® Eyespot. — The so-called eyespot, or stigma, present
oil droplets in in the flagellates and in the zoospores and gametes of many
perianttTof'poZ?- ^^S* ^^^ Certain characteristics in common with plastids
anthes tuberosa; and may therefore receive consideration here. This body,
small pL^stids at which nearly all workers agree is a light-sensitive organ,
right. {After is an elongated or circular and flattened structure lying
in the anterior region of the cell (flagellates) or near its
lateral margin, usually in close association with the chromatophore and
the plasma membrane^ (Fig. 30). With respect to its mode of origin, it
has been variously reported to arise de novo in each newly formed zoospore
in several green algse (Overton), to multiply by fission at the time of cell-
division in flagellates (Klebs), to disperse as granules which reassemble in
the daughter cells in Euglena (Jahn), to develop from a plastid in the
antheridial cell in the case of the spermatozoid of Fucus,^ and to arise as a
differentiated portion of the plastid in the zoospores and gametes of
Zanardinia (Yamanouchi).

It is thought that the eyespot in many instances consists of a finely
reticulate stroma in which an oily red pigment with many of the charac-
teristics of hsematochrome is held in the form of minute droplets or gran-
ules.^ The stroma may also bear one or more refractive inclusions, which
in the Chlamydomonadaceae and Volvocace* consist of starch and in the
Euglenoideae of paramylum. These inclusions were thought by Franze to

« Wakker (1888), A. Zimmermann (1893), Raciborski (1893), Kuster (1894), Beer
(1909a), Politis (1914a), Guilliermond (19226), Harper (1929), W6ycicki (19296).

7 E. Overton (1889), Klebs (1883, 1892), L. N. Johnson (1893), Strasburger (1900a).
WoUenweber (1907, 1908), Hall and Jahn (1929).

sQuignard (1889), Mangenot (1920e, 1921), Kylin (1920).

8 Schilling (1891), Klebs (1883), Franze (1893), Wager (1900a), WoUenweber
(1907, 1908).

PLASTIDS

67

increase the sensitivity of the eyespot by concentrating the Hght at cer-
tain points.

Of a different type is the eyespot in the zoospore of Cladophora
(Strasburger, 1900a), which appears to arise as a swelHng of the ectoplast
and to consist of an external pigmented layer with a lens-shaped mass of
hyaline substance beneath it (Fig. 30, B). In
Gonium and Eudorina (Mast, 1916) the lens-
shaped portion lies outside with the cup-
shaped opaque portion under it (Fig. 30, A),
an arrangement suggesting the primitive eyes
of certain animals. In neither portion has
any finer structure been detected. Mast has
shown that the orientation of the colony is
brought about through changes in the inten-
sity of the light falling upon the light-sensitive
substance. As the unoriented swimming
colony rotates on its axis, those zooids turning
away from the light have the hyaline portion
of the eyespot shaded by the opaque cup ; this
sudden reduction in the amount of light energy
received brings about an increase in the
activity of the flagella of those zooids, so that pj^ 30.— Eyespots of vari-

the colony as a whole turns more directly ous types. A, zooid of Eudor-
ina; e, eyespot. {From Mast,
after Grave.) B, zoospore of
Cladophora. {After Strasburger,
1900.) C, anterior end of
Euglena viridis, showing eye-

strated about the chloroplast, although it spot at surface of oesophagus,

.I J J u Ai • 1 and near it a sweUing on one

appears to be surrounded by a thm layer .^^^ ^^ ^j^^ fiageiium; face
of modified cytoplasm.^" A prevalent view view of eyespot at right, show-
regarding the interior of the chloroplast is '^a»e^^'i900.)^'i?,"eyespo1^of

that it consists of a mass of somewhat denser Euglena velata. E, eyespot of
, „i ,1 , . I,- u J.U • 1- -J Trachelomonas volvocina, with

cytoplasm, the Stroma, m which there IS a hpide pjg^^^^ granules and crystal-
carrying chlorophyll. Starch granules appear loid body. {D and E after
at one or more points in the stroma; hence '■"'^^'''
after fixation the chloroplast may appear like a hollow sphere, a
honeycombed mass, or a series of threads or plates separating lighter
regions (Fig. 31) in which starch may be demonstrated. It is claimed by
Zirkle that one or more such regions, or "cavities," are present before
starch appears in them and that they communicate with the exterior
through fine pores (Fig. 32).

Because of the behavior of extruded chloroplasts in light, the reactions
of green tissues to enzymes, organic solvents, and stains, and the absorp-

10 Fitting (1909), A. Meyer (1920, 1922), Zirkle (1926). Zirkle reviews early views
regarding plastid structure.

toward the source of light.

The Structure of the Chloroplast. — No

definite visible membrane has been demon-

68 INTRODUCTION TO CYTOLOGY

tion spectra of chlorophyll mixtures it has been suggested that the chloro-
phyll may be in the colloidal state or adsorbed at the surface of colloidal
particles in the stroma. ^^ K. Stern (1921), however, showed that chloro-
phyll exhibits its characteristic fluorescence only when molecularly
dispersed, as in a true solution; moreover, he reported that chlorophyll
mixtures are fluorescent only when lipide is present. ^- Such facts indicate
that chlorophyll, itself in the molecular state, exists in and perhaps on
colloidal lipide droplets in the stroma.

A special structural feature of some plastids is the pyrenoid. Pyre-
noids are small refractive masses of some proteinaceous substance lying
in or on the chromatophores of many green algse, red algae, flagellates, and

Fig. 31. Fig. 32.

Fig. 31. — Chloroplasts in maize leaf , showing starch-containing regions. {Photograph
by Weier.)

Fig. 32. — Diagram of cross section of chloroplast of Elodea as interpreted by Zirkle
(1926). a, cytoplasmic granule adhering to the cytoplasmic sheath (6); c, pore in stroma;
d, stroma; e, starch inclusion as it appears in polarized light;/, central cavity.

certain liverworts. ^^ They have been reported to originate de novo,^^
by division, 1^ or by both methods. ^^ During the reproductive phases
they may vanish and reappear. Pyrenoids may be simple (Protococ-
caceae, probably), double (Ulothrix), or multiple (Conjugatse, Anthoceros).
It seems clear that the pyrenoid is associated in some way with the
synthetic processes carried on by plastids, although the precise nature of
this association is by no means clear. When the product of synthesis is
starch, as is commonly the case in Conjugatse and Chlorophycese, it often
appears as a series of grains about the pyrenoid (Fig. 26, G), but in other
cases {e.g., certain Rhodophycese) the starch appears outside the plastid
so that the pyrenoid is surrounded by no such "starch sheath." Some
algae with pyrenoids, for example certain diatoms and Chrysophycese,

" Tswett (1906), Willstatter and Stoll (1913, 1918), Zirkle (1926).

1^ See Lloyd (1924) on the fluorescent colors of plants.

1^ See the general account by Geitler (1926) and the paper by Czurda (1928).

1^ Schmitz (1882, 1884), Schimper (1885), G. M. Smith (1913, 1914) on Tetradesmus
and Scenedesmus, W. Zimmermann (1921) on Volvox, Hazen (1922) on Brachiomonas,
Kater (1929a) on Chlamydomonas.

1* M. Hartmann (1921) on Eudorina, Ishikawa (1921a) and Ikari (1923) on
Porphyra, Bold (1931) on Chlorococcum.

i« McAllister (1914, 1927) on Anthoceros, Peterschilka (1922) on Mougeotia,
N. Carter (1926) on Ulva, Czurda (1928, 1929) on Spirogyra, Geitler (1926).

PLASTIDS

69

form no starch at all, the products of synthesis being compounds of other
kinds (p. 62). In Anthoceros it is reported that the outer elements of
the group of "pyrenoid bodies" develop starch while the inner ones
multiply by division. In Selaginella also, the starch appears to develop
from such proteinaceous bodies (R. Ma, 1930).

Origin and Multiplication. — The differentiated plastids seen in
mature tissues may be traced back to plastid primordia, or proplastids,
in the young cells of the meristem or embryo." These appear in the
cytoplasm of living cells as minute bodies grading off to the limit of
visibility.^® In the leaf they enlarge, sometimes becoming rod shaped,
and develop chlorophyll (Fig. 33) when they are still no more than 0.5/i
in diameter. Starch grains can be detected inside of them with polarized

Fig. 33. — Development of chloroplasts from their primordia (proplastids) in living meso-

phyll of Zea Mays. (After Randolph, 1922.)

light (Zirkle, 1927a). They may be markedly altered by fixing reagents, ^^
fluids containing potassium bichromate often causing them to elongate
and acetic acid destroying them altogether; later on they become more
resistant to the latter reagent. After osmication or silver impregnation
they may appear like hollow structures with a blackened periphery.

At all stages up to maturity chloroplasts can be seen to divide,
although constriction often occurs without resulting in division (Kass-
mann). Division generally seems to occur in either of two ways: by
simple constriction or through the formation of a hyaline cleavage zone.
The process may occupy many hours or even several days. 2° Few, if any,
proplastids are left by the time the leaf-cell becomes fully differentiated.
In the cells of the root tip the development of the leucoplasts is much the
same, except for the absence of chlorophyll. Their division appears to be

'^ Pensa, Lewitsky, Guilliermond, Dangeard, Emberger, Noack, Friedrichs,
Mottier, Randolph, Kassmann, Kiyohara, Bowen, Zirkle, Weier, Motte, and others.

^* Randolph (1922) on Zea, Kassmann (1926) on Cabomba (chondriosomes ?,
see p. 85 of this book). Bowen (1929a) disagrees for Vicia.

1^ Zirkle (1927a), Kiyohara (1927, 1930), Weier (1931a).

20 Heitz (1922), Kiyohara (1926).

70 INTRODUCTION TO CYTOLOGY

independent of that of the nucleus and cell, although they may assume a
characteristic polarized arrangement about the mitotic figure (Fig. 25,/).

It was believed by the early observers, notably Schimper (1883) and
Meyer (1883), that plastids never originate de novo but always arise from
preexisting plastids by division. This view has the recent support of
Bowen (1929a). Fully differentiated plastids, such as chloroplasts, can
readily be seen multiplying in this manner in growing tissues with a
frequency sufficient to account for the large number of plastids present
in mature plant parts. However, since the individual plant arises from a
zygote or a spore in which the plastids are usually in a relatively undiffer-
entiated state, the problem of the individuality of the plastid is mainly
one of determining whether these undifferentiated "plastid primordia,"
later developing into chloroplasts and other types, are continuous through
the critical stages of the life cycle, multiplying only by division, or arise
de novo as new differentiations of the cytoplasm.

Light on this question has been sought in a number of investigations
on bryophytes."^ In Anthoceros each cell of the gametophyte contains a
single plastid which divides with the nucleus at each cell-division. The
egg likewise contains a plastid, but apparently the spermatozoid has
none; the zygote and sporophyte cells which it later forms are, therefore,
like the cells of the gametophyte, characterized by the presence of one
plastid. Although it is difficult to demonstrate the plastid in the young
sporogenous cells, every sporocyte shows one very clearly. The sporo-
cyte plastid divides twice as the sporocyte begins to divide into a quartet
of spores so that each spore receives one plastid. Upon germination the
spore produces a gametophyte with one plastid in each cell, and the cycle
is complete (Davis, Scherrer). According to Scherrer, the plastids
remain as morphological individuals throughout the whole life cycle,
multiplying exclusively by division. A similar claim is made for the
plastids of mosses by Sapehin.

More recent studies have added much to our knowledge of plastid
behavior in the reproductive phases. In Polytrichum commune, Weier
has followed the plastids through both sporogenesis and spermatogenesis.
The cells of the young sporophyte contain several small plastids which
multiply by division, and in each sporocyte there are usually two larger
ones. In fixed preparations these show a deeply staining peripheral
portion ("plastonema") and a fighter internal region ("plastosome")
(Fig. 34). They pass through a temporary phase in which they appear
loose and granular; they then divide to form four which are included in
the four spores as the sporocyte divides. In the spore the plastid soon
assumes a structure characteristic of the chloroplast. In the antherid-

21 Davis (1899), Scherrer (1914), Sapehin (1915; see also 1911 and 1913, on
pteridophytes), Senjaninova (19276), Motte (1928), Weier (1930a, 1931a6), Chalaud
(1929-1930).

PLASTIDS

71

ium, also, the plastid shows a plastosome substance and a plastonema in
the form of a network or series of plates. In the androcyte (spermatid),
or cell which is to become a spermatozoid, the plastid becomes a large
limosphere; this buds off a small portion which becomes an apical body
at the anterior end of the spermatozoid (see Chapter XIV). In the
sporocyte of Catherincea undulata the large plastid is said to be formed
by the aggregation of several small ones present in earlier stages
(Senjaninova). The plastid lying in each spore divides to several, each
of which consists of a series of plate-like elements and clearer regions
containing starch. ^^

In such cases as those just described the plastids in the spores divide
and develop into those of the ensuing gametophyte generation. These in
turn give rise to the plastids of the egg, in which, as a rule, they seem to be

Fig. 34. — Behavior of plastids during sporogenesis in Polytrichum commune, a,
division of plastid being completed in archesporial cell, h, reticulate stage of plastids in
lobed sporocyte. c, quartet nuclei formed; each cell after cytokinesis will contain one
plastid. d, young spore with two plastids formed by division. {After Weier, 1931a.)

reduced to primordia or small leucoplasts. The spermatozoid carries a
plastid product (apical body) but apparently no true plastid; hence the
plastidome of the sporophyte is derived from that of the egg.

Our knowledge of parallel phenomena in vascular plants is rather
meager. In Ginkgo each microspore receives about one-fourth of the
plastids of the sporocyte (Mann, 1924). A number of investigators^^
have described a more or less equal distribution of numerous small
bodies to the four spores as the sporocyte divides. Although these
bodies have been referred to wholly or in part as chondriosomes, it is
obvious that at least some of them are plastids or their primordia. Very
little is known about plastids in angiosperm gametes. Guilliermond
(1924) figures small plastids or chrondriosomes in the egg of Lilium.
Ruhland and Wetzel (1924) find that the chloroplasts gradually lose their
color and come to resemble chondriosomes in the generative cell in the
pollen tube of Lupinus luteus, but their behavior in the uniting gametes

" In this and several other works in this field the minute bodies developing into
or arising from plastids are referred to as "chondriosomes," and the thready or plate-
like elements of the plastid are regarded as "chondriosomal" in nature. This involves
a puzzling question discussed in Chap. VI.

" Nicolosi-Roncati (1910), W6ycicki (1912), Wagner (1915), Guilliermond
(1920e, 1924), Suessenguth (1921), Devise (1922), Lewitsky (1925), Senjaninova
(1927c), Py (1929). See the review by Wagner (1927a).

72 INTRODUCTION TO CYTOLOGY

has not been reported. There is genetic evidence that plastid primordia
are transmitted by both parents in some species and by the mother alone
in others (Chapter XXV).

A single interesting case from the algae may be cited. In Zygnema
each vegetative cell contains one nucleus and two plastids, all of which
divide at each vegetative cell-division. In sexual reproduction the
entire protoplast, with its nucleus and two plastids, passes through the
conjugating tube as a "male" gamete and unites with a similar complete
protoplast ("female" gamete) of another filament. The two nuclei fuse,
giving the primary nucleus of the new individual (zygospore nucleus),
while the two plastids contributed by the male gamete degenerate, leaving
the two furnished by the female gamete as the plastids of the new indi-
vidual (Kurssanow, 1911). A similar process occurs in Spirogyra
(Trondle, 1911) (Fig. 162).

Conclusions. — With the possible exception of certain bacteria and
some other protista, the entire organic world is dependent for its suste-
nance upon plastid activity, for it is by virtue of their chloroplasts that
green plants are able to synthesize carbon-containing food necessary
to the life of both plants and animals. Many theoretical questions,
including that of the mechanism of heredity, involve the history of
plastids as individuals. So far our knowledge of this history is incom-
plete. In some organisms plastids can be traced with fair confidence
through the life cycle, but in most cases the situation is not clear. Not
only is it difficult to obtain satisfactory evidence for the division of the
smallest visible proplastids, but it is wholly impossible to determine by
direct cytological observation what may be their history before they have
passed above the limit of visibility. Hence "the question regarding the
extent to which the plastids are to be considered permanent cell organs
with an unbroken genetic continuity throughout the life cycle must
remain an open one" (Randolph). The whole problem is complicated
by the debated question of the relation of plastids to chondriosomes, a
topic to be discussed in Chapter VI.

It may be remarked that cytologists have often been inclined to under-
estimate the capacity of protoplasm for epigenetic differentiation and so
have been too averse to the idea of origin de novo. If plastids represent
transformations of the cytoplasm resulting from the localization of certain
processes, they may well be expected to differentiate anew as these
processes begin, and to preserve varying degrees of permanence depending
upon the processes carried on (Harper, Pensa). Their individual
continuity through certain life cycles may accordingly be interpreted
to mean that in such forms there is a persistence of certain types of
physiological activity through all or nearly all the stages. In the next
chapter it will be of interest to compare with plastids certain cytoplasmic
differentiations in animals, whose metabolism differs in important
respects from that of plants.

CHAPTER V

THE GOLGI MATERIAL

A characteristic constituent of animal cells is the Golgi material.
Interest in this substance has recently been stimulated anew by sugges-
tions concerning its possible relation to certain components of plant
cells. ^

Occurrence and General Characters. — In 1898 Golgi, using a modifi-
cation of a method devised by Cajal for the study of nervous tissue,

lU/

Fig. 35. — The Golgi material in animal cells of various types, a, spinal ganglion cell
of rabbit. {After Golgi, 1899.) h, erythroblast of guinea pig, fixed in formalin and potas-
sium bichromate, c, the same, fixed in osmic acid. (Jb and c after E. V. Cowdry, 1921.)
d, fat cell from human skin. (After Deineka, 1912.) e, cell from pancreas of cat. /,
epithelial cell from prostate gland of dog. g, cartilage cell from cat. (e-g after von Bergen,
1904.) h, red blood corpuscle of frog, prepared by Golgi's silver impregnation method.
{After Sinigaglia, 1910.)

found in the Purkinje cells of the barn owl's brain a structure which he
called the "internal reticular apparatus." It consisted of a closed net
of fine fibrils in a rather definite region of the cytoplasm between the
nucleus and the cell surface. Subsequent investigation of a great
variety of tissues from many animals showed the "Golgi apparatus"
to be of general occurrence although varying considerably in form (Fig.
35). After the customary methods it commonly appears as a network

1 For general accounts, see von Bergen (1904), Duesberg (1914a6), Cajal (1914),
Pappenheimer (1916), E. V. Cowdry (19236, 1924a), Nath (1926), Kopsch (1926) on
human tissues, King (1927) on Protozoa, W. Jacobs (1927), and Bowen (1926c;',
1929d). For flagellates, see Hall (1929) and literature there cited; also later papers
of Hall on Protozoa. For microtechnical methods, see Lee (1921), Pappenheimer
(1916), and Bowen (19286-gf). Valuable literature lists are given by Duesberg
(1914a), Cowdry (1924a), and Bowen (1929d).

73

74 INTRODUCTION TO CYTOLOGY

or group of fibrils lying at one side of the nucleus or entirely surrounding
it. Often it consists of a few scattered vacuole-like "Golgi bodies,"
as in insect spermatocytes. In Protozoa the small, rather numerous
vacuoles react like Golgi material (Hall et al.). Although the largest
and most complex forms are found in vertebrates (spinal ganglion cells)
while the simpler non-reticulate forms prevail in invertebrates, there is
no constant correlation between form and taxonomic grouping. Further-
more, within some groups the form in different types of tissue is com-
paratively uniform, whereas in other groups it shows great diversity.
The appearances presented are nevertheless rather characteristic in
different cell types and in different stages of development: the "appara-
tus" is large in gland cells and small in muscle cells; it is well developed
in active stages of differentiation and becomes less conspicuous as the
cell ages. In pathological or physiologically abnormal tissues it often
shows marked alterations, the significance of which is not understood.^

It has proved very difficult to investigate the Golgi material in living
cells^ because of its low visibility. It is best seen in spermatocytes.
The blackened images observed after impregnation with silver (Cajal,
Golgi, Da Fano) or prolonged immersion in osmic acid (Kopsch, Kolat-
chev) create false impressions regarding the nature of the material in
the living state; the clear canals appearing after other treatments (for-
malin and potassium bichromate) are somewhat better. In the living
cell the Golgi material seems to be a fluid which is physically rather
similar to the rest of the cytoplasm. Its solubility in alcohol and reac-
tions to osmic acid and other reagents suggest the presence of some
lipide.* The fact that impregnated globules or strands of Golgi material
often show chromophilic and chromophobic portions suggests that two
main components are present, though not necessarily with the arrange-
ment they show in the preparations. Different treatments often result
in very different images according to the way in which the components
are affected. This has led to the view that in the Golgi material we
have to deal with a formless fluid rather than an individualized organ.
However, we shall point out farther on that the material in question has
come to be regarded by some workers as one component of a specialized
cytoplasmic region where a definite function is being performed.

Behavior in Cell-division. — The Golgi material is apportioned with
various degrees of regularity between the daughter cells at the time of
cell-division. In the spermatocytes of a snail, Paludina vivipara,
Perroncito (1909, 1910) observed the fragmentation of the Golgi network

2 Cowdry (1924a) lists the alterations reported by many observers.

3 Gatenby (1920), Nath and Nangia (1931), Murray (1898), Brambell and Rau
(1925), Karpova (1925), Avel (1925). See Zweibaum and Elkner (1926) and Ludford
(1927) on tissue cultures. Chambers does not detect it in his microdissection studies.

^ Weigl (1910, 1912), Nussbaum (1913), Gatenby (1920), W. Ma (19286), Ma and
Chang (1928), Ma, Chang, and Liu (1929).

THE GOLGI MATERIAL

75

into a number of elongated pieces, which formed a crown-like group and
then passed to the daughter cells. He called the pieces dictyosomes
and the entire process dictyokinesis. He reported a similar process in
certain mammals. In opossum spermatocytes, according to Duesberg
(1920), the process is much less regular; the network becomes a coiled
thread, irregular fragments lie scattered between the two nuclei at
anaphase, and the network is reconstructed in the daughter cells. In
insects, on the other hand, Bowen (1920) finds that the distribution
of the Golgi material is accomplished with much precision. In Euschistus,
for example, it consists of scattered plate-like bodies (Fig. 129), and, as
the nucleus prepares to divide, these bodies form a circular series at the
equator of the cell and then fragment, after which they pass toward the
poles in advance of the chromosomes. In some species they become
arranged in two ring-like groups, the migrating chromosomes passing

/

't * •'»

n

^

Fig. 36. — The division of the Golgi material (dictyokinesis) in epithelial cells of the cornea

of the cat. (After Deineka, 1912 )

through the rings. Eventually they lie scattered in the daughter cells
and undergo further fragmentation.

The first clear account of dictyokinesis in somatic tissues was given
by Deineka (1912). In the connective and epithelial tissues of the cornea
in young dogs and cats he observed the fragmentation of the Golgi
net into small pieces which were distributed more or less fortuitously
as two groups to the daughter cells (Fig. 36). The process has been
observed since in other tissues. In a protozoon. King and Gatenby
(1923) find Golgi material in the form of rods which behave like those
of a metazoon at the time of cell-division.

Role in Secretion. — Cytological phenomena in glandular tissues^

(Figs. 37 to 40) are of particular interest because of the evidence they

furnish regarding the function of the Golgi material. Ordinarily the

material lies between the nucleus and the side of the cell from which the

secretion is delivered; such glandular cells have a definite physiological

and morphological polarity. Cowdry (1922) and Reiss (1922) observed

that a reversal in the secretory polarity is accompanied by a movement

^ See the valuable review, with bibliography, by Bowen (1929c?); also Special
Cytology, ed. by Cowdry (1932), Sees. VI-X.

76

INTRODUCTION TO CYTOLOGY

of the Golgi material to the opposite end of the cell. The theory that
the Golgi material is intimately concerned in the elaboration of secre-
tions was placed on a firm foundation by the researches of Nassonow
and of Bowen. It had long been known that the secretion in such cells
appears in the form of small droplets or as small granules about which
fluid accumulates (see Renaut, 1907, 1911). Parat (1928) found the
fluid to be stainable with neutral red. It was clearly shown by Nassonow,
Bowen, and others that these secretory droplets arise in the Golgi region.
In intestinal goblet cells, for example, the secretion first appears in the
form of minute granules or droplets along the strands of the basket-like

\ :\

5

i.s

1 ' ^ iS 4 6"

Fig 37. — The relation of the Golgi apparatus to secretion. 1-5, stages in the forma-
tion and accumulation of secretory droplets to form a typical "goblet cell" in the intestinal
epithelium of Molge pyrrhogastra. 6, individual secretory granules with attached bits of
Golgi material in the pancreas of Cryptobranchus. (After Bowen, 1924a.)

Golgi network. The droplets pass toward the distal region of the cell,
where they collect in large masses and complete their growth. As they
move away from the net, each is seen to have a small chromophilic
cap or girdle (Fig. 37, 6).

The principal interpretations which have been placed upon such
observations may be outlined as follows. According to Nassonow and
Bowen, the Golgi material in such cells is a definitely formed system with
a reticulate structure like that illustrated in Fig. 37, and its special
function is to produce the secretion. Whether it has a part in the actual
synthesis of the secretion (Bowen) or only acts to concentrate a secretion
elaborated elsewhere (Nassonow) is uncertain. The latter alternative
would seem to be favored by the "secretion" of injected trypan blue,

THE GOLGI MATERIAL

77

an acid dye, in the Golgi region of liver and kidney cells.^ The chromo-
phihc girdle on the secretion droplet is regarded as a bit of the Golgi
material. The gradual disappearance of this girdle as the droplet enlarges
suggests an actual transformation of the Golgi substance into the secre-
tion (Jacobs, 1928, 1929).

The view of Morelle (1923, 1926, 1927) is that the Golgi region, or
"Golgi spot," in cells of the pancreas is a formless mass of substance

Fig. 38. — Formation of lipoidal secretion droplets by scattered Golgi bodies in sebaceous

gland of mouse. (After Ludford, 1925.)

■■■K

with fairly dejfinite limits but without the organization shown in fixed
preparations. The secretion droplets are formed within it, one of the
materials for the synthesis being furnished by chondriosomes which
appear to enter the Golgi region after being elaborated
in the "basal protoplasm" (Fig. 39). The chromo-
philic girdle is attributed to unequal impregnation of
the secretion droplet. Saguchi (1920) had previously
described the formation of prozymogen granules from
chondriosomes in this " secretogenous area" of the cell.
Ludford (1928) suggests that a synthesis through
enzyme activity occurs at the surface of the chondrio-
somes and that the product is concentrated in the form
of droplets at the surface of the Golgi material.

Another interpretation is that of Parat and his
collaborators.'^ According to these workers, the cyto-
plasm of the animal cell includes only two constant pancreas of ^rog,
formed elements: chondriosomes and vacuoles. In showing elongated

1 1 11 ,1 ic /~i 1 • ») • J. r r chondriosomes in

gland cells the "Golgi zone" consists of a group of middle portion of the
secretory vacuoles, which stain with neutral red and cell where the secre-

1. . ,, • 1 J. r •^^ ^ n i r j. i tion is produced.

lie in the midst oi an ill-denned mass oi cytoplasm con- (^y^g^ Morelle, 1923.)
taining "diffuse lipoids" and "active mitochondria"
Fig. 40, B). It is not an organ with definite morphology, but a region
in the cytoplasm where active secretory vacuoles accumulate and attract
the other elements about them. The net-like aspects so often described

6 Jasswoin (1925), Nassonow (1926), Ludford (1928).
^ 1924-1930. See especially Parat (1928).

78

INTRODUCTION TO CYTOLOGY

are attributed to faulty preservation of the materials in and between the
vacuoles.*

It will be observed that Parat holds the vacuoles to be the important
active element of the Golgi region, whereas the other
investigators regard them as results of an activity on
the part of the material about them. Decision on the
matter is scarcely warranted at present, but the fact
remains clear that the Golgi region of many gland cells
is intimately concerned in the function of secretion.

This general conclusion is supported by studies on
oocytes and spermatids of animals. A number of
workers^ have associated the Golgi material with the
production of fatty yolk in odcytes. In the spermatid,
or cell which is to transform into a spermatozoon, the
Golgi material appears to form a definite body known as
the acrohlast; from this is differentiated and budded off
an acrosome (apical body), which becomes in part the
perforatorium of the spermatozoon.^'^ Bowen compares
the development of the acrosome with the formation of
secretion globules in goblet cells and inclines to the view
that it, too, is a secretion of the Golgi material with a
maSed rtpresenta- ^pecial role in fertilization. The topographical dis-
tion of two views tinctness of the acroblast and chondriosomes is opposed
of the^ecretogenous ^° ^^^ view that the latter are incorporated in the secre-

region in a gland tlon (PolHster, 1930).

apparatAs^^rnd^lS The fact that Golgi material occurs in cells with no
relation to the secre- pronounced secretory activity indicates that it is not
cording^°to'' Bown Concerned solely with secretion in the ordinary sense
and others. B, the (Cowdry, 19236). We may adopt the provisional view
(i^n^th°efr eaHi^er ^^^^ ^^ general the Golgi material, whatever its exact
phases, the vac- form may be, characterizes a cytoplasmic region in
lat^n to the^^^dH- which Certain synthetic processes occur, and that in
fuse lipoids" (more specialized gland cells we observe the results of a
eavi y s ipp e pj-Qnounced synthetic activity of a specific kind.

Comparison with Plant Cells. — The tendency to
"homologize" structures in plants and animals has

area) and "active
chondriome" (black
rods) of the secreto-
genous region, ac-
cording to Parat,
1928. (After
Bowen, 1929c?.)

^ This interpretation of phenomena in gland cells is adversely
criticized by Gatenby (1929, 1930), Beams (1930o6), and Beams
and King (1932). Nath and Nangia (1931) distinguish Golgi

bodies, vacuoles, and chondriosomes by their different colors in living oocytes of

Ophiocephalus and Rita. See also Payne (1932).

9 Hirschler (1913), Cattaneo (1914), Gatenby and Woodger (1920), Voinov (1925),
King (1926), Parat (1927), Ikeda (1928), Kater (1928c), Hibbard (1928), Nath and
collaborators (1928, 1929, 1931), Bhattacharya et nl. (1929, 1930).

10 Bowen (1920, 19226, 19236, 1924a). See, further, Chap. XIV.

THE GOLGI MATERIAL

79

found expression in three hypotheses regarding the relation of the Golgi
material to components of plant cells.

In 1910 Bensley treated root tips of Allium, Iris, and Lilium, and
the tapetum of Lilium, with fixing reagents (composed chiefly of neutral
formalin and potassium bichromate) which had been employed in the
investigation of the Golgi region in animal tissues. In very young cells
the vacuolar material had the form of a system of fine canals; in older
cells these "canaliculi" enlarged and gradually coalesced to form the
large vacuole (Fig. 4:1, A, B). Bensley succeeded in observing the various
stages in living cells. In view of the striking resemblance between the
vacuolar system and the Golgi canals of animal cells he ventured the sug-
gestion that the two are morphologically and physiologically equivalent.
This view has been supported, since, chiefly by Guilliermond." Guillier-

* B - C

Fig. 41. — A, B, cells from the root tip of Allium, showing development of cytoplasmic
canals into vacuoles. {After Bensley, 1910.) C, cells of the root of barley preserved by the
method of Golgi. (After Guilliermond and Mangenot, 1922.)

mond and Mangenot (1922) treated barley roots with silver-impregnation
methods and obtained blackened networks corresponding in form with
the canalicuh observed by Bensley (Fig. 41, C). They, too, regarded
these stages of the vacuolar system as homologous with the Golgi
networks of animal cells. "^^ Further support for this view was seen by
Guilliermond in the work of Parat, who considered the vacuole system
(vacuome) to be a system common to both plants and animals. Zirkle
(1932) observes the similarity between the tannin-filled vacuome of
plant cells and the Golgi apparatus. Moreover, when such cells con-
taining only traces of tannin are fixed with the salts of heavy metals,
the insoluble tannates collect at the periphery of the vacuoles and give
the impregnation pictures so commonly reported in the Hterature.

The second hypothesis is that proposed by Bowen,i^ who found in
plant cells subjected to osmic impregnation considerable numbers of
"osmiophiHc platelets." These were small flattened bodies in the cyto-

"GuilUermond (1926, 1927, 1928, 1929a6e); see especially 1927 and 1929a. See
also Drew (1920), Laburu (1916), Sanchez (1922), Scott (1929), and Bose (1927, 1931).

12 Long before this de Vries (1885) and Bokorny (1888) had blackened plant
vacuoles with osmium and with silver. The reactions seem to be due to the presence
of tannins; see Zirkle (1932).

^^ (1926/1, 1927a6, 1928a, 1929a6c.) Gatenby (1928—1930) favors this hypothesis.

80

INTRODUCTION TO CYTOLOGY

plasm, and their blackened rim after osmic treatment strongly suggested
the discrete Golgi bodies of insect spermatocytes. Bowen concluded that
these elements, rather than the vacuoles, correspond to the Golgi material
of animals, an interpretation which he thought was supported by phe-
nomena in plant spermatids to be mentioned below. That the platelets
are not a special class of elements but chondriosomes or young plastids
showing a particular type of impregnation picture is claimed by several
observers.^*

The third hypothesis, namely, that it is the plastid in plants which
most nearly corresponds to the Golgi material in animals, has been
advocated chiefly by Weier (1930a, 1931, 1932), although it had been
suggested by Bowen (1926c) only to be abandoned for the osmiophilic

_ •♦« « • ■ /

*^.%

a b c d

Fig. 42. — Comparison of Golgi zone and plastid. a, nerve cell of Bufo tadpole; silver
impregnation, b, spermatogenous cell of Polytrichum; osmic impregnation. Note
similarity of plastids in 6 and Golgi zone in a. c, Golgi bodies in spermatocyte of Helix;
osmic impregnation, d, plastid in sporogenous cell of Polytrichum; osmic fixation. (From
Weier, 1932; a and c after Parat.)

platelet view. Weier has made a detailed comparison of the fixation
images of the Golgi region in animal cells as described by Parat and other
investigators with images obtained by similar methods (osmium and
silver impregnation) in moss cells. He finds a striking similarity in the
two series of cases. Before their characteristic activities begin, both
Golgi region and plastid may appear relatively homogeneous, but after
starch or the secretion product has accumulated each of them shows a
blackened constituent in the form of strands or plates running through
a mass of lighter substance or appears as a dense mass with one or more
"cavities" inside it (Fig. 42). Starch occurs in these regions in the plastid.
The dense substance and the cavities are compared respectively with
the modified cytoplasm and "secretory vacuoles" of Parat's Golgi zone;
the characteristic "network" or "platework" fixation image produced
in both cases is attributed to a general similarity in constitution. It
is concluded that the Golgi zone, like the plastid, should be considered
as primarily a specialized region of the cytoplasm having to do with the

"Owens and Bensley (1929), Kiyohara (1930), Guilliermond (1928, 19296e).
Weier (1931) argues for their distinctness in mosses.

THE GOLGI MATERIAL 81

elaboration of certain compounds : carbohydrate in the moss and secretion
droplets in the gland cell.

Since such comparisons are based so largely upon the results of
microtechnical methods known to be somewhat capricious in their action,
more cogent evidence has been sought in cells of other types. It was
shown by Bowen that the Golgi material in the animal spermatid performs
a curious but very definite morphogenetic function: as already noted,
it becomes an acroblast, which in turn buds off or secretes the acrosome
of the spermatozoon (Figs. 130, 133). It was also known that in the moss
spermatid a limosphere gives rise by division to the apical body at the
anterior end of the developing spermatozoid (Figs. 120, 121) (Allen,
1917a). Since it seemed reasonable to suppose that this very special
function would be performed in the two cases by similar components
of the cell, Bowen turned to the limosphere for evidence regarding the
plant's analogue of the animal's Golgi material. In a preliminary study
(19276) he found the limosphere apparently developing in the midst
of a group of "osmiophilic platelets"; in this he saw a confirmation of
his view that the "platelets" in plants correspond to the Golgi material
of animals. Weier, who has made a more extensive study of this matter,
finds that the limosphere is derived from the plastids of the earlier
spermatogenous cells; moreover, it appears that the osmiophilic platelets
are in part small plastids modified in appearance by the methods of
fixation (p. 69). The phenomena in sperm-forming cells, therefore,
emphasize the similarity of Golgi region and plastid.

Such comparisons of plant and animal cells are of great interest,
but they should not be pressed too far. Especially should it not be
concluded that because two structures impregnate somewhat similarly
with osmium or silver they are therefore homologous. Osmium tetrox-
ide is reduced not only by unsaturated fats but also by certain proteins
and phenolic compounds; it therefore may blacken structures which are
neither homologous nor physiologically equivalent. The plant vacuole
and the animal Golgi region are both so blackened; neutral red,
however, colors the vacuole but only the secretion droplets (Parat's
vacuome) in the Golgi region. Hall (1931a) warns against the use of
impregnation methods as a criterion in identifying cell structures in flagel-
lates and Protozoa, where they may often blacken contractile vacuoles,
chromatophores, eyespots, flagella, and other bodies, in addition to the
small vacuoles which best meet the criteria for Golgi material in such
organisms. The evidence becomes somewhat stronger when a definite
morphogenetic function can be cited, as in the case of acrosome formation
in spermatids. Perhaps the chief value of such comparisons at present
lies in the fact that they lead to improvements in our technical procedures
and foster a more critical attitude toward the results obtained through
their use.

CHAPTER VI

CHONDRIOSOMES

Chondriosomes, or mitochondria, are small globules, rods, and threads
almost universally present in cytoplasm. They had no single discoverer;
the elements described by many early observers correspond with them in
some degree. Thus the "fila" of Flemming (1882), the ''bioblasts" of
Altmann (1890), and the "cytomicrosomes" of Strasburger (1882) and
others are all recognizable among the chondriosomes of today. In 1897
and the following years Benda, through the use of newly devised technical
methods, discovered chondriosomes in cells of many types, notably in the
spermatogenous cells of animals, and applied to them the term "mito-
chondria." It was somewhat later, through the researches of Meves,
Regaud, Faure-Fremiet, Lewitsky, Guilliermond, and others, that they
came into prominence. Since that time they have been very intensively
studied, and a special literature of large volume has developed. Owing to
the difhculties attending the observation of such minute objects and the
determination of their relation to other cytoplasmic constituents, opinion
regarding the origin, behavior, and biological significance of chon-
driosomes is still in a very unsettled state. ^

Occurrence and General Characters. — Chondriosomes have now
been reported in plants and animals belonging to nearly all of the larger
natural groups. It is asserted by N. H. Cowdry (1917) that "in all forms
of animals, from amoeba to man, which have been investigated with
adequate methods of technique, they occur without exception." Their
presence has been reported, furthermore, in practically all tissues. In
plants it is probable that they are no less universally present, although
they have not yet been demonstrated with certainty in Cyanophycese
and some Chlorophycese (Guilliermond).^

' Reviews of the subject are given by Faure-Fremiet (1910a), Duesberg (1911,
1919), E. Schmidt (1912), Cavers (1914), E. V. Cowdry (1916a, 1918, 1924a), Meves
(1918a), Guilliermond (1919a, 192U', 1923), Meyer (1920), Lundeg;\rdh (1922), and
Nath (1926). Giroud (1925) reviews researches on the physical and chemical nature
of chondriosomes. For the effects of various reagents on chondriosomes, see Kings-
bury (1912), E. V. Cowdry (1914, 1918), N. H. Cowdry (1917), Meyer (1920), Ozawa
(1927), and Milovidov (1928c, 1929). Findlay (1927) describes changes in injured
cells. The valuable account by E. V. Cowdry (1918) has been drawn upon in the
preparation of this chapter.

2 They are abundant in myxomycetes (N. H. Cowdry, 1918; Lewitsky, 1924),
Charales (Mirande, 1919; Riker, 1921), brown algae (Mangenot, 1920abde), and red
algae (Nicolosi-Roncati, 1912). Alexieff (1923, 1925) reports their presence in
bacteria.

82

CHONDRIOSOMES

83

The chondriosomes have generally been regarded as essentially com-
parable in plants and animals,^ although their behavior may not be the
same according to the view of some workers. N. H. Cowdry finds plant
and animal chondriosomes to be practically identical in morphology,
reaction to fixatives and dyes, and distribution in resting and dividing
cells; any conspicuous differences in arrangement seem to be due to the
more pronounced polarity of many animal cells.

Chondriosomes appear in living cytoplasm in the form of minute
globules, vesicles, straight or curved rods, smooth threads, chains of
granules, nets, and other more irregular bodies (Fig. 43). These forms

Fig. 43. — Chondriosomes in plant and animal cells. A, nerve cell of guinea pig.
(After E. V. Cowdry, 19146.) B, tapetal cell of Nymphwa alba. (After Meves, 1904a.)
C, living epidermal cell of tulip petal. D, ascus of Pustularia vesiculosa. E, hypha of
Rhizopus nigricans. F, portion of embryo sac of Lilium; chondriosomes clustered about
nucleus. G, cell of root tip of Allium. (C-F after Guilliermond, 1918.)

can be seen to change into one another, especially when the cultural
conditions are altered.^ Such changes are in part the result of cyto-
plasmic streaming. The same variety of form is encountered in fixed
tissues. Particular types tend to predominate in certain tissues.
Although it may be convenient at times to designate rods or threads as
"chondrioconts" and chains of granules as "chondriomites, " it is to be
remembered that the forms assumed by the chondriosomal material are of
minor importance. For practically all purposes the now synonymous
general terms chondriosomes and mitochondria are sufficient. The total
chondriosomal content of the protoplast has been called the chondriome.^

3 N. H. Cowdry (1917), Mangenot and Emberger (1920), Bouygues (1924).

« Lewis and Lewis (1915, 1924), Chambers (1915, 1924), Anitschkow (1923),
GuiUiermond (1925a). N. H. Cowdry (1920) finds them to be more stable in Pisum
roots.

* Meves, GuiUiermond. P. A. Dangeard (1924, 1931) uses the terms cytosomes and
cytome for these elements in plant cells. For an older and more prevalent use of the
term "cytosome," see p. 2.

84 INTRODUCTION TO CYTOLOGY

The number of chondriosomes present varies greatly with the tissue
and the degree of its differentiation. They are usually abundant in
young or active cells and relatively few or even absent in fully differ-
entiated ones. In living cells, moreover, they can be seen constantly
appearing and disappearing. The arrangement of the chondriosomes
within the cell varies; this is often clearly related to certain functional
activities, as in certain polarized gland cells. ^ In pathological animal
tissues they show pronounced qualitative and quantitative changes, of
which one of the most characteristic is the breaking up of filaments into
granules (see E. V. Cowdry, 1924a6).

Physical and Chemical Nature. — Chondriosomes have a semifluid
consistency. Under either bright- or dark-field illumination they appear
homogeneous (Guilliermond, 1929c). It is reported that they are doubly
refractive by polarized light (Giroud, 1928). When the cytoplasm is not
too viscous they may be centrifuged out, which shows that their specific
gravity exceeds that of the cytoplasm (Faure-Fremiet, 1913). In both
plants and animals they melt at a temperature of 48° to 50°C.'^ In
hypotonic solutions they become swollen and vesicular, whereas in hyper-
tonic media they shrink and become slender. In animal cells Rum-
jantzew (1926), studying the effect of variations in the pH of the medium,
observed that they remained unchanged between 6 and 8, broke up or
agglutinated between 5.8 and 3, and formed networks and finally dis-
solved as the pH was raised to 10. Lewis and Lewis (1924) observed
filamentous ones become vesicular at 4.4 and shorten into granules at
9.6. As would be expected, many fixing reagents bring about decided
alterations in their form,^ while those with much acetic acid destroy them
altogether. They are well preserved by formalin and potassium bichro-
mate, provided the solutions are not too acidic.

Chemical studies, though incomplete, indicate that chondriosomes are
composed of phospholipides and albumins.^ Besides staining with
hsematoxylin and several other dyes commonly employed with fixed
material, they show a characteristic affinity for certain intra-vitam
stains, notably Janus green. According to E. V. Cowdry (1916), chon-
driosomes may be provisionally defined as "substances which occur in
the form of granules, rods, and filaments in almost all living cells, which
react positively to Janus green and which, by their solubilities and stain-
ing reactions, resemble phospholipins and, to a lesser extent, albumins. "

Origin and Multiplication. — The question of the origin and multiplica-
tion of chondriosomes has been much debated. Evidence for their

^Bensley (1916), E. V. Cowdry (1918).
'Policard (1912), N. H. Cowdry (1917).
sSchaxel (1911c), Kiugery (1917).

3 Regaud (1908), Faurc-Fremiet (1910a), Lowschin (1913), Lewitsky (1924),
Giroud (1925a6, 1929), Milovidov (1928c).

CHONDRIOSOMES 85

division in somatic cells has frequently been reported, and some investi-
gators have even held this to be their sole mode of origin — that they
arise only from preexisting chondriosomes and are, therefore, permanent
cytoplasmic organs. ^° Others have questioned much of the evidence
for division and are convinced that, whether or not division occurs,

.i ^'N ~ Vj, .-^^

d e f

Fig. 44. — Behavior of "chondriosomes" during microsporogenesis in Hdleborus.
a, young sporocyte. 6, prophase of first division, c, interkinesis. d, e, cytokinesis after
second mitosis. /, young microspore. {After Wagner, 1927a.)

chondriosomes arise de novo in the cytoplasm. ^^ A third view, namely,
that they arise from the nucleus, has not been well substantiated.

Researches on living material ^^ leave no doubt that chondriosomes
may appear anew and disappear, probably with some relation to metabolic
processes in the cytoplasm. They are often seen to divide, though the
division appears to be passive. In the leaf-cells of Cabomha, Kassmann
(1926) saw them rise from the limit of visibiUty, one or two days being

10 Guilliermond (1912a), Terni (1914), Moreau (1914), Duesberg (1911), Arnold
(1912), Friedrichs (1922), Horning (1926).

" Forenbacher (1911), Orman (1913), Lowschin (1913), Scherrer (1914), Beckwith
(1914), Chambers (1915), Lewis and Lewis (1915), Twiss (1919), Meyer (1920),
Morelle (1926), Kassmann (1926), Wagner (19276).

12 Lewis and Lewis (1914, 1915, 1924).

86 INTRODUCTION TO CYTOLOGY

required to reach the typical size; he also observed actual division several
times. From his observations on myxomycetes (fixed material) Lewitsky
(1924) concluded that the chondriosomes, which are capable of division,
may become progressively smaller until they pass below the limit of
visibility, and that by growth they may pass the limit in the reverse
direction, giving the appearance of origin de novo. This places the
problem of ultimate origin in the realm of the invisible.

The behavior of the chondriosomes at the time of nuclear division and
cell-division varies widely in different cases. In somatic tissue cells
their distribution is quite fortuitous, though approximately equal if the
cytoplasm is equally divided. In microporocytes the chondriosomes tend
to group about the nucleus and the mitotic figure and are apportioned

more or less equally to the four spores (Figs. 44,
45). In Nephrodium they form an equatorial
layer between the two nuclei after the first divi-
sion; this layer is then divided into four parts by
the developing cell membranes. ^^ In the living
I spermatocyte of a grasshopper, Dissosteira Caro-
lina, Chambers (1915) saw the chondriosomes
form a mantle about the nucleus, the mitotic
figure, and the daughter nuclei, much as in the
Fig. 45.— Young spore niicrosporocyte of Larix (Devise, 1922) (Fig. 82).
quartet of Nephrodium, In other Spermatocytes the chondriosomes are

showing cell partition j. i ]l i ■ t • i i t • ■ j-j^ xi

formed in mitochondrial reported to Undergo mdividual division after the
layer. {After Senjaninova, division of the chromosomcs.^'* In EuscMstus the

chondriosomal filaments lying across the equator
of the cell are passively cut in two by the constriction furrow as the cell
divides^^ (Fig. 129), but in Gryllotalpa borealis they appear to break and
move apart before the furrow appears (Payne). In Gryllotalpa vulgaris,
Voinov (1916, 1925) states that the "mitochondria" fuse to form a thread
which then segments into 60 or more "chondriosomes. " These units are
arranged in the spindle along with the chromosomes, which they may
resemble, divide at both meiotic mitoses, and are thus equally distributed
to the four resulting spermatids (Fig. 46).

In certain scorpions the chondriosomal material of the spermatocyte
is distributed with remarkable precision (Wilson, 1916). In Centrums
it takes the form of a single ring-shaped body which lies by the side of
the spindle figure. The ring divides accurately at both meiotic divisions
along with the chromosomes, each of the four spermatids, and hence each
spermatozoon, receiving a quarter of its substance. In Opisthacanthus

13 Senjaninova (1927c). Cf. Yamanouchi (1908a). See also Lewitsky (1925) on
Equisetum.

" Faur6-Fremiet (1910a), Korotneff (1909), Terni (1914), Payne (1916).
16 Montgomery (1911), Bowen (1920).

CHONDRIOSOMES

SI

about 24 hollow spherical bodies are formed instead of a ring. These
show no evidence of division but are separated into four approximately
equal groups by the cell-divisions, each spermatid receiving six or occa-
sionally five or seven. ^^ It is not improbable that this regularity of
distribution in spermatocytes bears some relation to the definite function
performed by the chondriosomal substance in the development of the
spermatozoon (p. 218).

The Function of Chondriosomes. — Our knowledge of chondriosomes
is far too incomplete to warrant categorical assertions concerning their
function. The literature is not only complicated by conflicting state-
ments regarding their observed behavior, but it is further encumbered
with a variety of hypotheses, some of which rest on very narrow founda-

i

46. — Examples of regular behavior of chondriosomes in cell-division. A-C
spermatocyte of Gryllotalpa vulgaris: A, chondriosomal material in cytoplasm; B, first
meiotic mitosis, showing chondriosomes (at sides) occupying the achromatic figure with the
chromosomes (at center) ; C, stages in the division of a chondriosome. {After Vo'inov, 1916.)
D, dividing cell of Geotriton fuscus, showing division of chondriosomes as cell constricts at
equator. (After Terni, 1914.)

tions. The more prominent views on the subject may be outlined as
follows.

Meves in 1908 propounded a general theory according to which all the
visible differentiations which develop in different types of cells during
ontogenesis were regarded as modifications of the same elementary
cytoplasmic constituents, namely, the chondriosomes. These were
thought not only to be concerned in the formation of fibrils, plastids, and
the like" but also to play an important role in heredity. A close associa-
tion was observed between chondriosomes and myofibrils, and it was
claimed that the fibrils were actually transformed chondriosomes.^^
A similar claim was made for neurofibrils^^ and other such differentiations.
This interpretation of the genesis of fibrils has been adversely criticized, ^°
and it now seems probable that, although the chondriosomes may
possibly furnish material or cooperate in some other way in the formation

16 Cf. Sokolow (1913) and Mark and Wyman (1922).
" See E. V. Cowdry (1918, p. 102).

18 Benda (1899), Meves (1907a6, 1909), Duesberg (1909afe).

19 Meves (1907a), Hoven (1910a), G. Arnold (1912).

20Heidenhain (1911), Levi (1911, 1916), Gurwitsch (1913), Gaudissart (1913),
Lewis (1917), E. V. Cowdry (1914d, 1918), Laguesse (1926), Conklin (1931), and
other!..

88 INTRODUCTION TO CYTOLOGY

of fibrils of certain types, they do not actually transform into them.
Probably the clearest case of the formation of a definite structure by
chondriosomes in animal cells is furnished by the nebenkern, which is a
chondriosomal body developing into an important constituent of the tail
sheath of the spermatozoon (p. 219).

The observations of several investigators have suggested a connection
between chondriosomes and the formation of secretion and storage
products. In the pancreas, for example, it was thought^'^ that chon-
driosomes become zymogen granules, but Regaud (1911), who with Meves
first emphasized the secretory theory in general, thought it more probable
that the chondriosomes in some way synthesized the zymogen from
materials selected from the cytoplasm (the ''electosome theory").
Reference has already been made to the newer view that chondriosomes
furnish a material for the synthesis of secretions in the Golgi region of
gland cells (see p. 77). The development of the secretion product in
glandular hairs of Salvia has been associated with chondriosomes. ^^
Chondriosomes have also been assigned a role in the elaboration of certain
types of yolk in developing eggs^^ and of fat in liver cells. ^^

The theory that chondriosomes are in any sense protoplasmic organs
with special roles in differentiation and secretion was strongly opposed
by A. Meyer (1911, 1920), who contended that they are simply ergastic
accumulations of an albuminous nature. Their ergastic nature, according
to Meyer, is indicated by the fact that their distribution and behavior
are just what would be expected of reserve substances necessary as sources
of building material and energy (in meristematic cells, eggs, regenerating
tissues, muscles, etc.). They do not transform into differentiations such
as myofibrils, but they may lie near them and possibly furnish materials
or energy for their upbuilding by the cytoplasm. They do not elaborate
or secrete ergastic substances but are themselves such 'substances in
process of formation by the cytoplasm. The general view that chondrio-
somes are products of metabolic activity rather than distinct proto-
plasmic organs has been held in one form or another by many workers
and appears to be well supported by many observations on both living
and fixed cells.

The almost universal occurrence of chondriosomes in protoplasm
suggests a connection with some fundamental process common to all
living matter. That this process may be oxidation, the chondriosomes
being a "structural expression of the reducing substances concerned in
cellular respiration," was suggested by Kingsbury (1912), who pointed

21 Hoven (19106), G. Arnold (1912).

22 Jaretzky and Triebel (1932).

23Loyez (1909), Dubreuil (1913), Van Durme (1914), Shaffer (1920), Gatenby and
Woodger (1920), L. Harvey (1925), Konopacki (1927), Bhatia and Nath (1931).
See Wilson (1925, p. 341).

2" D. Smith (1931), Kater and Smith (1932).

CHONDRIOSOMES 89

out that they are best fixed by oxidizing agents depending for their effect
on reducing substances, probably the lipidal chondriosomes, in the cyto-
plasm. The chemical fitness of chondriosomes for processes involving
oxidation and reduction was further emphasized by the work of Mayer,
Rathery, and Schaeffer (1914), who also pointed out that various reagents
which diminish respiratory oxidations attack lipides. Joyet-Lavergne
(1928) reports that chondriosomes give a positive test for glutathione,
which is thought to be of special importance in cell oxidations and
reductions (probably because of a respiratory ferment associated with it,
according to Warburg). The observations of E. V. Cowdry on the action
of vital dyes are also in harmony with the respiration theory. Evidence
regarded as unfavorable has been brought forward by Kropp and May
(1924), who find that the chondriosomes in the white blood cells of
animals made to inhale oxygen, carbon dioxide, and ether differ in no
discernible way (Janus-green method) from those of normally respiring
animals.

A theory that chondriosomes are the site of enzymatic syntheses has
been put forward by Marston (1923, 1926), w^ho finds evidence that they
contain proteolytic enzymes and that protein synthesis in vitro is acceler-
ated by colloidal lipides. Such synthesis would be greatly facilitated by
adsorption in the extensive interface between the chondriosomes and the
cytoplasm (Cowdry, 19266). The enzyme theory is supported by Horn-
ing (1926, 1927afo, 1928a), who observes their adherence to food particles
in the Protozoa and their disappearance as the food is digested.

One of the most striking views regarding chondriosomes is that they
are microorganisms. Altmann (1890) thought many years ago that
protoplasm was essentially a vast colony of living "bioblasts" in a
non-living ground substance. Recently Portier (1917, 1918) and Wallin
(1922-1927) have independently suggested that ''mitochondria are, in
reality, bacterial organisms, symbiotically combined with the tissues of
higher organisms." Wallin finds evidence for this view in the fact that
bacteria and chondriosomes show certain similarities in form, staining
reaction, chemical composition, physical properties, and activity, and in
peculiarities in the development of Bacillus r'adicicola in the cells of the
clover nodule. Assuming that chondriosomes develop into plastids,
Wallin suggests further that chloroplasts are not organs developed in the
cytoplasm, but chlorophyll-forming organisms that have invaded proto-
plasm, with which they live in a state of complete symbiosis.-^

This bacterial theory has been severely criticized. ^^ Cowdry has
shown that chondriosomes and bacteria simultaneously present in the

" See in this connection Pascher (19295) on endosymbiosis by blue-green algse.

26Regaud (1919), Guilliermond (1919c), Cowdry and Olitsky (1922), Cowdry
(1923a, 1924o), Nicholson (1923), Bowen (1923a), Horning (19276), Milovidov
(19286).

90 INTRODUCTION TO CYTOLOGY

clover nodule show distinct differences in fixing and staining reactions.
Similar results are obtained by Milovidov, using another method on
lupine nodules. Horning reports that chondriosomes, but not bacteria,
are stained with a new vital dye derived from Janus green. Bowen
cites as further evidence against the bacterial interpretation the remark-
able behavior of the nebenkern (chondriosomal material) in the animal
spermatid. Wallin attributes the peculiar properties of chondriosomes
to their long symbiotic history and is inclined to interpret the nebenkern
as a stage in the bacterial cycle somewhat analogous to the " symplasm "
in other bacterial forms (Lohnis). He reports further that experiments
appear to indicate that chondriosomes can be cultivated independently
on nutrient agar. The final evaluation of this evidence is awaited with
the greatest interest.

Chondriosomes and Plastids. — The general theory of Meves that
many intracellular differentiations are due to transformations of chon-
driosomes included the proposition that the plastids of plant, cells arise
from these bodies. This view has been expressed in one form or another
by a large number of workers." In Asparagus and Pisum, for example,
Lewitsky concluded that chondriosomes become leucoplasts in the root
and chloroplasts in the stem and leaf. Other investigators^^ have main-
tained that plastids are surely or in all probability quite distinct from
all other elements in the cell and that confusion has arisen because differ-
ent kinds of minute bodies are so similar in appearance. No problem
in the cytology of recent years has been more perplexing than this one.^^

That some distinction must be made between the small bodies which
develop into plastids and those which do not has become increasingly
evident. Guilliermond, whose extensive studies^" are particularly note-
worthy, came to recognize such a distinction, but he considered both
types as chondriosomes essentially equivalent to those of animals: the
"active" ones are elaborative elements developing into plastids, while
the relatively "inactive" ones remain small and perform undetermined

27 Lewitsky (1910, 1925), Forenbacher (1911), Guilliermond (19116 et seq.), Cavers
(1914), Moreau (1914), Nassonow (1918), Emberger (1920, 1927), Alvarado (1923),
Friedrichs (1922), Bouygues (1924), Mangenot (1925), Kirby (1928), Cowdry (19266),
Senjaninova (19276c), Motte (1928), Cunha (1929), Zirkle (1929c), Loui (1930), and
others.

28 Meyor (1911), P. A. and P. Dangeard (1919 el seq.), Limdegardh (1910), Rudolph
(1912), Mottier (1918, 1921), Scherrer (1914), Noaek (1921), Harper (1919), Lowschin
(1913, 1914), Sapehin (1915), Krupko (1926), Bowen (1927a6, 1929a), Bowen and
Buck (1930). Kassmann (1926) expresses uncertainty.

29 See the discussions by Bowen (1929a) and P. A. Dangeard (1931). The indis-
criminate use of the terms "chondriosomes" and "mitochondria" for small bodies of
many kinds must be borne in mind when reading the literature in this field.

^ A classified list of Guilliermond's researches up to 1921 is given by himself
(1921z), together with a list of works by his associates. See also Guilliermond,
Mangenot, and Plantefol (1933).

CHONDRIOSOMES

91

)6

functions. Others contended that the proplastids should not be included
under the heading of chondriosomes nor homologized with anything in
animal cells. Meyer's (1920) claim that plastids constitute a funda-
mentally distinct class even in their earliest stages of development has
been supported by Bowen (1927a6, 1929a), who has employed a variety
of methods little used by botanists. In root meristems and other plant
tissues Bowen claims that the two classes of elements can be distinguished
on the basis of general form, structure, reactions to stains, and behavior
during nuclear division and cell-division. As a rule the chondriosomes^^
in the root tips are round and vesicular, are
best preserved and stained by the Champy-
KuU method, and show no regular arrange-
ment in the cell during mitosis; whereas the
proplastids are elongate and usually not
vesicular, are best preserved by the Mottier-
Benda method, and show a characteristic
polarized arrangement during mitosis (Figs.
25, 47). Bowen further finds, with others,^-
that the two classes react somewhat
ently in impregnation procedures and
reports^^ of unlike reactions to vital dyes \f,
and heat. A difference in appearance and ^'^•♦,.6

behavior in tissue affected with mosaic dis- "<w

eases is described by Dufrenoy (1931). As p^^ 47.-Piastids and chon-

a result of his studies on living cells, Pensa driosomes. a, plastids (large) and

concludes that plastids may arise either by t^fnt'^S 'oTt„t,r t
division or by a direct differentiation of the chondriosomes in root tip of Vida;
cytoplasm; in the latter case the chondrio- :r:h»dSZ ("darf t"S

somes group about the plastids and seem to during mitosis in Hyadnthus root.

furnish material for the latter as they grow ^'^^''' ^'^^"" ^^^^"^"^
or become green. Loui (1930), who has used the fluorescence microscope,
can find but one kind of initial body which he regards as chondriosomal
in nature.

It is plain that the confusion in this subject is in part a matter of
terminology, since the words " chondriosome " and "mitochondrion"
have been used in such different ways. Hence it has been suggested that
the terms should be dropped altogether (Mottier, Dangeard). Zirkle
(1929c), on the other hand, uses the term "mitochondria" for all small
inclusions which are preserved by bichromates with a pH higher than

differ- »?V^J^

d cites %•?. ■ 5;^?:>.\

^^ Not wishing to commit himself on the question of the relation of these bodies
to the chondriosomes of animals, Bowen employs for them the term "pseudochon-
driosomes." Dangeard calls them "cytosomes."

32 Pensa (1925), Ruhland and Wetzel (1924).

«« Guilliermond (1923a), Policard and Mangenot (1922).

92 INTRODUCTION TO CYTOLOGY

4.2 to 5.2 and are destroyed by more acid fluids, and the term "plastids"
only for those bodies containing starch or chlorophyll. We have here
chosen somewhat arbitrarily to retain the term " chondriosome " but to
restrict its application to those elements with a fairly characteristic
composition which do not behave as the primordia of plastids. When the
nature of a small element is unknown, such non-committal terms as
"microsome" and "particle" are always available. It remains for
future research to reveal more precisely the chemical and genetic relation-
ship of proplastids and chondriosomes at the time of their first appearance
in the cytoplasm and to evaluate the claim of Meyer and others that the
chondriosomes are, like all other formed bodies in the cytoplasm except
plastids, ergastic in nature.

Conclusion. — In the present state of our knowledge no final judgment
can be rendered on the question of the nature and function of "chondrio-
somes." Bearing present probabilities in mind, we may adopt as a
tentative working basis the view that in both plants and animals the
chondriosomes, or mitochondria, are a special class of small bodies fairly
distinguishable chemically from other materials of an ergastic nature,
that they represent elaborated products which are somehow employed
as sources of matter and energy for further growth and differentiation,
and that they are best regarded as distinct from the plastids of plant cells.
This provisional disposition of the matter will be convenient until wholly
decisive evidence is obtained.

In spite of the fact that the study of chondriosomes has so far raised
more problems than it has solved, it has proved of much value, for it has
turned to the cytoplasm some of the attention so long directed almost
exclusively to the nucleus. It has also been of great service in bringing
about a closer scrutiny of the effects of fixation and a renewed emphasis
upon the importance of the study of living protoplasm.

CHAPTER VII

ERGASTIC SUBSTANCES

In Chapter II emphasis was laid on the conception of the protoplast as
a living system of active components which by themselves would be non-
living. It is nevertheless convenient to deal separately with materials
which, for the time at least, are relatively inactive. These, for the most
part, are accumulations of the products of protoplasmic activity and
represent by-products, supporting structures, and reserves which are
later to be used in metabolism. They are thought of as non-living sub-
stances, but to whatever extent they affect the vital activities of proto-
plasm they must logically be regarded as a part of the living system.

The relatively inactive or "lifeless" substances in or on protoplasm
were called metaplasm by Hanstein (1868). This term has been com-
monly employed in this sense, but unfortunately it has been widely used
in another meaning (see p. 45). We have, therefore, adopted Meyer's
(1896) expression, ergastic substances. "■

Vacuoles. — Although the semipermeable membranes bounding vacu-
oles are definitely a part of the protoplasmic system (p. 42), it is con-
venient to treat vacuoles in this chapter because of the ergastic nature
of their contents.

Any spaces within the protoplast containing ergastic liquid or (very
rarely) gas may be regarded as vacuoles, but the term is ordinarily
used with reference to those occupied by the aqueous mixture know^n as
cell sap. Vacuoles of this general nature are small and comparatively
inconspicuous in animals, but in plants they appear to be almost uni-
versally present and clearly play a prominent role in metabolism. In
terminal meristems of vascular plants, as shown especially by the recent
work of Zirkle (1932), they are usually rather numerous, small, and
spherical, although they may be drawn out into other shapes by the
streaming cytoplasm. In the apical cells of Osmunda (fern) and Lunu-

1 For an extensive account of the ergastic materials in plants, see A. Meyer (1920,
1926). For the chemistry of plant products, see R. W. Thatcher (1921), Onslow
(1923), Czapek (1913, 1920), Molisch (1913), Rigg (1924), Trier (1924), Haas and Hill
(1928), Gortner (1929), and Wiesner et al. (1932). Ergastic materials are not to be
confused with the ergastoplasm of Gamier, Bouin, Prenant, and others. This term
was applied to a supposedly very active or "superior" type of protoplasm; see Faure-
Fremiet (1910o) and Wilson (1925). For general accounts of vacuoles, see Meyer
(1920-1921; Chap. VI, Sec. 6), Lundegardh (1922; Pt. 2, Chap. VIII), P. Dangeard
(1923o) and Guilliermond (1929a).

93

94

INTRODUCTION TO CYTOLOGY

laria (liverwort) they are very large. In the cambium of woody plants
they are very abundant and exhibit a surprising variety of form (Fig.
48) (Bailey, 1930). As the meristematic cells multiply, the vacuoles
are distributed, often after passive division, to the daughter cells. Dur-
ing the final growth and differentiation of the cells the vacuoles coalesce,
commonly forming a single enormous vacuole which far exceeds the
volume of the cytoplasm in which it lies. The vacuolar system of a cell
or other protoplasmic mass, whether this system consists of one or more
vacuoles, is called the vacuome (Dangeard).

Much of the difference of opinion regarding the origin and occurrence

of vacuoles has been due to the fact
that many fixing fluids, particularly
those containing acetic and chromic
acids, may destroy the true vacuoles
and greatly alter the appearance of
the cytoplasm. Certain fluids con-
taining iron or chromium salts pre-
serve very well the size and form of
the vacuoles but not their membranes
(Zirkle), The only trustworthy stud-
ies on this subject, as in the case of so
many others in the field of cytology,
are those which are checked as far as
possible by observations on living
material.

As just intimated, the mode of
Fig. 48.-Various forms assumed by origin of vacuoles has long been a

the vacuome in fusiform cambial initials of debated qUCStion. An old and Still

Robinia. (After Bailey, 1930.) prevalent vicw is that they simply

arise de novo in the cytoplasm wherever water and certain dissolved sub-
stances become abundant enough to form visible droplets (von Mohl,
Nageli). Pfeffer (1890), who found that droplets with membranes
were formed when granules of asparagin were introduced into protoplasm,
favored this view. Strasburger (1898), who regarded protoplasm as
mostly alveolar in structure, accounted for the origin of vacuoles by
the enlargement and coalescence of alveoles, while Meyer (1912, 1920)
classed them as accumulations of ergastic fluid around which membranes
are secondarily formed.

Sharply opposed to this interpretation was that of de Vries (1885),
who advanced the theory that vacuoles do not arise de novo but rather
from individualized bodies which he called tonoplasts. As the tonoplast
secretes cell sap within itself, it gradually enlarges and becomes the
vacuolar membrane, which is still referred to as the tonoplast. Since
the tonoplast bodies were supposed to multiply only by division, de Vries

ERG AST IC SUBSTANCES

95

looked upon vacuoles as permanent constituents of protoplasm. This
theory had the support of various other workers,^ but the general tend-
ency for many years was to view it with skepticism.

A new period in the study of vacuoles began with the more recent
researches of P. A. and P. Dangeard,^ who again advanced a theory that

Fig. 49. — Behavior of vacuole system in certain plant cells, a-d, successive stages
in bud of Abies, e, pollen grain of Cephalotaxus. f-j, formation of aleurone grains from
vacuome in endosperm of Ricinus. k, deeply lying endosperm cell of Ricinus, with typical
aleurone grains, l—o, peripheral cells of Ricinus endosperm, showing development of
vacuole from simple aleurone grains during germination. {After P. Dangeard, 1923a.)

the vacuome is a permanent system arising not de novo but from small
units in the cytoplasm. According to these observers, the vacuome
exists at iSrst in the form of minute "metachromes"; these absorb
water, enlarge, develop into a system of canals,^ and finally become one
or more large vacuoles (Fig. 49, a to d). It was reported further that in

2 E.g., Van Tieghem (1888) and Went (1888).

= P. A. Dangeard (1916 et seq.), P. Dangeard (1922, 1923, 1927c).

* Such a system of canals had been seen several years earlier in root tips by Bensley
(1910), who, like Dangeard, found that they were not well preserved by ordinary
methods of fixation (see p. 79).

96 INTRODUCTION TO CYTOLOGY

the maturing endosperm of Ricinus the protein-containing vacuole passes
through a reticular stage and breaks up into smaller ones which, through
dehydration, become aleurone grains (Fig. 49, / to j). At the time of
germination the process is reversed : the grains absorb water and become
small vacuoles, which then coalesce to form a network and finally a
large vacuole (Fig. 49, I to o). It has accordingly been concluded by
the Dangeards that the vacuome is an autonomous system present in all
plant cells and multiplying by repeated division.

That vacuoles may arise de novo is maintained by Guilliermond, who
has made intensive studies of fungi and terminal meristems in the living
condition. In vitally stained young branches of Penicillium hypha? and
developing buds of yeast they are said to appear often without any
connection with the vacuome of the main portion. The same is reported
for Saprolegnia. Dangeard (1927c) contends that in untreated hyphse
and yeast the new vacuoles can be seen to originate from the old ones
by budding or constriction and that the vital dyes used by Guilliermond
cause certain alterations in the morphology of the young vacuome. No
evidence for origin de novo is found in Erisiphe.^ The question of the
origin of vacuoles in hyphse therefore remains unsettled.

In their studies on terminal and lateral meristems of vascular plants
Bailey and Zirkle found no evidence for the origin of vacuoles de novo,
although, as Zirkle points out, such a mode of origin in a cell whose
vacuoles are constantly fragmenting, changing their shape, and fusing
would easily escape notice.

Cell Sap. — The fluid in the ordinary vacuoles of plants is somewhat
viscous and usually homogeneous in appearance, and it quickly shows a
marked increase in viscosity when exposed to the air. It consists df
water with a variety of substances in molecular and colloidal solution.
Analyses have shown that the following elements and classes of com-
pounds occur in such saps: magnesium, aluminum, sodium, potassium,
calcium, manganese, iron, nitrogen, phosphorus, sulphur, chlorine, iodine;
organic acids (oxalic, malic, citric, acetic, tartaric, formic, etc.); alcohols;
carbohydrates (dextrose, fructose, lactose, inulin, etc.); slimes, gluco-
sides; anthocyanin and soluble yellow pigments, most of which exist in
the form of glucosides; amides (glutamin, asparagin) ; alkaloids; albumins;
certain enzymes; tannins; a variety of other aromatic compounds (see
A. Meyer, 1920). The vacuole is thus a reservoir of nutritive materials
and a depot for by-products.

Although the sap rather characteristically shows an alkaline reaction

in meristematic cells, its behavior toward vital dyes indicates a change

to a neutral or acid state with the appearance of organic acids and certain

phenolic compounds, such as tannin (P. Dangeard, 1923a). In the

* Guilliermond (19256) on Penicillium and yeast, Cassaigne (1931) on Saprolegnia,
Baache-Wiig (1925) on Erisiphe.

ERG AST I C SUBSTANCES 97

cambium of woody plants and other tissues Bailey and Zirkle^ find two
kinds of vacuoles in the same cell: relatively alkaline ones staining
reddish orange in neutral red (B-type), and markedly acid ones staining
bluish magenta with the same dye (A-type). Those of the latter type
contain phenolic 'compounds and tend to form copious precipitates.
It is observed that vacuoles in the cambium of conifers and many dicoty-
ledons are alkaline when stainable and become acid in the xylem and
phloem; whereas, in some dicotyledons they are acid and show changes
to alkalinity and vice versa in the differentiating cells. Seasonal varia-
tions also occur. Although the accumulation of basic dyes appears to
be correlated with the presence of specific substances in the vacuoles,
these workers do not favor Dangeard's hypothesis that a substance called
"metachromatin" is chiefly responsible for their staining reactions and
other activities. It is further found that colorimetric methods are very
unreliable for determining the pH of B-type vacuoles. It is this type
which occurs in Nitella and Valonia, which are so widely used in physio-
logical studies.

Nearly all of the red, blue, and purple colors of flowers, fruits, and
other plant parts are due to anthocyanin pigments in the cell sap. These
pigments are usually reddish in an acid medium and bluish in a neutral
or alkaline one, though these colors may be masked by other pigments in
the sap or plastids. The yellow flavone and flavonol pigments are widely
distributed in the cell sap of plants, but they occur in such dilute solution
that they do not give a noticeable color to tissues except in rare cases
(e.g., Antirrhinum), Yellow color in plants is usually due to plastid
pigments.'^

Frequently the cell sap contains visible solid or fluid particles in
suspension; these may be so numerous as to give the sap a milky appear-
ance. The latex found in special cells or vessel systems in certain plants
is a sap which contains a great variety of substances in solution, together
with suspended droplets or granules of oils, tannins, gum, starch, resin,
caoutchouc, and other compounds. As familiar examples may be cited
the juices of the rubber tree, dandelion, milkweed, and poppy.^

Under certain circumstances organic and inorganic substances dis-
solved in the cell sap may crystallize or precipitate. This may result
from an increase in the concentration of such substances beyond the
saturation point, often because of a decrease in the amount of solvent, as
in drying seeds; it may also be due to the appearance of some other com-
pound which precipitates them. As examples may be cited the formation

6 Bailey (1930), Bailey and Zirkle (1931), Zirkle (1932a). See also Went (1888)
and Mangenot (1927, 19296) on the presence of two vacuole types.

^ For accounts of plant pigments, see Onslow (1923), Mobius (1927), Meyer (1926),
Howard (1925), and Gortner (1929).

^ For accounts of such saps, see Czapek (1913), Meyer (1920), and Went (1926).

98

INTRODUCTION TO CYTOLOGY

of aleurone grains in maturing endosperm (p. 96), the appearance of
stained masses when certain vital dyes are used, and the formation of
crystals. Very striking alterations in the form, number, and reactions
of vacuoles have been observed in stimulated secretory and conducting
cells of insectivorous plants^ and in diseased tissue. ^° '

Carbohydrates. — The most conspicuous visible carbohydrate mate-
rials in plants are starch and cellulose. In most green plants the excess
carbohydrate elaborated by the process of photosynthesis (p. 65) is
deposited in the form of starch granules. These range in size up to
about 200m and vary considerably in appearance in different plants.

Each granule is made up of a series of
concentric layers successively depos-
ited about a center, or "hilum."
Meyer showed that in certain cases
the stratification is correlated with
the alternation of day and night and
therefore with a periodic activity of
the protoplast. Granules from wheat
grown under constant conditions are
reported not to show it (Sande-
Bakhuyzen, 1926). In case the gran-
ule starts to form near the middle of
an amyloplast it may develop sym-
metrically, but commonly it lies near
the periphery and becomes very
eccentric in form, owing to the une-
qual deposition of new material on its various sides. The amyloplast
may become greatly distended as the granule grows, often reaching
invisible thinness; in extreme cases it becomes ruptured and remains in
contact with the granule only at one side, where all new material is
thenceforth deposited. Several granules may start to develop simul-
taneously in a single amyloplast and later grow together to form a "com-
pound granule" with more than one hilum. In case the parts making
up the compound granule are enveloped in one or more common outer
layers, the granule is said to be "half-compound." The successively
deposited layers making up the granule differ mainly in water content,
the innermost layers being richest and the outermost poorest in water.
As a result of this non-uniformity the granule often splits radially when
dehydrated. Viewed through a polarizing microscope with crossed Nicols
the granule appears as a light body traversed by a dark cross (Fig. 50).
By this means starch can often be detected in very minute plastids.

9 Gardiner (1885), Dufrenoy (1927), Mangenot (1929a6), Homes (1929).
i« Dufrenoy (19286c, 19296c, 1930c, 193 lac), Dufrenoy et al. (1929de). Kuster
(1929) describes pathological changes in protoplasm.

Fig.

50. — Potato-starch grains photo-
graphed by polarized Hght.

ERGASTIC SUBSTANCES 99

As a result of his classic researches Nageli (1858, 1881) developed
the theory that the starch granule is made up of ultramicroscopic particles
("micellae"), differing in size and in the thickness of their surrounding
water films in the various layers of the granule. He finally decided that
the micellae are crystalline in nature, a conclusion supported by the work
of Schimper (1881) with polarized light. This conception of the starch
granule as a spherocrystal with radially arranged elements was adopted
and elaborated by A. Meyer (1883, 1895), who attributed the stratifica-
tion of the granule to differences in the length, thickness, closeness, and
richness of branching of the constituent needle-shaped crystals, or
"trichites." The more recent X-ray analysis by Sponsler (1922, 1923)
indicates that the granule is made up of units regularly arranged in a
space lattice; it is therefore crystalline in the modern sense of the term.
Instead of having single atoms in planes as in an ordinary crystal, it
consists of CeHioOs units arranged in curved layers.

?^o o

Fig. 51. — Carbohydrate reserves in endosperm of maize 50 days after pollination.
a, simple grains of starch from starchy maize, b, compound grains of starch from sweet
maize, c, globules of liquid dextrin from sweet maize; some of them contain simple and
compound starch grains. (After Lampe, 1931. Figure redrawn and furnished by that
author.)

Starches vary considerably in composition and in reaction to reagents.
The principal constituents are a-amylose and /S-amylose, which usually
become reddish and bluish, respectively, with iodine. In maize endo-
sperm, according to Brink and Abegg (1926), the two amyloses occur in
different proportions in waxy and non-waxy starches; furthermore, both
turn red in the waxy starch and blue in the non-waxy. It may be that
such differences are due to variations in the degree of colloidal dispersion
(W. Harrison, 1911).

In the endosperm of maize the visible reserves of carbohydrate, which
are deposited in plastids, are specific in form and composition in the
four genetic types: starchy, waxy, sweet, and waxy-sweet. In the non-
sweet maize simple grains of solid carbohydrate occur. They are com-
posed of starch in starchy maize and of red-staining "starch" in waxy
maize (Fig. 51, a). In the sweet types there are compound grains, which
are composed of starch in sweet maize and of the red-staining "starch" in
waxy-sweet maize (Fig. 51, h). In the sweet types globules of liquid
dextrin also occur in the upper central portion of the endosperm. In
sweet maize these globules may contain small simple and compound

100 INTRODUCTION TO CYTOLOGY

grains of starch, while in waxy-sweet maize they contain similar grains
of the red-staining "starch" (Fig. 51, c).^^

Cellulose is the chief constituent of the cell wall in most groups of
plants. It is not often found in the pure state in the wall, other sub-
stances, notably lignin, ordinarily being present in physical or chemical
combination with it (p. 176). The proportion of pure cellulose may be
as high as 90 per cent in cotton fiber, but in beech and oak wood it is as
low as 35 per cent. Although chiefly supporting in function, cellulose is
sometimes used as a reserve product; the hemicelluloses more often func-
tion in this capacity. Closely allied to the celluloses are the pectins. It
is a striking fact, as remarked by Sponsler (1923), that starch, cellulose,
and pectic substances, which are about the only solid materials deposited
directly and in quantity by plant protoplasm, have the same proportional
formula CeHioOs.

Glycogen, a substance of great importance in animals, is found also
in the Cyanophycese, myxomycetes, fungi, and bacteria. It may exist in
the form of viscous or solid masses in the cytoplasm, or in colloidal
solution in the vacuoles. In these plants it appears to function much
as starch does in higher plants. The many mucilages and gums which
occur so widely in plant tissues are composed chiefly of carbohydrate
materials, the former being condensation products of various sugars and
the latter these products together with complex acids (Onslow). Plant
slimes may apparently arise in different cases as modifications of cell-wall
substance, within the cytoplasm, or at the boundary between the cyto-
plasm and the vacuoles (Czapek; E. L. Smith, 1923). Sugars of several
types are of special importance in the metabolism of plants and are fre-
quently present as storage products.

Proteins. — Ergastic protein bodies are constantly being encountered
in cytological study. These may be either crystalline or non-crystalline
and may lie in the cytoplasm, plastids, nucleus, or vacuoles. In animal
eggs the storage materials commonly occur in the form of yolk globules,
or "deutoplasm spheres," which consist for the most part of relatively
complex protein compounds; globules of fat or oil are usually associated

" Lampe and Meyers (1925), Lampe (1931). For the composition of starch, see
Meyer (1895, 1913, 1920), Czapek (1913), Abderhalden (1923), Reichert (1913),
and Brink and Abegg (1926). For the structure of the starch granule, see papers of
Nageli, Schimper, Meyer, Kabsch, Binz, Dodel, Salter, Kramer, and Sponsler. For
the occurrence of starch, see Meyer (1895) and Winkler (1898). Belzung (1887) and
Eberdt (1891) deal with the origin of starch in chloroplasts and amyloplasts, respec-
tively. For accounts of "Floridean starch," see Schmitz (1882), Bruns (1894),
O. Darbishire (1896), Henckel (1901), Kylin (1913), and Mangenot (1923a). The
development of maize endosperm and its storage products is described by Lampe
(1931). The relation of genes to the production of such products in endosperm or
pollen is discussed by Brink and MacGillivray (1924), Demerec (1924), Longley (1925),
Brink and Burnham (1927a6), Brink and Abegg (1926), and Brink (1927ce, 1928,
1929a6).

ERGASTIC SUBSTANCES 101

with them. The eggs of gymnosperms may contain large globules or
shapeless masses of albuminous reserves. Refractive "metachromatic
corpuscles," composed of metachromatin, a nucleic acid compound, may
occur in the vacuoles and cytoplasm of certain algae, fungi, and Protozoa
(Guilliermond) ; these are what A. Meyer calls volutin globules. In
Meyer's opinion both chondriosomes and nucleoli are ergastic protein
masses.

Protein crystals occur widely in both plants and animals. They con-
sist chiefly of albumins and globulins and may be found in the cytoplasm,
plastids, nucleus, or vacuoles. ^^ The best known albumin crystals are
those found in aleurone grains, which are ordinarily made up of both
crystalline and amorphous protein elements. These grains occur in the
endosperm, embryo, and perisperm of ripe seeds, being
especially prevalent in such oily seeds as those of
Ricinus, Juglans, and Bertholletia. In maize and wheat
kernels they lie in the outermost layer of endosperm
cells. Aleurone grains differ considerably in color,
form, and structure. ^^ In many cases {e.g.,Pisum) the
grain consists only of an amorphous substance. In ^ig "52 — Aieu-
other cases this ground substance encloses a rounded rone grain from en-
"globoid" (in grasses), a crystal of calcium oxalate (in nuT^^m°lunlT.
certain Umbelliferse), or a large angular albuminous (After A. Meyer,
"crystalloid." The well-known aleurone grain of the
deeply lying endosperm cells of Ricinus consists of a protein ground sub-
stance, a crystalloid, and a globoid composed of a double phosphate of
calcium and magnesium together with certain organic constituents
(Fig. 52).

The development of the aleurone grain has been repeatedly studied,
especially in Ricinus. It now seems clear that the early investigators
(Maschke, Gris, Wakker) were correct in their statement that the grains
appear in vacuole-like cavities as the seed matures. They regarded these
cavities as actual sap vacuoles, a view which was again emphasized by
the Dangeards.'^'* According to this interpretation, the vacuolar material
passes through a reticular stage and breaks up into a number of small
vacuoles in which the gradually condensing constituents differentiate
as crystalloid, globoid, and ground mass. According to Mottier (1921),
aleurone formation involves the activity of permanent plastid primordia.
These aggregate in large numbers in the vacuole-like cavities, where their
combined products unite to form the aleurone grains. Vouk (1925)

^2 Protein crystals are treated at length by Meyer (1920). For nuclear crystals,
see also Tischler (1921-1922) and W6ycicki (19296).

"Hartig (1856), Maschke (1859), Gris (1864), Pfeffer (1872), Tschirch (1887),
Wakker (1888), Liidtke (1890), Guilliermond (1907a).

" P. A. Dangeard (1919, 1920ac), P. Dangeard (1920, 1921a6c, 1922a, 1923a).

102 INTRODUCTION TO CYTOLOGY

maintains that the vacuole-Uke cavities in Triticum are not true sap vac-
uoles but masses of an albuminous material which condenses about the
plastids with the aid of certain enzymes, the plastids themselves even-
tually disappearing. An analogy with starch formation by leucoplasts
is pointed out. This conflicts with the Dangeards' claim that aleurone
grains represent a stage in the evolution of the vacuolar system.

Fats and Allied Substances. — Fats and oils are of widespread occur-
rence as reserve materials in plants as well as in animals. In plants they
are found commonly in seeds, spores, embryos, and meristematic tissues,
and occasionally in differentiated vegetative parts. They are chiefly
neutral, free fatty acids seldom being present in any considerable amount.
They occur emulsified with water and appear in the form of droplets in
the cytoplasm, and occasionally in the nucleus also in animals. The
assemblage of oily or osmiophilic bodies in the cell is called the ergastome
by P. A. Dangeard.

It appears that materials of this class are ordinarily elaborated directly
by the cytoplasm, although in certain plants elaioplasts are evidently
concerned (p. 66). Mangenot (19236) attributes oil formation to phgeo-
plasts in certain brown algae. The characteristic "oil bodies" in the cells
of many liverworts appear to be formed by the fusion of small masses
arising in the cytoplasm. ^^ Cytoplasmic origin of essential oils is reported
by Popovici (1925) for glandular hairs, and Leeman (1928) describes the
passage of such oil into special preformed droplets. It has long been
the claim of Guilliermond and his associates that volatile oils have a
chondriosomal origin (Guilliermond and Mangenot, 1923).

Waxes also bear a resemblance to fats in composition and form water-
proof coatings on many fruits, stems, and leaves.

Crystals. — Crystals of many kinds occur in the differentiated tissues
of plants. They may lie in the cytoplasm, vacuoles, and occasionally
the nucleus. They may be attached to or imbedded in the cell wall;
often the cells containing them are considerably modified in size and
appearance. They are usually salts of calcium, the oxalate being
especially prevalent, and are chiefly by-products. The bundles of
needle-shaped crystals of calcium oxalate known as "raphides," which
are found in many leaves, arise in the vacuole and come to be surrounded
by a layer of mucilage^*' (Fig- 53, L). Definite homogeneous regions
in the cytoplasm are thought by Robyns to be concerned in their produc-
tion. The spherical crystalline structures known as "druses" (Fig.
53, C) are also chiefly calcium oxalate, though they have a central
mass of some more complex organic substance. The origin of the druse
and its relation to the protoplast have been a subject of controversy,

15 Pfeffer (1874), Rivett (1918). Gargeanne (1903) held them to arise in sap
vacuoles.

i« E. L. Smith (1923), Robyns (1928).

ERGASTIC SUBSTANCES

103

Jeffrey's (1922) view that the druse is formed as a casing around the
protoplast being opposed by Lloyd (1923), who contends that druses,
more than one of which may be present in one cell, arise within the
protoplasm and may later pass into the vacuole. Gaiser (1923) finds
that the stellate crystal of Anthurium arises in the vacuole, and that
after it comes to occupy nearly the whole cell the cytoplasm with the
nucleus can still be seen surrounding it.

The curious "cystoliths" in the Ficus leaf (Fig. 53, A) represent
outgrowths of the cellulose wall heavily impregnated with calcium
carbonate. In the cystoliths of certain Acanthacese the calcium may
later disappear (Linsbauer, 1921). Crystals of silica are very abundant

Fig. 53. — Crystalline and other ergastie materials in plant cells. A, cystolith in
subepidermal cell of Ficus leaf. B, crystals in Arctostaphylos. C, druse in Rheum pal-
matum. D-K, aleurone grains: D, E, from Myristica; F, from Datura: G, from Ricinus;
H, from Amygdalus; I, from BerthoUetia; J , from Faeniculum; K, from Elceis. L, raphides
from Agave leaf. AI, inulin crystals in preserved cells of artichoke. (B-K after Tschirch.)

in the thickened walls of wood cells and in many other tissues, such
as the outer portion of the Equisetum stem. In an earlier section refer-
ence was made to the protein crystals of aleurone grains and to those
frequently observed in the nucleus. Mirande (1923) states that the
radiocrystals in the epidermis of white-lily-bulb scales consist of a
phytosterol which he calls " liliosterine." The carbohydrate inulin, which
often occurs in solution in the vacuole, appears as nodules of radiat-
ing crystals in tissues which have been preserved in alcohol (Fig. 53, M).

Recapitulation: Structure of the Protoplast. — In the preceding
chapters the various structural elements of the protoplast have been
passed in review. Before proceeding further it will be well to draw
up a classification of these elements — a classification which in some
points must be regarded as provisional only. From the point of view
of convenience and present probabilities the differentiations and inclu-
sions of protoplasts may be listed as follows:

A. The Nucleus, a highly specialized organ consisting of

1. Nuclear membrane, lying against the cytoplasm;

2. Reticulum, composed chiefly of chromonemata of chro-

mosomes;

104 INTRODUCTION TO CYTOLOGY

3. Karyolym'ph, or nuclear sap;

4. Nucleolus or nucleoli; and

5. Occasional ergastic matter.

B. The Cytosome, the extra-nuclear region comprising

6. Cytoplasm, with differentiated

7. Membranes at its outer surface (plasma membrane) and

bounding the sap vacuole (tonoplast) ;

8. Plastids, characteristic of plants, with a special role in the

elaboration and storage of carbohydrates (chiefly) ;

9. Golgi material, or "Golgi zone," characteristic of animals,

and concerned in the elaboration of secretions; regarded
by some workers as ergastic;

10. Centrosomes, present in animals and some lower plants; and

11. Ergastic substances, non-protoplasmic constituents compris-

ing

(a) Chondrio somes, small masses of a substance reacting
as phospholipide and albumin, produced and used
by the protoplast; regarded by many as cytoplasmic
organs ;

(6) Vacuolar materials, in particular the cell sap of plants ;

(c) Other ergastic substances, chiefly reserves and by-
products.

C. The Cell Wall of plants, mainly ergastic in nature, but possibly

incorporating protoplasm; or
The intercellular substance of animals.

Because of their prominence in the hterature, the partial classifications employed
by P. A. and P. Dangeard, Guilliermond, and Meyer for plant cells are presented
here.

Dangeard (1923, 1929, 1931):

1. The nucleome, the nucleus or nuclei.

2. The vacuonie, comprising all the vacuoles.

3. The plastidome, comprising all the plastids.

4. The cytome, or assemblage of cytosomes [plant chondriosomes].

5. The ergastome, including the oily or osmiophilic bodies called liposomes by

Faure-Fremiet.
Guilliermond (1919 et seq.):

1. The chondriome, comparable to that of animal cells and comprising chon-

driosomes of two kinds:

(a) Ordinary ones common to plants and animals;

(6) Active ones forming plastids in green plants.

2. The vacuome, or vacuole system.

3. The lipoid granulations, which are ergastic.
[4. The nucleus.]

Meyer (1896, 1920):

1. The nucleus.

2. The cytoplasm.

3. The plastids.

4. Ergastic substances.

CHAPTER VIII
SOMATIC CELL-DIVISION

In most organisms growth involves a multiplication of cells by divi-
sion. In unicellular forms this results in the multiplication of the
organisms themselves. In multicellular forms the protoplast which is
to undergo development into a new individual initiates a series of sub-
divisions which will eventuate in the many cells of the body, or soma.
Ordinarily each subdivision involves both the division of the nucleus
by a complicated process known as mitosis, or karyokinesis, and the
division of the cytosome, called cytokinesis. These two processes may
be correlated in various ways.

In the present chapter typical somatic cell-division will be described
in its main outlines by way of preparation for detailed discussions of the
more specific and problematic points in subsequent chapters.^

Outline of Somatic Mitosis. — The remarkable character of the process
of mitosis finds its meaning in the peculiar organization of the nucleus.
The nucleus contains a number of well-individualized units, the chromo-
somes, each of which in turn has a characteristic organization. In
normal cell-division and differentiation it appears to be essential that
each chromosome should be so divided that this organization, and hence
the organization of the nucleus as a whole, will be reproduced in each
of the two daughter nuclei.

In such a tissue as that of the root tip the nucleus in the metabolic
condition consists of a bounding membrane, a mass of karyolymph, a
reticulum composed chiefly of thread-like chromosomal elements (chrom-
onemata or their persistent basis), and one or more nucleoli. As the
prophase of mitosis begins (Fig. 54), the reticulum gradually separates
into its constituent chromonemata through the disappearance of the
small strands connecting them. At first the chromonemata are thin
and crooked. They are also longitudinally double; in some cases this
split condition is visible from the very beginning of the prophase.

The double chromonemata soon become straighter and thicker. As
they do so their split condition becomes more obvious, so that they
appear as double and somewhat twisted threads imbedded in the karyo-
lymph. Their arrangement is often very irregular, but in rapidly multi-

' A useful list of works on mitosis in angiosperms is given by Picard (1913). Ruys
(1925) lists the angiosperm genera in which nuclear studies have been made. A
valuable review of researches on many chromosome problems is given by Reuter
(1930). See also the works of Tischler (1921-1922) and Schiirhoff (1926).

105

106

INTRODUCTION TO CYTOLOGY

plying nuclei they usually tend to lie more or less parallel. During this
middle portion of the prophase a second component of the chromosome,

■«|!f!|H'f-1"ft«ft

8

Fig. 54. — Semidiagrammatic representation of somatic mitosis based on studies of
species with large chromosomes. 1 , metabolic stage: the chromonemata with anastomoses
form a reticulum. 2, early prophase: chromonemata individually distinct and show
longitudinal doubleness. Note relation of certain chromosomes to nucleolus. 3, medium
prophase: matrix becoming more evident; spindle-attachment regions distinct. 4< later
prophase: matrix becoming more chromatic, obscuring chromonemata. 6, metaphase:
attachment regions all in equator of spindle formed by karyolymph. 6, anaphase: diver-
gence of the chromosomes. 7, early telophase: matrix less chromatic; nucleoli developing
in connection with certain chromosomes. 8, medium telophase: anastomoses forming
between chromonemata; karyolymph developing; spindle disappearing. 9, later telophase;
nuclei larger; reticula more fully developed. For further explanation, see text.

namely, the matrix, becomes increasingly evident. This is a substance of
uncertain history. It is probable that in some form and amount it

SOMATIC CELL-DIVISION 107

accompanies the more stainable chromonema at all times. Although it
may sometimes be distinguishable from the surrounding karyolymph
rather early, it ordinarily becomes conspicuous only when the prophase
is more advanced.

The chromosomes, each composed of two chromonemata and sur-
rounding matrix, now become markedly thicker and often shorter. In
many nuclei this involves a contortion of the chromonemata, which then
appear to be crowded or coiled within the translucent matrix. At this
period the matrix develops a strong affinity for the stains commonly
employed, so that the whole chromosome may look like a solid body with
no internal structure. As the prophase draws toward a close each chrom-
osome tends gradually to assume its final form, which may differ charac-
teristically from that of the other chromosomes of the group. At this
time the nucleolus commonly disappears, although a portion of its sub-
stance may sometimes persist through the subsequent phases.

At the end of the prophase a marked change occurs in the other
constituents of the nucleus. The nuclear membrane commonly dis-
appears, and the clear karyolymph in which the chromosomes are lying
develops a polarized arrangement which appears in fixed preparations
as a series of striations or fibrils lying parallel to the longitudinal axis
of the developing "mitotic figure." This mass of modified karyolymph
rapidly assumes the form of a bipolar spindle and the double chromo-
somes group themselves in its middle region.

In the metaphase every chromosome lies at least in part in a well-
defined equatorial plane through the spindle. If the chromosomes are
very short, they may lie wholly in this plane; if they are long, all but a
small portion of each one may lie with no regular arrangement in the
figure. The portions lying in the equatorial plane are definitely deter-
mined: each chromosome has a specially differentiated and constantly
located "attachment region" at which it manifests a peculiarly intimate
connection with the spindle in the equatorial plane. Hence in the meta-
phase and immediately succeeding stage a given chromosome usually
exhibits clearly its characteristic morphology; the attachment region is
indicated by its relation to the spindle and by other features so that the
relative length of the "arms" on either side of this region can be easily
determined. At the attachment region the two longitudinal halves of
each chromosome lie facing the two poles of the spindle; in other portions
of the chromosome they often show no such orientation (Fig. 55). In
fixed preparations the most strongly developed "spindle fibers" extend
poleward from the attachment regions.

In the anaphase the two halves of each chromosome move apart and
pass through the spindle toward its two poles, the movement beginning at
the attachment region. The shapes assumed by the various chromosomes
during this phase depend upon the location of the attachment region and

108

INTRODUCTION TO CYTOLOGY

the positions in which the remaining portions happened to He during the
metaphase. Long chromosomes, because of their trailing ends, may thus
present a rather confused picture during these phases (Fig. 56). The
attachment regions reach the poles in advance of the other portions, often
before the trailing ends have separated at the equatorial plane in the
case of very long chromosomes; such chromosomes may shorten consider-
ably after their ends draw away from the equator. Eventually all the
chromosomes lie more or less parallel in two fairly compact groups
between which the spindle substance may be seen. In certain cases
persistent nucleoli have been observed to pass poleward.

In the telophase each group of chromosomes reorganizes as a metabolic
nucleus. This involves a series of changes which in many respects are
the reverse of those seen in the prophase. During the anaphase the

12 3 4

FiQ. 55. — Development of metaphasic arrangement of chromosomes. Spindle-attachment
regions indicated by dots. P, "pole field." {.After Belaf, 19296.)

chromosome matrix is highly chromatic, but as the telophase begins this
chromaticity decreases, so that the chromonemata again become evident.
Furthermore, these chromonemata may be double as the result of a
splitting which has been shown in some cases to have taken place shortly
before the metaphase. Meanwhile the nuclear membrane, karyolymph,
and nucleoli appear. As the two nuclei grow, the chromonemata tend to
become less basichromatic and join to form the more or less continuous
and uniform reticulum characterizing the metabolic stage.

In rapidly growing tissue with the mitoses occurring in quick succes-
sion, as in the meristem of the root tip, the telophasic changes often are
not carried far enough to obscure the limits of the chromosomes in the
reticulum before the changes of the ensuing prophase begin. In such
nuclei it can often be seen that many or all of the attachment regions
occupy a rather restricted area ("pole field") at the side away from
the equator (Fig. 55), and that the parallel arrangement of the chromo-
somes assumed in the anaphase persists until the next prophase. The

SOMATIC CELL-DIVISION

109

nucleus as a whole may, however, show a change in orientation. ^ The
period between two rapidly succeeding mitoses is referred to as the
interphase.

As a result of the mitotic process, the organization characterizing the
original nucleus is reproduced exactly in the two daughter nuclei. These

Fig. 56. — Configurations often assumed by long chromosomes in anaphase. Spindle-
attachment regions indicated by dots. {After B'elar, 19296.)

nuclei are structurally alike and have the same functional capacities.
When it is remembered that all of the nuclei of the body are produced by a
succession of such mitoses, it should be obvious that the equational char-
acter of the process is of the greatest importance with respect to problems
of metabolism, development, and heredity.

Fig. 57. — Diagram of cytokinesis by cell-plate formation (first row) and by furrowing

(second row).

Cytokinesis. — The division of the cytosome is accomplished in a
variety of ways in different organisms (Fig. 57). A furrow may form at
the plasma membrane and gradually extend inward, cleaving the proto-

2 See the discussion by Belaf (19296).

110

INTRODUCTION TO CYTOLOGY

plast into two portions. In other cases a delicate membrane appears in
the cytoplasm and develops into a partition between the two resulting
cells. In the meristems of higher plants this membrane commonly forms
before the spindle substance has disappeared from the equatorial region,
so that the spindle seems to give rise to it.

In the last mentioned case the formation of a "cell-plate" appears
to be a feature of the mitotic process, but it should be pointed out that
this is probably because cytokinesis follows mitosis so closely. All
degrees of correlation between these two processes are known. No
correlation whatever is seen in certain plasmodial masses, cleavage fur-
rows developing through the cytoplasm without any evident relation
to the nuclei. In other cases the division of the cytosome is in some way

Fig. 58. — Diagram of a typical case of nuclear division and cell-division in animals.

related to nuclear influence but not to the mitotic process. Thus cleav-
age furrows or membranes may develop in positions clearly dependent
upon the positions of the nuclei, the result being definitely uninucleate
cells rather than the irregular multinucleate blocks seen in certain cases
of plasmodial division. Frequently, as in the budding of yeast and the
division of certain sporocytes, division of the cytosome follows so closely
upon nuclear division that it seems in some way to depend upon it,
without, however, involving the mitotic mechanism itself. Finally,
cytokinesis may be so intimately connected with mitosis that the two
are like a single process, the presence of the spindle between the nuclei
causing a special series of changes in the plane of cytokinesis. In the
interest of accuracy, however, the term "mitosis" should be applied only
to nuclear division; it is not synonymous with "cell-division."

Cell-division in Animals. — Cell-division in animals is fundamentally
similar to that in plants. Typically it differs, however, in the presence
of centrosomes and in the mode of cytokinesis (Figs. 58, 59). As mitosis

SOMATIC CELL-DIVISION 111

begins, the centrosome, if not already double, undergoes division, the
daughter centrosomes then moving apart. Each of them occupies the
center of a semisolid region, or aster, with conspicuous "astral rays," and
between them is a central spindle with fine fibrils. The centrosomes,
surrounded by their asters, reach opposite sides of the nucleus and
remain at the poles of the mitotic figure through the metaphase, anaphase,
and telophase. Cytokinesis is commonly brought about by a cleavage
furrow which grows inward from the periphery of the protoplast, rather
than by the differentiation of a plate-like wall as in the somatic tissues of
higher plants.

Although cell-division in animals usually differs from that in plants in
the above two respects, the distinction is by no means a sharp one.
Centrosomes are regularly present in many algae and fungi, and cytokine-
sis by furrowing also occurs in certain cells in both the lower and the higher
plant groups. The point to be borne in mind is that the essential features
of mitosis, the general results of cell-division, and the significance of
these events in the life of the organism are the same in the two kingdoms.

Duration and Periodicity of Cell-division. — The duration of the
process of cell-division, particularly that of the various phases of mitosis,
has been determined by observing living material.^ In Spirogyra, de
Wildeman (1891) found that mitosis was accomplished in 45 minutes at
12°C., but that several hours were required when the temperature was a
few degrees higher or lower. In the Tradescantia stamen hair mitosis
was carried through in 30 minutes at 45° (about the maximum tempera-
ture at which it would occur at all), in 75 minutes at ca. 25°, and in 135
minutes at ca. 10°C. In stigma cells of Arrhenatherum at 19°C. Martens
(1927c) finds that the prophase occupies 36 to 45 minutes, the metaphase
7 to 10, the anaphase 15 to 20, and the telophase 20 to 35; total, exclusive
of interphase, 78 to 110 minutes. In Sphacelaria fusca, a brown alga,
growing at 17° to 18°C., the prophase occupies 10 minutes, the meta-
phase 7, the anaphase 4, and the telophase 9; total, 30 minutes (W.
Zimmermann, 1923). W. and M. Lewis (1917) give the following figures
for mesenchyme cells of the chick growing in tissue cultures at 39°C. :
prophase, 5 to 50 minutes, usually more than 30; metaphase, 1 to 15,
usually 2 to 10; anaphase 1 to 5, usually 2 to 3; telophase up to cytokine-
sis, 2 to 13, usually 3 to 6; telophasic reconstruction of daughter nuclei,
30 to 120; total, 70 to 180 minutes. In similar cultures of choroidal
cells from the eyes of chick embryos and cartilage cells from adult fowls,
Strangeways (1922) finds the process to be more rapid at the same
temperature, complete division being accomplished in from 23 to 65
minutes, with the average at about 34 minutes. In a statistical study of
mitosis in fixed onion root tips Laughlin (1919) observes that each stage
shows a characteristic velocity reaction to temperature increments, and

2 See Tischler (1921-1922), Martens (1927c), and Jaretzky (1930).

112

INTRODUCTION TO CYTOLOGY

that these approximate the expectations based on Van't Hoff's law for
the velocity of chemical reactions.

When cytokinesis follows mitosis immediately, as it does in most
tissues, it is carried through with considerable rapidity. In higher
plants the cell-plate commonly appears during the closing phases of
mitosis and by the time the daughter nuclei are fully reorganized the
new cell membrane is well formed. In accelerated motion pictures of
living fibroblasts and animal eggs the cells, after a series of interesting
movements which escape the observer of fixed material, constrict and
complete their division with dramatic suddenness.

In root tips, which are favorite objects for the study of somatic
mitosis in plants, several investigators'* have found a periodicity in the
occurrence of cell-division. Although their results are not in close

«

«

Fig. 59. — Mitosis in a living Chorthippus lineatus spermatocyte in lA'' Ringer solution.
The change from 1 to 2 occupied 13 minutes; from 2 to 3, 21 minutes; from 3 to 4, 46 min-
utes. {After Belar, 1929a.)

agreement, they indicate that there are often about two division maxima
during a 24-hour period, one of these falling near the middle of the
day, and also that the rate of root elongation tends to be highest at the
time of minimum cell-division. Many experiments have shown that
while the periodicity in such cases may be altered by changing the
environmental conditions, there is a noticeable tendency to retain the
habitual rhythm. This indicates the action of both external and inherent
factors, whose respective roles in determining the observed results have
not been fully analyzed.

Summary and Conclusions. — Typical somatic cell-division includes
both mitosis and cytokinesis. In the prophase of mitosis the nuclear
reticulum is resolved into a number of threads; these threads, or chro-
monemata, are the chromosomal elements which together formed the
reticulum in the preceding telophase. They are double as the result of
an accurate longitudinal splitting. A less highly stainable chromosomal
matrix becomes evident about the chromonemata. In the metaphase

^Kellicott (1904), Karsten (1915, 1918), Friesner (1919, 1920), StSJfelt (1919,
1921), Fortuin (1926), Kojima (1928).

SOMATIC CELL-DIVISION 113

the thickened double chromosomes are arranged with their attachment
regions in the equator of the spindle, which is formed chiefly by the
karyolymph. In the anaphase the longitudinal halves of each double
chromosome pass toward opposite poles of the spindle. In the telophase
the chromosomes of the two resulting groups reorganize two daughter
nuclei, the chromonemata becoming joined to form the reticula while the
matrix substance becomes less evident.

Anticipating evidence to be presented in following chapters, it may be
stated further that in any particular kind of organism the chromosomes in
the nucleus occur in a characteristic number and are differentiated among
themselves in function and frequently in visible structure; they con-
stitute a definitely organized system. Moreover, this organization is
maintained by virtue of the genetic continuity of essential constituents
of each chromosome through successive nuclear generations. This means
that the chromosomes are not merely bodies w^hich are temporarily formed
by the nucleus but represent definite and persistent individuals repro-
ducing by division and passing through a complicated series of visible
changes in each nuclear cycle.

In view of these facts, it appears that the significant feature of somatic
mitosis is this: each chromosome is longitudinally divided into equal halves
ivhich are distributed to the two daughter nuclei. These two nuclei are
consequently similar to each other and to the original nucleus as regards
their chromosome complements; in other words, somatic mitosis is equa-
tional. Furthermore, since all the nuclei of the body are normally derived
through such mitoses from a single nucleus, each of these nuclei contains
descendants of all the chromosomes present in the first nucleus of the
series: the somatic nuclei are all alike in their chromosome complements,
barring, of course, the effects of occasional aberrant chromosome behavior
and other alterations to be described later. The great theoretical impor-
tance of these features of somatic nuclear behavior will be apparent when
we take up the application of cytological phenomena to the problems of
heredity and development.

Cytokinesis, or the division of the cytosome, follows mitosis quickly
in most tissues and tends to separate the various elements — cytoplasm,
plastids, chondriosomes, and vacuoles — more or less equally according to
their arrangement in the protoplast. Occasionally some of these elements
are passively divided. The daughter cells are initially similar in architec-
ture and functional capacity. The course of their further differentiation
depends largely upon their position in the developing whole.

CHAPTER IX
THE MORPHOLOGY OF THE CHROMOSOMES

As they pass through a mitotic cycle, the chromosomes undergo a
remarkable series of changes in form and structure. Nevertheless,
in the metaphase and anaphase, when they are most condensed and
clearly evident as individuals, they exhibit many characteristics of
size and form which have proved useful not only in determining the
functions with which they are associated, but also in comparing related
species and hybrids. For the study of chromosome morphology in
vascular plants the root tips and dividing microspores are particularly
favorable. In animals the tissues of young embryos and the sperma-
togonia have been most frequently used. Different fixing reagents
may produce a considerable variation in the appearance of chromosomes,
but the studies of S. Nawaschin, Lewitsky, Taylor, and others have
furnished us with methods which are very trustworthy when properly
employed.^

Size and General Form. — As they appear in the metaphase or
anaphase of somatic mitosis, the chromosomes of different organisms
show a great range in size. In some cases they are extraordinarily
minute, being less than Iju long, while in others they may reach a length
of 20iu or more; the breadth may vary likewise. Some natural groups,
such as fungi and certain insect orders, have small chromosomes as a
rule, while in others, notably amphibia, grasshoppers, and liliaceous
plants, they are characteristically large. Within narrow circles of
affinity, chromosome size sometimes affords evidence for probable
taxonomic relationship. In this connection it should be noted that the
size may be somewhat altered by cultural conditions and microtechnical
treatments.

The chromosome is typically an elongated body. Sometimes very
small chromosomes may appear practically spherical at metaphase or
anaphase, but they are usually elongated in the prophase. Moreover,
studies on larger chromosomes lead to the inference that even the smallest
spherical chromosome contains an elongated chromonema. The essential
point is that every chromosome adequately known possesses a longi-
tudinally differentiated organization. This differentiation belongs
primarily to the chromonema, but it is usually evident also in the entire
metaphase chromosome with its abundant matrix.

' For an account of the development and present status of our knowledge of
chromosome morphology, see Lewitsky (1931a); see also 19316 for fixation.

114

THE MORPHOLOGY OF THE CHROMOSOMES

115

Noteworthy in this connection is the fact that the characteristic
size differences shown by the several chromosomes of the same nucleus
are almost wholly a matter of length; commonly the diameter of all of
them is the same. This suggests that chromosomes are composed of
smaller units arranged in a row, and that the longer chromosomes of a
group have more units than the shorter ones. This interpretation may
not be universally applicable, but genetical evidence to be presented
in later chapters indicates its general validity.

Spindle -attachment Region. — The metaphase or anaphase chromo-
some usually shows at some point a differentiation which has commonly

Fig. 60. Fig. 61.

Fig. 60. — A chromosome with submedian spindle-attachment region passing to the pole
in anaphase. The shorter arm has a "secondary constriction."

Fig. 61. — Diploid chromosome complement at metaphase in root tip of Vicia faba.
Spindle-attachment regions of all chromosomes near equator. Nucleolus-forming regions
are by the "secondary constrictions" above and below. In this strain one pair of short
chromosomes has conspicuous "constrictions" also (left and right). X1750.

been referred to as a "constriction," since it appears as a relatively
slender region in most preparations showing it clearly in these stages
(Fig. 60). Careful studies have shown that the region in question
differs from the rest of the chromosome in its structure and achromatic
nature, and not merely in apparent diameter. In some preparations,
especially of the prophase, it may appear as wide as or even wider than the
adjacent portions; hence the term "constriction" is not truly descriptive.
Some chromosomes have two or more achromatic regions. It is a
striking fact that in a given chromosome these have definite and con-
stant locations, 2 although they may be very differently placed in different
chromosomes.

2 Exception should of course be made for individuals or races in which their posi-
tions differ because of translocation, inversion, or other alteration. See McClung
(1917), Carothers (1921), King (1923), Helwig (1929); also McClintock (1931) on
Zea. It was found by Sakamura (1920) that chloral hydrate shortens and thickens
the chromosomes, thus accentuating the "constrictions." The effects of fixation
have been studied by S. and M. Nawaschin, Lewitsky (see 19316), and others.

116 INTRODUCTION TO CYTOLOGY

It was observed by Agar (1912) in a fish that it is at an achromatic
"constriction" that the chromosome estabHshes connection with the
spindle in the metaphase and separates first in the anaphase. This
is now known to be true of chromosomes generally. Hence the region
functioning in this manner has been variously called the "fiber-attach-
ment point," "insertion region," "primary constriction," "kinetic
constriction," "attachment constriction," and "Trennungstelle" (separa-
tion place). ^ Chromosomes with apparently terminal spindle attach-
ment are said to be telomitic; those with attachment elsewhere are
atelomitic (Carothers, 1917).

As the result of the definite location of the spindle-attachment
region, each atelomitic chromosome has two main segments, or "arms,"
with a characteristic length ratio. This is easily seen in side views of
anaphase figures, also in polar views of metaphase ones if the chromosome
is not too long. Such a chromosome passes poleward as a V or V, the
apex leading, whereas a telomitic one appears as an unbent rod. The
same mitotic figure may include all types. It has been held by certain
investigators^ that all chromosomes are probably two-armed, "telomitic"
ones having an extremely minute second arm which easily escapes
observation. Supposedly telomitic chromosomes have been shown in
some instances to have their attachment region slightly back from the
end, and in other cases a minute body seen at the end may represent the
second arm; but that strictly one-armed chromosomes do not exist is
at present improbable. What may have been the primitive location
of the attachment, and how other types have arisen, are interesting
subjects for speculation.

The structure of the spindle-attachment region has been the subject
of some study. It may appear clearly in the prophase as a region in
which highly stainable matter is lacking. It may be straight sided or
somewhat swollen in some preparations (Fig. 152), and in certain instances
it is known to have a characteristic length (Fig. 188). It appears to
be homogeneous except for minute granules^ at the middle point (Figs.
62, 63). The reaction which "attaches" the chromosome to the spindle
seems to center in these "kinetic bodies," for it is from them that the
strongly developed "spindle fibers" appear to extend in fixed prepara-
tions, and it is they which take the lead in the anaphasic movement.
They have been observed at the extreme end of the attachment region

^ The convenient term kinetochore ( = movement place) has been suggested to the
author by J. A. Moore. The use of this term is recommended.

^ S. Nawaschin (1916), Delaunay (1929), Heitz (1928a), Lewitsky (1930, 1931a).
Chromosomes with apparently equal arms are termed isobrachial and unequal armed
ones heierobrachial by Sorokin (1929). Lewitsky (1931a) calls those with a small,
rounded second arm "cephalobrachial," or "headed" chromosomes.

' Observed by S. Nawaschin (1913, 1916), Belling (19286), Belaf (1929a), Tran-
kowsky (1930a), Sharp (Fig. 63), and others.

THE MORPHOLOGY OF THE CHROMOSOMES

117

of "telomitic" chromosomes. In Trillium delicate strands extend out
to the granules from the single arm of the telomitic chromosome and
from both arms of atelomitic ones (Fig. 63). A comparison of these
two types strongly suggests that in the former the attachment point is
truly terminal. What relation the delicate strands may bear to the
chromonemata is difficult to determine, especially since the chromosome
tends to stain very deeply on either side of the attachment region.

The spindle-attachment region, then, is a well-differentiated feature
of the chromosome: it is a region specialized with reference to the meta-
phasic arrangement and anaphasic separation of double chromosomes

\f

-^

c /

I

Fig. 62. — Kinetic bodies at spindle-attachment regions. A, in GaJtonia microspore.
[After S. Nawaschin, 1927 (1913).] B, prophase in Najas major; C, anaphase in Crepis
palestina. (After Trankowsky, 1930a.)

Fig. 63. — Submedian, subterminal, and apparently terminal spindle-attachment regions

in Trillium grandiflorum.

(p. 107) and is not to be confused with other achromatic regions or
"constrictions." That it persists through the interphase is indicated
in Impatiens, where it can be seen at all stages (Fig. 24, B). What is
known about the behavior of fragmented chromosomes (p. 317) suggests
that spindle-attachment regions cannot be formed anew. In all prob-
ability the regular occurrence of one such region in every chromosome
is due to the eventual loss of fragments without them because of their
inability to interact normally with the spindle, and to the irregular
behavior of any chromosome which happens to get an extra attachment
region through translocation. Hence the constancy and the regular
behavior of a group of chromosomes are directly dependent upon the
attachment regions. Whether or not a chromosome may fragment

118 INTRODUCTION TO CYTOLOGY

directly through the attachment region, giving two chromosomes with
terminal attachment regions, is not certainly known, but the possibility
is strongly suggested by certain aberrations in Zea (p. 317).

Nucleolus-forming Region. — In addition to the spindle-attachment
region the chromosome may exhibit one or more other differentiations
affecting its general morphology. Among these perhaps the most
interesting is the nucleolus-forming region, which seems as a rule to be
conspicuously developed in but one chromosome of a set. Although
it is reported to occupy the end of the chromosome in certain cases, it
is more commonly situated in a non-terminal position. Moreover,
its location is normally constant in a given race; like the spindle-attach-
ment region, it is a definite "organ" of the chromosome.

The structure of this region is best known in sporocytes of Zea Mays,
where it appears at certain stages as a broad and chromatic region of
chromosome VI immediately adjacent to an achromatic region setting
off a "satellite," or small portion of the chromosome arm (Figs. 65, 170).
It is the chromatic region that is active in the accumulation of the
nucleolar matter in the telophase. This is shown by the fact that in
strains lacking the satellite, the achromatic region, and a portion of this
chromatic region, the nucleolus is seen to arise from the remaining
portion of the chromatic region. Normally, when chromosome VI is
present in its entirety, the growth of the nucleolus causes the achromatic
region to become extended as a slender filament lying over the nucleolar
surface, so that the satellite may be situated at some distance from the
remainder of the chromosome arm. In the ensuing prophase this
filament may shorten more or less as the nucleolus decreases in size and
disappears, but it remains visible as a conspicuous achromatic region,
or "secondary constriction."^

In most of the papers on this subject so far published it has been
stated that the nucleolus is associated with the "secondary constriction"
and satellite, the active chromatic region not having been recognized.
Thus S. Nawaschin and his associates'^ observed that during certain
phases of mitosis, notably the late prophase, the satellites lie on the
surface of the nucleolus (Fig. 64). In early prophases the satellite may
appear like any other equal portion of the extended chromosome (Fig.
65), but during the condensation of the chromosome the satellite typically
becomes a small spherical body (Figs. 64, 67, 72). In Viciafaha, investi-
gated by Heitz (1931a6), the somatic chromosome complement (Fig. 61)

* Data in thi.s paragraph from McClintoek (1931& and unpublished).

7 S. Nawaschin (1912, 1915, 1916 et seq.), Sorokin (1924, 1929), Baranov (1926),
Senjaninova (1926). SatelHtes were first described by S. Nawaschin (1912) for
Gallonia candicans. Wenrich (1916) observed the attachment of the nucleolus to a
certain portion of a chromosome in Phrynotettix. Kuhn (1928a) reviews the subject of
satellites and lists the plants in which they have been reported.

THE MORPHOLOGY OF THE CHROMOSOMES

119

includes two long members with conspicuous achromatic regions setting
off segments larger than those usually called satellites. Owing to the
position assumed by the chromosomes in late anaphase these two regions
lie at a certain level in each telophase nucleus, and a nucleolus develops
near each of them. If the two chromosomes concerned lie far apart
in the nucleus the two nucleoli remain separate, but if they lie near
each other the nucleoli may come into contact and fuse. Hence some
nuclei in the root show two nucleoli wdiile others show one, and as a
rule sister nuclei recently formed by division are mirror images of each
other. This feature is represented in Fig. 54. In Zea roots the nucleolus
is seen to be connected with the developing chromosomes at two points

Fig. 64.

Fig. 65.

Fig. 64. — Satellited chromosomes attached to nucleolus in Galtonia. [After S.
Nawaschin, 1927 (1913).]

Fig. 65. — Chromosome VI (synapsed pair) attached to nucleolus in microsporocyte of
Zea Mays. The satellite projects upward from the chromatic swelling against the nucleolus.
A short distance below the swelling is the spindle-attachment region, which here appears
like a gap. Note chromatic knob toward left end. Compare Fig. 170. {After McClintock,
1931b, 1933.)

(Zirkle, 19286); these are presumably the nucleolus-forming regions of
the two chromosomes VI.

Because of the mode of their formation, it seems that nucleoli are as
a rule connected with certain parts of certain chromosomes in the nuclear
reticulum. At present too little is known to warrant anything more
than suggestions regarding the significance of this phenomenon. It
has long been thought by many observers that some nucleolar constituent
passes into the chromosomes in the prophase and out of them in the
telophase. This view is supported by the appearance of nucleoli as
the chromosome matrix diminishes in amount and loses its chromaticity
in the telophase, their disappearance as the chromaticity returns and
the matrix becomes abundant in the prophase (Martens, 1922), and
the results obtained with special fixing reagents (Zirkle, 19286). Fre-
quently it seems that only one of two principal nucleolar constituents
functions in such a manner (Selim, 1930). If there is such a transfer

120

INTRODUCTION TO CYTOLOGY

of substance, microchemical tests indicate that it cannot be nucleic
acid, "chromatin," or "karyotin." Heitz, who reports that in Vicia
both nucleolus and secondary constriction react negatively in the Feulgen
test for nucleic acid,'^ inclines to the view that the nucleolus is formed
by a substance existing throughout the nucleus and later accumulated
near the constriction. In Zea sporocytes it is clear that the nucleolus
bears a very close relation to the chromosome matrix (Fig. 65a). An

i i -^

AT

n

Fig. 65a. — Chromosome matrix and nucleolus in Zea. A-D, four stages in prophase
of second meiotic division in microsporocyte. The nucleolus and the matrices of the
several chromosomes are at frst confluent. The distinction between matrix and chro-
monema shows well in B and C. E, normal microspore with one principal nucleolus.
F, microspore lacking the region of chromosome VI specially concerned in nucleolus
formation; many scattered nucleolus-like bodies present. {After McClintock, 1934.)

association of nucleolar behavior with the transfer of products of genie
activity to the cytoplasm has been suggested by Zirkle (19286) and
Fikry (1930) (see p. 309).

The observations and hypotheses cited above indicate that certain
chromosomes of the complement have regions specialized in connection
with the transfer of material to and from them during the nuclear cycle
(Haase-Bessell, 19286). Accordingly, it might seem that every nucleus
must have at least one such chromosome in order to pass through a

* Negative tests for the nvicleolus are also reported by Wermel (1927), Yamaha
(1932), Shinke and Shigenaga (1933), and others.

THE MORPHOLOGY OF THE CHROMOSOMES 121

normal cycle, this in turn suggesting why practically every chromosome
set, well studied, shows at least one achromatic region, or "secondary
constriction," which so often lies near a nucleolus-forming region.
It is known, however, that nucleoli may develop at other points in
the chromosome set under certain circumstances, as when the nucleolus-
forming region has been removed in the deletion of a portion of the
chromosome. Thus when a strain of Zea Mays in which one member
of chromosome pair VI had lost this region produced microspore quartets,
it was found that two spores of each quartet had the region and a single
large nucleolus, while the other two had no such region and a considerable
number of small nucleolus-like bodies (Creighton) (Fig. 65a). These
small masses of substance, which would normally contribute to the forma-
tion of a single nucleolus, may appear at one or more points on each
chromosome. Heitz (19316) reports that when a small extra nucleus
is formed by a lagging chromosome in Vicia, it may contain a small
nucleolus in addition to the two normal ones in each main nucleus.
From such facts it may be concluded that all of the chromosomes give
off a material during the telophase, and that under normal circumstances
this material is incorporated in typical nucleoli formed in close associa-
tion with specialized regions of certain chromosomes.

Other Specialized Regions. — Besides the spindle-attachment region
and the nucleolus-forming region, other differentiations can frequently
be observed in the chromosomes at metaphase and anaphase. These
may sometimes appear as "constrictions" (Fig. 61), but very little is
known about the functions they may perform or concerning the number
of kinds of them which may be present in a chromosome set. It seems
improbable that constrictions are necessarily places where fragments of
chromosomes have formerly joined,^ although translocated pieces in
Drosophila are sometimes set off by narrow regions.

The Chromosome Complement. — In any given kind of plant or
animal each nucleus contains an outfit, or complement, of chromosomes
composed of a certain number ^° of members showing characteristic
differences in form and function. As a general rule, the nucleus of an
egg before fertilization contains a complement made up of one each of
several kinds of chromosomes. Such a complement is called a set, or
genom. Because each kind of element is represented but once, a nucleus
(or organism) with such a chromosome outfit is said to be mono-ploid

^ M. Nawaschin (1931c), Lewitsky and Araratian (1931).

1" The known chromosome numbers in all plant groups are listed by Tischler
(1927, 1931). Gaiser (1926, 1930) gives lists for angiosperms. See also Aase and
Powers (1926) and Sisa (1929) for crop plants, Stolze (1926) for grains, Avdulow
(1931) for Gramineae, Kawakami (1930) for Leguminosse, and Kihara, Yamamoto,
and Hosono (1931) for plants cultivated in Japan. For animals, see Bresslau and
Harnisch (1927) and Harvey (1916, 1920); also Oguma and Makino (1932) on verte-
brates. Wilson (1925) gives a fairly extensive list for plants and animals.

122 INTRODUCTION TO CYTOLOGY

(or often haploid) . The set is evidently a definitely differentiated group
of elements all of which are usually necessary for normal development.
In the male gamete there is a similar set of chromosomes. After the
union of the gametes, therefore, the fusion nucleus of the zygote contains
two sets of chromosomes. Since every kind of chromosome is present in
duplicate, the nucleus is said to be diploid. All of the nuclei of the higher
plant or animal body which develops from the zygote are derived by a
series of equational mitotic divisions from the zygote nucleus; hence they
are all diploid.

In the case of animals, gametes are formed when the individual
becomes sexually mature; in this process the diploid zygotic number of
chromosomes is reduced to the monoploid gametic number. This is done
in such a manner that each gamete contains one complete set of elements,
although this set may include elements from both of the original sets
(Chapter XVI).

In vascular plants, bryophytes, and some thallophytes the situation is
somewhat more complicated. The zygote and the sporophyte body into
which it develops are typically diploid. A reduction to the monoploid
number occurs when reproductive cells are formed, but in such plants
these are spores rather than gametes. Each spore develops into a body
of another type, a gametophyte with monoploid nuclei. Eventually the
gametophyte produces gametes without further change in chromosome
number, and these unite to form new zygotes. Hence such a plant life
cycle differs from that of a higher animal in having two kinds of repro-
ductive cells (spores in addition to gametes) and a monoploid body
developing between sporogenesis and gametogenesis. It shows an
"alternation of generations" which is usually, though not always, asso-
ciated with an alternation of monoploidy and diploidy in the nuclei. ^^
Chromosome morphology in plants has been studied most in root tips,
where two chromosomes of each kind are present, but it is often advan-
tageous to use gametophyte tissue or spores because a monoploid group
is easier to interpret, other things being equal.

Since the description of the chromosomes of Brachystola by Sutton in
1902, morphological differences in the members of the complement have
been reported for a considerable number of animals belonging to various

^1 The two nuclear phases, irrespective of their relation to the "generations,"
have been called gamophase and zygophase (Winkler). It is generally supposed that
in the course of evolution the monoploid condition was first developed through a
differentiation of the multiplying nuclear elements, the diploid condition arising as a
result of fusion and necessitating a reducing process. The diploid generation is
thought to have developed as the latter process became delayed in the cycle and to
have hastened the evolution of diverse types by affording larger opportunity for the
formation of new combinations through meiosis and syngamy (Svedelius, 1921).
The diploid condition is also advantageous in affording a measure of protection
against the detrimental effects of unfavorable recessive mutations.

THE MORPHOLOGY OF THE CHROMOSOMES 123

natural groups, especially the insects. ^^ In Drosophila melanog aster, so
extensively used in genetical studies, the set is made up of four unlike
members: one medium-sized chromosome with terminal spindle-attach-
ment region (chromosome I), one large chromosome with median attach-
ment (II), one slightly larger chromosome of the same type (III), and
one very small chromosome (IV) (Fig. 71). In somatic cells and imma-
ture germ cells there are two such sets ; as is characteristic of the Diptera,
the corresponding chromosomes (the "homologues") actually lie near
each other in pairs. ^^ The functional characteristics of these chromo-
somes will be discussed in a later chapter.

The morphology of the chromosome complement has been described in
a large number of plants, particularly among the angiosperms. Several

Fig. 66. — Photographs of Zea chromosomes in late prophase of mitosis in microspore.

a, monoploid group; note spindle-attachment regions in chromosomes in good focus.

b, chromosome I. c, chromosome IV, showing "knobs" near lower end. d, chromosome
X. Compare Figs. 152 and 170. {Photographs by McClintock.)

well-known illustrative examples are the following. In Zea Mays^* the
monoploid group comprises 10 chromosomes. These can be distinguished
from one another on the basis of absolute length, the relative length of
the two arms (each has a submedian spindle-attachment region), and
other structural characteristics visible at certain stages (Figs. 66, 152, 170).
One of them, number VI, has a conspicuous achromatic region setting
off a satellite. In some races certain members of the set possess definitely
located chromatic "knobs" which differ in character from large chro-
momeres; these aid further in identifying the various members. It is
known that the chromosome sets of different races of maize vary in
certain minor structural details, some such variations presumably being
correlated with genie differences. Moreover, certain variations should
also be expected in view of the observed fact of occasional translocations,

12 McClung (1905 et seq.), Harman (1915, 1920), W. R. B. Robertson (1916 et
seq.), Carothers (1917, 1921), Metz (1914 et seq.), and many others.

" Bridges, Morgan, Muller, Metz, Dobzhansky, Painter.

1^ Kuwada (1919), Fisk (1925, 1927), Longley (1927c), Randolph (1928 et seq.),
McClintock (19296 et seq.).

124

INTRODUCTION TO CYTOLOGY

deletions, and inversions (Chapter XVIII). The same is doubtless also
true of many other species in which a "typical" or "standard" chro-
mosome set has been described.

In Datura stramonium there are 12 chromosomes in the set. These
vary somewhat in different races. In "line lA " there are one very long,
two long, five large medium, two small medium, one short, and one very
short members. ^^ According to Lewitsky, all 12 may be distinguished
on the basis of size, arm ratio, and the presence of small rounded
segments. In Pisum sativum the seven pairs in the root cells are distin-
guishable^^ (Fig. 67, A). In Vicia faba there are five pairs with subter-

Fig. 67. — Somatic chromosome complements in various higher plants. A, Pisum
sativum. {After Lewitsky, 1930.) B, C, Crepis capiUaris, after regular treatment and
after shortening by cooling. (After Delaunay, 1930.) D, Allium allegheniense, with
translocated fragment on one member. {After Levari, 1932.) E, Najas major. {After
Tschernoyarow, 1914; see also Midler, 1912, Winge, 1927a, and Takamine, 1927.) F,
Nicotiana alata var. grandiflora. {After Avery, 1929.)

minal spindle-attachment regions and one much larger pair with a
median attachment region and a conspicuous "secondary constriction^^
(Fig. 61). The chromosome set of Crepis capiUaris (= virens) consists
of a large chromosome with its attachment region between the middle
and end, a medium-sized one with very unequal arms and a satellite, and
a small one with unequal arms. Hence the somatic cells show three
distinguishable pairs ^^ (Figs. 69; 72, B). In Nicotiana alata var. grandi-
flora the nine pairs of chromosomes fall into five classes on the basis of
their morphology (Fig. 67, F).

In a large number of plants and some animals the chromosome com-
plements of gamete and zygote do not have merely one set and two sets of

1^ Belling and Blakeslee (1922 el seq.), Blakeslee, Belling, Farnham, and Bergner
(1922), Lewitsky (1930, 1931a). In much of the literature on Datura the term "set"
is used rather for any group of homologous chromosomes, a diploid plant having 12
"sets" of two, a triploid 12 "sets" of three, and so on.

"Lewitsky (1930), Marshak (1931).

" Sharp (1913, 1914a), Sakamura (1914, 1915, 1920), Maeda (19306). For other
species of Vicia, see Sweschnikowa (1927a6, 1928, 1929).

IS Rosenberg (1909a, 1918, 1920), de Smet (1914), Collins and Mann (1923),
Mann (1925), M. Nawaschin (1925afe, 1926), W. R. Taylor (1925c), Hollingshead
(1930c), Lewitsky and Araratian (1931).

THE MORPHOLOGY OF THE CHROMOSOMES 125

chromosomes respectively, as in the foregoing "diploid" types, but other
numbers, such as two and four sets (" tetraploid " types), three and six
sets ("hexaploid" types), and so on. Such individuals or species are
said to be polyploid. This phenomenon and its significance are to receive
detailed consideration in Chapters XX to XXII.

The Arrangement of the Chromosomes in the Mitotic Figure. —
As a general rule it seems that the various chromosomes of the comple-
ment have no constant relative position in the nucleus or mitotic figure.
A comparsion of their positions in a number of metaphases in the same
plant usually shows that the arrangement varies greatly. It frequently
happens, however, that the arrangement is the same in figures which lie
near each other, as in the same row of cells in a root tip, or in neighboring
sporocytes. This is easily understood when it is remembered that the
halves of the chromosomes pass rather directly to opposite poles from
the equatorial plane and thus form similar patterns in the sister nuclei
in the telophase. If the next mitosis follows soon, this pattern may be
retained through another nuclear and cell generation. As the division
rate becomes retarded and the cells compared come to lie farther apart,
the arrangement is somehow altered. To what extent the chromosomes
may change their relative position in interphasic and metabolic nuclei is
not known, but irregularities in their grouping at the end of the anaphase
seem to be in part responsible for the alteration observed.

What has been said above applies particularly to the elongated somatic
chromosomes of plants whose morphology has been most studied. An
examination of the chromosomes in certain sporocytes, where they are
short and well separated from one another in the developing mitotic
figure, shows that they tend strongly to assume arrangements like those
of floating magnets of the same relative dimensions; they behave as if
they were all acting under a mutual repulsion, especially of their spindle-
attachment regions. The most stable arrangement occurs most
frequently, other less stable ones being due to such modifying factors
as the viscosity of the medium and the time required to assume the
arrangement.^^

In animals also, particularly in the insects, cases are known in which
the chromosomes show a more or less constant and characteristic arrange-
ment in the metaphase. Often the smaller chromosomes lie in the middle
of the figure with the larger ones around them (Fig. 215), or they may
form a circle with certain members inside or outside it.^ Here again
the phenomenon is best displayed where the size and spacing of the
chromosomes are such as to permit their free movement as the metaphase
stage develops. In the Diptera, as already mentioned, the chromosomes

i^vuwada and collaborators (1929). Cf. R. S. Lillie (1905), Cannon (1923),
Midler (1912), and Heimans (1928).

2" See Wilson (1925, various figures in Chap. XI; also 1932).

126 INTRODUCTION TO CYTOLOGY

of the diploid complement tend to show a very regular paired arrange-
ment (see Metz, 1916). Similar but less distinct pairing is sometimes
reported in plants. An especially interesting case is described by Robert-
son (1930) in Paratettix texanus, a grasshopper (Fig. 68). In individuals
produced by the union of two gametes in the usual w^ay the two parental
chromosome sets tend to remain distinct in the developing tissues,
whereas in individuals produced by parthenogenesis the two sets (evi-
dently formed here by chromosome division in the incomplete maturation
of the egg) have a distinctly paired arrangement. In both cases the

configuration in the egg as it begins development is
maintained through the successive cell-divisions.

All of these facts suggest that there are always
factors, some of them purely physical and some involv-
ing the chemical and genetic constitution of the
chromosomes, which tend to give the members of a
complement a certain arrangement, and that if these
factors were always given unrestricted opportunity
for action each type of complement might always
exhibit about the same characteristic configuration.

Chromosome Complements of Related Organisms.
The discovery of the relative uniformity of the number
of chromosomes in an individual or a species led to the
5^ g determination of the number in many organisms
Fig. 68. — Chro- belonging to all of the major groups. A certain
uxZ^s.^ °A^iTomhi- amount of speculation regarding the general phylogen-
parentally produced etic significance of chromosome number has been
Iri'^'paTses*^^^^^^^^ indulged in, but students of the subject have reached
the parental sets. B, the conclusion that the data at hand do not warrant
ca°lS prfd^ucld^TiTdi- ^^^y broad generalizations. So far as the large
vidual. {After w. groups are Concerned, there appears to be no correla-
son, .) ^^^^ between taxonomic position and structural com-

plexity, on the one hand, and the number, length, width, or volume of
the chromosomes, on the other. It is, however, generally agreed that
within restricted circles of affinity the number of chromosomes, and
especially their size and form, may often afford important evidence in
the determination of genetic relationships.^^

The type of chromosomal complex characteristic of any individual or
group of allied forms may be called its karyotype (Lewitsky, 1924). ^^

21 McClung (1908), Strasburger (19106), Farmer and Digby (1914), Tischler
(1916, 1921-1922), Winge (1917), Gates (19206, 1924a6), Marchal (1920), Meek
(1920), Heilborn (1924). See especially Lewitsky (1931c) for chromosome morphol-
ogy. See also footnotes, pp. 23-28.

22 The term was originally used in a more restricted sense by Delaunay (1922).
See the discussion by Lewitsky (1931c).

THE MORPHOLOGY OF THE CHROMOSOMES 127

^^ Crepis pulcherrima

'^ ^ ^5 CD E

i/Ul-^v nil

Crepis grand! flora ^ ^ ., ^./•^/./-. ^'//-^/r^

m. # ^'^i^/j *'/>:

^'?i/i:a-^^i:,i

Crepis Dioscoridis ^Ai \ 1^^ €£z Crepis rhoeadifolia

It" tli/li/

Crepis fecforum ''' '

fl B C D E ^ ^ ^^^mCz

I

^^^^ Crepis rubra {\^

^1 Crepis parvi flora

D,

'•*i/\ 1^ ^ ^B C D E]

^'e.M ■ I • ^^ ^ A ^B C D E

'B,

ill ""' ^^ ^ 1^ ^

Fig. 69.— The chromosomes in 10 species of Crepis. Diploid complement in root cell
at left; monoploid set at right. {Ajter M. Nawaschin, 1925a.)

128

INTRODUCTION TO CYTOLOGY

The diagrammatic representation of a karyotype, as in Fig. 70, is called
an idiogram (S. Nawaschin, 1921). One of the most important lines of
investigation in modern cytology is that in which the nuclear consti-
tutions of related organisms are studied through comparisons of their
idiograms. Such studies afford invaluable evidence supplementing that
of the geneticist, taxonomist, and student of phylogeny.

In Crepis, which has come to be one of the most important genera for
investigations in this field, -^ there are many species with only three, four,
or five pairs of chromosomes. These appear to be of about five dis-
tinguishable kinds as regards size and shape, each species having a
characteristic complement composed of from three to five of these chromo-
some types (Fig. 69). It is observed that a chromosome of a given type

M./ongf

A B C) C^ C3 ol, 0I2 £^3 <^4

M.fen

%%%%

A B C| C2 Cj d| dg ^z "4

M. monsir.

Illilfiii

A B C| C2 C3 ol| d2 f^i 0)4

Fig. 70. — Somatic chromosome complements of three species of Muscari: longipes, tenui-
florum, and monstrosum. {After Delaunay, 1926.)

may vary considerably in length in the complements of the different
species. The fact that the order of the species, when arranged in a series
on the basis of a progressive lengthening or shortening of a given chro-
mosome of the set, may differ from the order in a series similarly arranged
for a different chromosome is taken to mean that the chromosome set is
not a simple unit, but is rather a harmonious system of autonomous
entities which are in some measure independent of one another in their
evolutionary alteration.

In Muscari, Delaunay (1926) finds that the idiograms in three species
differ chiefly in the absolute and relative length of the members (Fig. 70)
and believes that in many such cases a gradual shortening of the chromo-
somes may have occurred during the evolution of the genus. Studies
on the karyotypes of several groups, notably the Helleborese,^^ have led

23 See especially M. Nawaschin (1925a, 1926), Hollingshead and Babcock (1930),
and Babcock and Nawaschin (1930).

^^Lewitsky (1931a); also Senjaninova-Korczagina (1930, 1931) on ^gilops and
Vicia, Avdulow (1931) on Agropyrtim, and Lewitsky and Tron (1930) on Bellevalia
and Muscari.

THE MORPHOLOGY OF THE CHROMOSOMES 129

Lewitsky to the view that in various tribes and genera there has been a
progressive shortening of one arm in many of the chromosomes, primitive
members of a group having mostly isobrachial chromosomes and derived
members mostly heterobrachial ones. In Drosophila the idiograms
in the various species bear a general resemblance to one another but
show characteristic minor differences-^ (Fig. 71). Even within a Linnsean
species the idiograms may not be alike in all individuals. Thus in
Rumex acetosa the plants fall into several classes on the basis of the

H ir 11 H

p D. melanogaster 6? O.Simulans O.virilis

#;.%

4^4^

O.funebris 0- willistoni o D. obscura <?

Fig. 71. — The somatic chromosome complements of several species of Drosophila.
Pairs known to be sex-chromosomes shown in solid black; those presumed to be are marked
with cross lines. {After Metz, Moses and Mason, 1923.)

karyotype. Such cytological studies have now been made on a con-
siderable number of genera-'' and are to receive further consideration
in Chapter XX.

Groups of related genera, as well as the related species of a genus,
often have the same general karyotype. For example, in Haworthia,
Gasteria, and Aloe the complement consists of four long and three short
pairs, with minor peculiarities in each genus" (Fig. 72, E to G). A
notable example of similarity of chromosome complements throughout

25 Metz (1914, 1916), Metz and Moses (1923), Metz, Moses, and Mason (1923),
Frolowa (1926), Frolowa and Astaurow (1929).

"^^E.g., Vicia (Sweschnikowa, 1927a6, 1928, 1929; Heitz, 1931; Senjaninova-
Korczagina, 1932); Trilicujn (Kagawa, 1927a6, 1929a6c); Pellia (Heitz, 1928a6);
jEgilops (Senjaninova-Korczagina, 1930); Mecosfethus (McClung, 1928ab); Rumex
(Kihara and Yamamoto, 1931); Nigella, Delphinium, Aconitum, and other Helle-
borese (Lewitsky, 1931c).

27 W. R. Taylor (19256). See also Darlington (1926) on Scillete, Langlet (1928)
on Berberidaceae, Kachidze (1929) on Dipsacaceae, Tschechow (1930) and Tschechow
and Kartaschowa (1932) on Leguminosie, and Saez (1928) on mammals.

130

INTRODUCTION TO CYTOLOGY

a large group is afforded by the Acrididse, a family of grasshoppers.^^
It is stated that the degree of relationship here is as clearly expressed
in the chromosomes as in the externally visible characters, and that the
evidence indicates a descent by variation from a common ancestral
series of chromosomes paralleled by corresponding variation in somatic
structures (Robertson).

Very often among plants and occasionally among animals the chromo-
some complements in a related group of individuals, races, or species
differ in the number of sets present, i.e., they form a "polyploid series."

wm\

I -M

H^ r EP <; p A

^ F E p <: p A

G H

A P Q p e: F

H

nfii r

Fig. 72. — Morphology of somatic chromosomes in several angiosperms. A, Gasteria
verrucosa. B, Crepis capillaris (virens). C, Cyrtanthus parviflorus: the six forms exhibited
by the eight pairs of chromosomes. D, Allium cepa: chromosomes in metaphase and
anaphase, showing two satellites in tandem ; seen in one plant. E, Haworthia cymbiformis.
F, Gasteria verrucosa. G, Aloe arborescens. Compare E, F, and G. (After W. R. Taylor,
1924, 1925a6.)

Sometimes the chromosome numbers do not form a series of multiples.
Consideration of the origin and consequences of these conditions must
be postponed to later chapters.

It is not to be doubted that such similarities and differences in
chromosome complements are of the greatest importance to students of
genetic relationships among organisms. At the same time caution is
necessary in the use of such evidence. It should not be assumed simply
because two chromosomes in different organisms look alike that they
correspond in function, nor that chromosomes with similar functions
should always show exact resemblance (see Fig. 71). Not only is it

2« McClung (1905 et seq., 1923, 1924), W. R. B. Robertson (1916), Saez (1930).

THE MORPHOLOGY OF THE CHROMOSOMES 131

known that the size and morphology of the chromosome may vary to
some extent with cultural methods and mode of fixation, but in many
cases it has been found that a chromosome may break into pieces, one
of the pieces often becoming attached to another chromosome and so
altering the idiogram (see Chapter XVIII). In this way the karyotypes
of sister individuals oi" closely allied groups may come to show marked
differences. Conversely, the same general karyotype may characterize
species which are morphologically very unlike. Evidently the differentia-
tion of genera, species, and varieties has involved genetic alterations not
directly observable in the nuclear substance, as well as changes which
modify the chromosome in a more obvious manner. The fact remains,
however, that when these considerations are borne in mind, chromosomal
characters as well as external features should be of great service in the
solution of many taxonomic and phylogenetic problems. No student of
such problems can afford any longer to ignore the data of cytology.

CHAPTER X
THE STRUCTURE OF THE CHROMOSOMES

In most fixed and stained preparations the chromosomes in the
metaphase and anaphase of mitosis appear as uniformly colored, more
or less homogeneous bodies. Attention must now be given to the
important question of the actual internal structure of such chromosomes
and the alterations undergone by this structure during the various phases
of the mitotic cycle. Students of this subject have investigated inten-
sively somatic chromosomes, particularly those of root tips, but sporo-
cytes and spermatocytes have come to be the favorite objects for such
studies because of the size of their nuclei and the ease with which they
may be examined without imbedding or sectioning.

In the development of our knowledge of chromosome structure three
principal interpretations have been prominent. These are (1) the
chromonema theory, according to which the fundamental structural
element of the chromosome is a slender filament, or chromonema, present
in some form throughout the mitotic cycle and associated with a second
substance, the matrix; this interpretation was used as a basis for our
preliminary description of mitosis in Chapter VIII; (2) the alveolation
theory, according to which the filament is a temporary form assumed by
the chromatic nuclear matter in the prophase as the result of an alveola-
tion of the more or less homogeneous chromosome in the preceding
telophase; (3) the chromomere theory, according to which small autono-
mous bodies, the chromomeres, are supported by relatively achromatic
threads and reproduce regularly by division in mitosis. It will be seen
in what follows that our present interpretation of chromosome structure
incorporates elements of the chromonema and chromomere theories;
that is, the typical chromosome in its condensed stages is now regarded
as a mass of matrix enclosing one or more chromonemata in which there
are small differentiations called "chromomeres."

The Chromonema Theory. — In 1880 Baranetzky examined fresh
Tradescantia sporocytes in spring water and saw what appeared to be
spiral filaments within the chromosomes. Janssens (1901) suggested
that such spirals in the telophase were the same as those observed by
himself and many others in the prophase. This conception was embodied
in the chromonema hypothesis, developed especially by Bonnevie
(1908, 1911) and Vejdovsky (1912). As a result of her studies on
Ascaris, Allium, and other forms, Bonnevie concluded that each chromo-

132

THE STRUCTURE OF THE CHROMOSOMES 133

some in the telophase develops an endogenous spiral thread which persists
through the interphase and emerges from the chromosome in the following
prophase. The achromatic material is not continuous from one nuclear
generation to the next but is differentiated anew in each telophase as
the spiral develops. According to Vejdovsky, who first applied the
term "chromonema" to the spiral filament, the latter arises much earlier
than stated by Bonnevie: it first develops in the prophase within the yet
unsplit antecedent chromonema, and, as the latter splits, the new
chromonema becomes broken up into irregular rings or strands which
in some undetermined manner form a continuous spiral again in the
telophase. The achromatic portion of the chromosome swells and
becomes the karyolymph, at the periphery of which the nuclear mem-
brane is formed. Such chromonemata have since been observed and
discussed by many writers, one of the principal questions at issue being
that of the permanence of such filaments through the nuclear cycle.

That the chromonema is a permanent constituent of the chromosome
and not a temporary formation has been rendered evident by recent
studies on both somatic cells and sporocytes. In root tips prepared by
methods rendering the matrix less stainable the chromatic chromonema
can be observed as a contorted or coiled filament lying mostly in the
peripheral region of the metaphase or anaphase chromosome. After
certain other methods the chromatic matter appears to be more uniformly
distributed in the peripheral region of the chromosome, which thus has a
tubular appearance.^ In the telophase the chromonema becomes a
portion of a new nuclear reticulum, which resolves into its constituent
chromonemata again in the next prophase. What is known about the
morphology of the individual chromosomes and the characteristic
structural patterns exhibited by certain chromonemata (see p. 141)
indicates that the prophasic chromonemata are actually the same as
those which formed the reticulum in the preceding telophase, although
they have undergone temporary alterations in the meantime.

In large chromosomes it appears that the chromonema in the telo-
phase, metabolic stage, and prophase is double as the result of splitting
one mitotic cycle in advance of the anaphase in which the halves so
formed are to separate. ^ Whether or not this is also true of small
chromosomes is unknown.

The Mitotic Cycle. — Large chromosomes like those just mentioned
appear to pass through somatic mitosis essentially as follows (Figs. 73, 74).

1 E.g., Bonnevie (1908), Zirkle (1928), and Blunt (1932).

2 K. Schneider (1910) on Salamandra; Dehorne (1911) on Salamandra and Allium;
Kaufmann (1925, 1926a6, 1931a) on Tradescantia, Podophyllum, Allium, and Iris;
Sharp (1929) on Trillium, Vicia, Podophyllum, Allium, and Tradescantia; Telezynski
(1930a6, 1931o6) on Tradescantia and Hcemanthus; Nebel (1932) on Tradescantia;
Hedayetullah (1931) on Narcissus; Perry (1932) on Galanthus; F. H. Smith (1932) on
Galtonia; Huskins and Huates (unpubl.) on Anthoxanthum.

134

INTRODUCTION TO CYTOLOGY

Fig. 73. — Stages in somatic mitosis as they appear in preparations of root tips of
Vicia, Trillium., Podophyllum, and Allium. 1, metabolic stage. 2-9, prophase. 10,
metaphase figure developing. 11, 12, metaphase. 13-16, anaphase. 17, 18, telophase!
19, 20, interphase. {After Sharp, 1929.)

THE STRUCTURE OF THE CHROMOSOMES

135

Beginning with the anaphase, it is observed that each chromosome
consists of matrix and chromonema. The latter is double, i.e., there are
in reality two chromonemata; these may lie very closely parallel to each
other and so appear as a single thread, or they may be rather widely
separated. The chromaticity of the matrix usually obscures this struc-
ture unless special methods are employed. At the end of the anaphase
the chromosomes tend to form a fairly compact group at each pole
(tassement polaire), a condition which may be accentuated by fixation.
The chromonemata become somewhat more contorted when the chro-
mosomes shorten.

As the telophase begins, the chromaticity of the matrix decreases
markedly, so that the chromonemata are more easily observed. As each
group of chromosomes enlarges and becomes a telophase nucleus, the

Fi

early
proph
and 8

G. 74. — The chromonemata in somatic mitosis in Harmanthus. 1, anaphase; 2,
telophase; S, interphase; 4< early prophase; 6, prophase; G, mid-prophase; 7, late
ase; 8, metaphase. The magnification in S, 5, 6, and 7 is greater than that in 1,2, 4,
{After Telezynski, 19316.)

chromonemata of the several chromosomes become joined together by
anastomoses to form the reticulum. The origin and the nature of these
connecting strands are uncertain. They have generally been regarded as
short lateral extensions of some component of the chromonema, but in
Zea microsporocytes they are clearly formed by the matrix (McClintock)
(Fig. 65a). As the telophasic changes continue, the chromonemata of
the various chromosomes become increasingly difficult to distinguish
as individuals. In rapidly multiplying nuclei where the interphase is
short, the next prophase may begin before they are lost to view; otherwise
the condition of the interphase passes into that characteristic of the
metabolic stage, when the reticulum is finer and relatively uniform in
texture. Such fineness of texture is probably due in some measure to a
tendency on the part of the two crooked chromonemata in each chro-
mosome to become more independent during this stage.

Little is known about the fate of the matrix in the telophase and the
origin of the achromatic constituents of the nucleus. Because of the
large volume of the karyolymph in which the reticulum is imbedded at
the end of the telophase, it is obvious that at least some of its material

136 INTRODUCTION TO CYTOLOGY

must have entered from outside during the telophasic enlargement of the
nucleus. It is held by a number of investigators^ that this material is
primarily the spindle substance which has functioned during the preceding
stages. Although some have inclined to the view that the matrix and
the entering fluid remain distinct, it has also been commonly thought that
in such nuclei the two become intermingled to form karyolymph, new
matrix differentiating about the chromonemata again in the ensuing
prophase, when matrix and karyolymph are easily distinguishable.'' By
some investigators^ this has been interpreted as an actual impregnation of
the matrix by the other fluid, the metabolic nucleus thus consisting of
chromosomes swollen and in contact or even fused so far as their matrix is
concerned. Accordingly, in the prophase the matrix and the other fluid
again separate, the former condensing about the chromonemata and

becoming chromatic as the latter accumulates between
the chromosomes in the form of future spindle sub-
stance. On this hypothesis, therefore, the karyolymph
of the metabolic nucleus is matrix plus spindle sub-
stance (" parachromosomic substance": Koerperich),
while in the advanced prophase it is the latter sub-
stance alone. On the other hand, the conditions
observed in Zea sporocytes (Fig. 65a) strongly suggest
Fig. 75.— Chro- the possibility that in nuclei generally the matrix may
Tmbr^J'^ofTtiS^Js'! maintain its identity from telophase to prophase in the
{After Richards, form of anastomoses, nucleolar matter, and possibly
^^ ■-' thin sheaths about the chromonemata.

Of considerable interest are those nuclei in which every chromosome
of the telophase group forms an individual vesicle, or karyomere.^ In
some cases the karyomeres may eventually fuse partially or completely,
but in others they remain separate although in contact, forming what is
virtually a group of small nuclei containing one chromosome each (Fig.
75). It is thus possible to think of chromosomes as bodies cooperating
with the cytoplasm somewhat after the manner of plastids,^ from which
they differ, however, in acting in highly organized groups of differentiated
individuals and undergoing a complicated series of changes during their
reproductive cycle.

The nuclear membrane has usually been regarded as one which
forms, perhaps in the manner of a precipitation membrane,^ where the
3 E.g., de Litardigre (19216), Martens (19296), and Koerperich (1930).
^ Kaufmann (1926a), Sharp (1929).
6 Martens (19296), Koerperich (1930).

6 ConkUn (1901a) on Crepidula, Wenrich (1916) on Phrynotettix, Renter (1909) on
Pediculopsis, Richards (1917) on Fimdulus, Pinney (1918) on fish hybrids, Eisentraut
(1926) on Acridid(p, Heberer (1927) on Cijclops, B. G. Smith (1929) on Cryptobranchus.
' Gregoire (1925, 1928).
8 Gates (1909a), Tischler (1921-1922).

THE STRUCTURE OF THE CHROMOSOMES 137

telophasic karyolymph comes in contact with the cytoplasm. According
to the interpretation of the metaboHc nucleus as a group of chromosomes
in contact, the membrane may be regarded as being made up of the
surfaces of the outermost members of the group. In the prophase it is
often observed that the formed chromosomes remain in contact with the
nuclear boundary over a portion of their surface, particularly at their
spindle-attachment regions. At this stage the membrane obviously must
extend from these areas of contact over the mass of prophasic karyo-
lymph, or separated spindle substance. This point requires further
study.

As the prophase begins, the individual chromonemata composing the
reticulum separate from one another through a disappearance of the
anastomoses. It seems probable that the substance of the latter becomes
a part of the matrix appearing about the chromonemata. At first the
chromonemata stand out as contorted double threads, but they soon
tend to straighten out. From this stage onward each chromosome,
composed of a matrix with the halves of the split chromonema along its
sides, undergoes a progressive thickening and often some shortening.
Meanwhile the matrix becomes more abundant and highly chromatic,
obscuring the contorted chromonemata within it. Toward the end of the
prophase the matrix undergoes division, so that the chromosome as a
whole, as well as its chromonema, is double.

The prophase now passes into the metaphase, each chromosome estab-
lishing connection with the spindle figure by its spindle-attachment
region. In the large chromosomes here being considered each longitu-
dinal half of the chromosome shows its chromonema to be double.^
Exactly when this subdivision of the chromonema takes place is not
known. Certain appearances suggest that it first becomes visible some
time during the prophase when the chromonemata are still more or less
extended, although the multiplication of elements within the thread may
well occur at some other stage of the mitotic cycle. The new chromo-
nemata so formed remain together through the ensuing anaphase and
separate in the anaphase of the next mitosis. In other words, the
chromonema divides one mitotic cycle in advance of the anaphase in
which the halves so formed are to separate.

Slender and Small Chromosomes. — To what extent the above
interpretation of chromosome structure and the nuclear cycle can be
applied to chromosomes of small dimensions is not known. It has been
suggested that, if the division of the nuclear elements is related in some
definite way to their growth and absolute mass, the stage at which the
chromonema becomes visibly double may not be the same for all nuclei.
On the other hand, small chromosomes may differ from larger ones only
in the size or the compactness in arrangement of their constituent ele-
9 Kaufmann (1926a), Sharp (1929), Nebel (1932), Hedayetullah (1931.)

138

INTRODUCTION TO CYTOLOGY

ments. In any event the arrangement of the chromatic matter in the
form of a long, slender, and relatively straight thread during the prophase
strongly suggests that it is at this time that it becomes morphologically
double, whatever the number of nuclear cycles in advance of the anaphasic
separation. Very little can be said at present concerning how or at what
stages any smaller elements within the chromonema undergo multiplica-
tion. Physiological considerations suggest that this occurs during the
interphase or metabolic stage, but adequate evidence is not yet available.

i»J<^i>«»#9l?H» %

vv(|^Vfc5

/>w

Fig. 76. — Somatic mitosis in plants with slender or small chromosomes, a, telophase
in Ceratopieris. b, interphase in Pteris. c, prophase in Polypodium. d-h, anaphase,
telophase, interphase, early prophase, and late prophase in Azolla. {After de Litardiere,
19216.)

As examples of the appearance of smaller chromosomes in some of the
stages of the mitotic cycle may be cited certain cases in ferns described
by de Litardiere (19216). In Pteris cretica and other forms with very
slender chromosomes, the latter undergo no conspicuous changes in
internal structure during the telophase but are drawn out into filaments
connected by anastomoses to form the interphasic reticulum. In the
prophase the anastomoses disappear and the chromatic substance is
concentrated directly into slender threads which soon appear double and
thicker (Fig. 76, a to c). In Azolla caroliniana the chromosomes are
very small, ovoid bodies. They undergo no obvious change other than
the development of anastomoses during the telophase and remain clearly
visible through the interphase. In the prophase the anastomoses dis-
appear, after which the chromosomes elongate somewhat, become double,

THE STRUCTURE OF THE CHROMOSOMES

139

and again shorten (Fig. 76, d to h). These nuclei are of interest in
connection with the problem of the origin of karyolymph, which is rela-
tively abundant here. In the opinion of de Litardiere it moves in between
the chromosomes during the telophase, but its exact relation to chromo-
somal constituents is undetermined.

Chromonemata in Sporocytes. — The microsporocytes of certain
plants are favorite objects for the demonstration of chromonemata
because of the large size of the chromosomes and the ease with which
they may be treated with various reagents or examined in the living
condition. 10 The chromonemata stand out clearly at late prophase,

2$a

Fill. 77. — Photographs of chromonemata. a, sporocyte of
treated with hot water. (After Sakamura, 1927a.) b, sporocyte
anaphase /. (After Nebel, 19325.) c, sporocyte of Trillium
Hjiskins and S. G. Smith, unpublished.) d, salivary gland
Kaufm,ann.)

Tradescantia virginica
of Tradescantia refiexa,
erectum. (From C. L.
of Drosophila. (From

metaphase, and anaphase in smear preparations fixed with chrom-osmic-
acetic mixtures and stained with hsematoxylin (Kaufmann, Taylor) or
fixed with chrom-aceto-formalin and stained with crystal violet (Sax)
or brazilin (Belling); also in preparations in acetocarmine (Shinke),
neutral violet (Kuwada), or ruthenium tetroxide (Nebel). They can be
seen in living cells mounted in Ringer's solution (Martens), sugar solution
or olive oil (Sakamura) (Fig. 77). The matrix of the chromosome can
be dissolved away with hot water, leaving the spiral chromonemata iso-
lated (Sakamura). Prefixation treatments may increase their visibility
(Kuwada, Nebel). For the successful observation of chromonemata in
fresh sporocytes special attention must be given to the pH of the

1" For accounts of chromonemata in sporocytes, see Kaufmann (1926o?)) on
Tradescantia and Podophyllmn; Kuwada and Sugimoto (1926), Kuwada (1927,
1932a6), Kuwada and Sakamura (1926), Sakamura (1927a6), Martens (1929o) and
Nebel (1932) on Tradescantia; Belling (19286) on Lilium; Maeda (1928, 1930a) on
Lathyrus; Inariyama (1928) on Hosta; Babcock and J. Clausen (1929) on Crepis;
Shinke (1930) on Tradescantia, Lilium, N^arcissus, and other genera; Sax (1930c) on
Secale and Lilium; Taylor (1931) and Tuan (1931) on Gasteria; F. H. Smith (1932) on
Galtonia. Binder (1927) describes them in the spermatocyte of the kangaroo. Lucas
and Stark (1931) photographed them with ultra-violet light in living grasshopper
spermatocytes.

140 INTRODUCTION TO CYTOLOGY

medium. ^1 Certain studies on the chemical composition of plant
chromosomes suggest that the chromonemata consist of nucleo-protein
and probably lipide, and the matrix of lipides free or combined with
protein (Shinke and Shigenaga, 1933).

In many plants used in such investigations the chromonema appears
in late prophase, metaphase, and anaphase as a rather smooth thread
coiled with striking regularity within the matrix. The clearest prepara-
tions show it to be double. In other plants the chromosomes in the
sporocytes do not show such regularly coiled and smooth chromonemata
as those described above. In Zea Mays, for example, the shortened
chromosome in these stages presents an appearance rather similar to
that observed in the earlier phases. The chromonemata, which show
their chromomeres clearly, seem to shorten with the chromosome as a
whole and preserve much of their early structure without being thrown
into very wide coils. This point will be considered further in a subse-
quent section. The behavior of the chromonemata through the mitoses
in the sporocyte will be discussed in Chapter XVI.

^

Fig. 78. — Chromosomes in metaphase of first meiotic mitosis, showing aspects observed
after different fixations. (After Kaufmann, 1926a.)

The Alveolation Theory. — According to this theory of chromosome
structure, which was founded chiefly on studies of somatic cells in plants, ^^
the more or less homogeneous chromosomes undergo a progressive
"alveolation" during the telophase. Lightly staining regions appear in
irregular positions in the chromosomes, whose chromatic matter assumes
a spongy structure and forms the reticulum of the interphase and meta-
bolic stage. In the ensuing prophase the reticulum again breaks up into
its constituent "elementary nets," each of which gradually transforms
into a slender filament. This filament splits, shortens, and thickens to
become the double chromosome whose halves pass to the poles in the
anaphase. The slender chromatic thread is accordingly looked upon as a
temporary formation of the prophase related to splitting rather than a
structure persisting throughout the nuclear cycle.

It is true that such figures as those published by the advocates of this

theory represent rather accurately the aspects often observed in the

telophase and early prophase; but it is now held by various workers,

including some who formerly supported the alveolation theory, that they

should be looked upon as inadequate images of the chromonemata and

matrix during these stages (Fig. 78). The "alveolation" is therefore

" Kuwada and Sakamura (1926), Sakamura (1927a).

12 Gr6goire and Wygaerts (1903), Gregoire (1906), Lundegardh (1910, 1912), Sharp
(1913, 1920a), de Litardiere (19216), J. B. Overton (1911, 1922), Koerperich (1930).

THE STRUCTURE OF THE CHROMOSOMES 141

interpreted as a series of aspects observable when the matrix swells and
loses its chromaticity in the telophase. Certain cases of "telophase
splitting by median alveolation" formerly reported are interpreted on
similar grounds. The chromatic structure first appearing in the telophase
chromosomes is not actually produced at that time by alveolation or any
other process but is simply rendered visible by an alteration in the
chromaticity of the matrix.

The Chromomere Theory. — Many years ago the theory was pro-
pounded that the small chromatic lumps often visible in the reticulum are
arranged in a linear series in a slender thread during the prophase and by
their division initiate its splitting. ^^ It was further supposed by some
workers that these small bodies, or chromomeres, are composed of still
smaller "chromioles," which are supported in the achromatic substance

■4---i 14 ^ 4 t ff\

h ^ d f h

/

*-^ X \

\^

/ T h i ^ "V-

Fig. 79. — Chromosome B (synapsed pair) from spermatocytes of 13 individuals of
Phrynotettix magnus, showing constancy in size and arrangement of principal chromomeres.
The same constancy is shown in different cells of a single individual. {After Wenrich,
1916.)

of the reticulum. The general opinion that such chromatic bodies are
more or less persistent nuclear units multiplying regularly in mitotic
division harmonized w^ell with the theory of heredity propounded by
Roux and Weismann, according to which the chromatic matter is quali-
tatively unlike in different regions of the nucleus, the arrangement of this
matter in the form of a long thread prior to its splitting being a means
whereby all the qualities, and hence hereditary potencies, are divided
and distributed to the daughter nuclei.

Since 1900, chromomeres have been studied chiefly in animal sperma-
tocytes and the microsporocytes of plants. In the spermatocytes of
insects, especially grasshoppers, the chromomeres appear with great
clearness.^* In some examples studied with particular care, it has been
found that in the early prophase the chromomeres not only differ in size,
as claimed long ago by van Beneden, but are arranged in a characteristic

" Balbiani (1876, 1881), Pfitzner (1881), van Beneden (1883).
1* McClung (1905 et seq.), Carothers (1917), Pinney (1908), Robertson (1915,
1916), Wenrich (1916), Janssens (1924).

142 INTRODUCTION TO CYTOLOGY

and constant pattern in a given chromosome of the complement (Fig. 79).
That such chromomeres are not primarily artifacts is indicated by their
appearance in the same configurations after a variety of fixing reagents,
as well as by the further fact that they may be seen in threads in unfixed
nuclei, especially when stretched out by the micromanipulator (Cham-
bers, 1924). Although their appearance may be modified in some meas-
ure by microtechnical treatment, they surely correspond to local differen-
tiations of some kind in certain regions of the threads (Agar, 1923).

Very definite chromomeres have been described in the prophase of the
first meiotic mitosis in many sporocytes, notably those of liliaceous
plants. 1^ The significance of these bodies has been a much debated
question among botanists, some maintaining that they are autonomous
units, while opponents of such a view, especially those working on somatic
tissues, have suggested other explanations for the appearances observed. ^^
It is true that their irregularity and indefiniteness of form in many
preparations suggest that they are fortuitously thickened regions of a
more or less homogeneous thread. On the other hand, their great
distinctness and regularity in other cases, notably in smear preparations
of Lilium and Zea, exclude so simple an interpretation. It now seems
evident, for reasons which will appear below, that chromomeres should be
regarded neither as elements wholly distinct from the rest of the thread
nor as mere chance accumulations of chromatic matter, but as definitely
localized differentiations of the chromonema, which in all probability
indicate the sites of certain special reactions.

Chromomeres in the Chromonema. — In 1912 Vejdovsky, working
on the spermatocytes of Decticus, suggested that the chromonema is
made up of chromomeres which have been brought into contact. This
interpretation applies well to the many cases, particularly sporocytes, in
which chromomeres in the early prophase are reported to give way to a
comparatively uniform chromonema in later stages. Kuwada (1926a)
likens the chromomeres to "balls embedded in a rubber thread," which,
as it shortens, brings the balls into contact and then becomes contorted
within the contracting matrix. Similarly, in the sporocytes of Crepis,
Babcock and J. Clausen (1929) figure chromomeres in the middle prophase,
but at the end of the prophase only a spiral chromonema whose coils
may appear superficially like large chromomeres. In Lilium sporocytes,
fixed in chrom-aceto- formalin and stained wdth iron-brazilin, Belling
(19286cg, 1931a) finds the chromomeres as bead-like bodies about 0.23/x
in diameter and separated in the thread by regions of about twice this

15 E.g., by Strasburger (1884, 1905 et seq.), C. E. Allen (1905), Mottier (1907),
Muller (1912), Belling (19286c^), and W. R. Taylor (1931).

i«Gregoire and Wygaerts (1903), Martins Mano (1904), Gr6goire (1906 1907),
Marcchal (1907), Bonnevie (1908), Stomps (1910), Lundeg&rdh (1912), Sharp (1913,
1920), Tischler (1908, 1921), de Litardifere (19216).

THE STRUCTURE OF THE CHROMOSOMES 143

length in the earher portion of the prophase. ^^ At this stage all the
threads taken together have a total length of about 1,500/i, and as the
prophase advances they become reduced to about one-tenth of this
length. This brings the ''ultimate chromomeres " into contact and causes
coiling of the chromatic thread so formed. Aggregates of these chromo-
meres, together with additional chromatic matter, constitute the con-
spicuous "compound," or " secondary, " chromomeres seen in the later
portion of the prophase.

Although the chromosomal threads have chromomeres and probably
always shorten in some measure during the prophase of mitosis in sporo-
cytes, the appearance of the chromosome at the end of the prophase
varies greatly in different plants. In Tradescantia and Secale rather
uniform chromonemata lie coiled within the matrix (Fig. 77), but in Zea
the large chromatic accumulations in the threads continue to be visible,
the chromosome showing many of the characteristic structures of the
early prophase in spite of its greatly reduced length (Figs. 66, 152).
Hence such chromosomes, like those of grasshoppers (Fig. 79), are
especially well suited to studies on the functions of their component
parts. Vegetative nuclei {e.g., in root tips) commonly show rather
smooth chromonemata from mid-prophase onward, though it is likely
that improved methods will reveal more concerning the architecture of
such threads, at least in their earlier stages.

A useful hypothesis covering the above observations is that the
chromatic substance appearing in small masses, or chromomeres, at
certain regions of the thread, together with any additional chromatic
matter, varies in amount at different stages of the nuclear cycle and at
a given stage in different organisms. When such chromatic substance
is scanty the chromomeres are distinct, but when it is abundant they are
more or less united and the thread appears more uniform. Hence the
chromomeres should be expected to appear most plainly in the early
prophase, when the masses of chromatic substance are small and well
separated from one another because of the extended and straightened
condition of the thread.

That the structural differentiation exhibited by the chromonemata
determines in large part the general form of the metaphase chromosome
seems evident. In Zea, for example, the general pattern formed by
the spindle-attachment region, the nucleolus-forming region, larger
chromomeres, and chromatic "knobs" in the early prophase is maintained
as the chromosome shortens, but the positions of the smaller elements
become difficult to make out (Fig. 66). It remains to be ascertained to

" Early pachynema stage. The threads are paired in synapsis, hence the chromo-
meres appear double. In the late pachynema stage each component thread shows
its split, the chromomeres then appearing as groups of four "chromioles" (see Chapter
XVI).

144 INTRODUCTION TO CYTOLOGY

what extent the matrix shares in determining the form of the chromosome
aside from giving it a smoother contour.

Chromosome Structure and the Gene Theory. — In later chapters it
will be shown why the chromosomes are thought to contain a series of
persistent units, or genes, which affect profoundly the course of develop-
ment in successive generations and thus represent causal agents in hered-
ity. At this point, those who are familiar with the gene theory may
consider certain points of a hypothesis which attempts to relate the
genes to the visible differentiations in the chromosome. ^^

As suggested by Alexander and Bridges, the fundamental constituent
of the chromosome is the "gene string," a linear aggregate of genes held
together primarily by their own attractive forces. The exact nature of
the genes is unknown, but they may be thought of provisionally as minute
bits of substances growing by autocatalysis and synthesizing a number of
materials including basichromatin, the most conspicuous of such mate-
rials. In the early prophase each gene is surrounded by its own small
mass of basichromatic matter; this is a chromomere. As the prophase
advances, some chromomeres increase in size more rapidly than others
because of a greater activity on the part of their genes, and they sooner
or later fuse to form the coarser and more uniformly chromatic chro-
monema. Hence larger lumps in this thread indicate groups of more
active genes. As the thread becomes thicker, the basichromatin just
beneath its limiting membrane is transformed into oxychromatin; this is
the chromosome matrix surrounding the still basichromatic chromonema
with its gene string. Because of its liquid nature the oxychromatic
matrix tends to round up and thus shorten the chromosome as a whole in
the later prophase, the relatively firm chromonema then being thrown
into coils. The matrix now becomes basichromatic again. In the
telophase the basichromatin decreases in amount and may largely or
completely disappear by the time the metabolic reticulum is fully devel-
oped; in the next prophase it is elaborated anew by the genes. This
discontinuity of the basichromatin is taken to mean that "chromatin"
is not the important "hereditary substance" but only a by-product of the
autocatalytic or reproductive activity of the persistent genes. Belling
calls the chromatic matter about each gene "gene chromatin" and the
abundant substance present later "extra chromatin." In certain cases
he observes at the center of each chromomere a minute dot which he
regards as "either a bare gene, or close to one" (1931a, p. 156).^^

18 Alexander and Bridges (1928). See also Belling (19286c, 1931a) and Reuter
(1930).

1^ Certain provisional calculations of the possible size of genes place them well
below the limit of visibility with the ordinary microscope and suggest that they are
of the same order of magnitude as certain large protein molecules (see Morgan, 1922,
and Gowen and Gay, 1933). Recent evidence on the spacing of genes in the chromo-
some (p. 323) offers a basis for new speculations on this subject.

THE STRUCTURE OF THE CHROMOSOMES 145

On the basis of this hypothesis — and it is at present no more than a
hypothesis — the chromomere is regarded not as a fundamental autono-
mous unit but rather as a product of such a unit, the gene. As already
suggested, a way may be found between the view that the chromomere is
a fundamental unit and the view that it is only a chance thickening of
the thread, if we construe it as a mass of material definitely associated
with some localized reaction and often becoming continuous with neigh-
boring masses. The hypothesis summarized above goes a step further and
attributes these localized reactions to genes. Similarly, the division of
the chromonema is thought to result from the division of the genes. At
present very little can be said concerning the time relation which may
exist between gene-division (or other mode of multiplication) and the
visible splitting of the chromonema. It is conceivable that a double
chromonema might be more highly compound as regards its gene strings.
Finally, it should be pointed out that although the chromosome may have
a characteristic lengthwise differentiation visibly manifested by its
chromomeres, as well as a functional differentiation manifested in the
results of genie activity, there is as yet insufficient evidence to war-
rant a confident statement regarding the spatial and functional relation-
ships of chromomeres and genes. Research in progress promises to
yield evidence on this important point (see, further, p. 318).

The Continuity of the Chromosome. — In each succeeding prophase in
the nuclei of a growing tissue there appears a group of chromosomes made
up of a certain number of characteristically different individuals. Are
these chromosomes in any real sense the same as those which developed
the nucleus in the preceding telophase? That they do preserve their
identity as individuals through the metabolic stage, arise only by division,
and therefore maintain a genetic continuity throughout the life cycle, was
held by many early observers. ^^ The question has been much debated,
and, although many statements of the conception of chromosomes as
persistent entities have been too crude, it remains true that the chromo-
somes "must at least be regarded as genetic homologues that are con-
nected by some definite bond of individual continuity from generation
to generation of cells" (Wilson, 1909c).

The evidences upon which this view is based are briefly as follows.
With rare exceptions, which have been found not to militate against any
proper conception of continuity, the chromosomes in successive mitoses
are the same in number and form. When the total number is altered in
any way, or when a number of the group is changed by loss, fragmenta-
tion, translocation, or the like, the altered group appears in the next
mitosis; the original complement is in no way restored during the inter-
vening metabolic stage. The limits of the several chromosomes remain
visible through this stage in certain nuclei ; in extreme cases the nucleus is

20 E.g., van Beneden (1883), Rabl (1885), and Boveri (1887, 18886, 1891).

146

INTRODUCTION TO CYTOLOGY

■■■LjXiy

virtually a group of separate elementary nuclei, or karyomeres (Fig. 75).
Each chromosome may even have its own elementary spindle at the time
of mitosis; this is known as merokinesis (Reuter, 1909). It has also been
observed that when the chromosomes lie in a certain relative position
when the telophasic reticulum is formed, they tend to appear in the same
position in the following prophase. ^^ It is therefore inferred that, even
when the whole reticulum appears like a single unit under the microscope,

the integrity of the constituent chromonemata is
nevertheless somehow -preserved. This idea is
supported by those cases in which certain por-
tions of certain chromosomes remain dense and
deeply chromatic ("heteropyknotic") and hence
distinguishable while the remaining portions
develop an otherwise uniform reticulum (Fig. 80).
Furthermore, when two species with chromosomes
of unlike size are crossed, the chromosomes of the
two parents can be distinguished in the dividing
nuclei of the hybrid (Fig. 206). Often the
parental groups do not intermingle but tend to
remain rafher distinct through several embryonal
cell generations-"^ (Fig. 143).

Many years ago Boveri was led by the results
of his brilliant researches on echinoderm eggs to
conclude that the number of chromosomes arising
from the reticulum in the prophase is directly and
exclusively dependent upon the number which
built it in the preceding telophase; this, he con-
tended, finds its most logical explanation in a
genetic chromosomal continuity. These conclu-
sions have been confirmed repeatedly by researches
phase. B, late telophase, on the chromosomes of hybrids, by observations

The heteropyknotic re- ,, i • , i , ,1 ■ n e

gions are numbered, ^u ceils Subjected to the mtiuencc 01 various
Compare Fig. 220. {After agcucies causing aberrant chromosome behavior,

and by critical analyses of the chromosome com-
plements in organisms showing unexpected departures from the normal
chromosome number and morphology.

The chromosome is not a body with unchanging form and composition.
In the course of the nuclear cycle it passes through a complicated series of
chemical and structural alterations, as does the organism itself during
its individual life cycle. At certain stages, notably the metabolic stage

21 E.g., in the segmenting egg of Ascaris, according to Boveri (1887a, 1891, 1909c)
and Herla (1893). See also p. 125.

" Haecker (1895c), Riickert (1895), Conklin (1897, 1901a), Moenkhaus (1904),
Tennent (1912), Morris (1914), Richards (1916), B. G. Smith (1919, 1929)

B

'■<-^

S

Fig. 80. — Heteropyk-
nosis in chromosomes of
Pellia epiphylla. A, pro-

ff

THE STRUCTURE OF THE CHROMOSOMES 147

and the growth period in animal oocytes, the basichromatic character of
the chromonema largely or completely disappears and the limits of the
individual matrix, whether this is temporarily swollen or removed,
become indistinguishable. Later on, a reverse series of changes takes
place and the chromosome is again evident as an individual. This is not
to be construed as an actual destruction and recreation of the chromosome
but rather as a cyclic change undergone by a definite group of materials
which must assume a structure suitable at one stage to the performance of
metabolic functions and at another stage to individual division and
distribution to daughter nuclei.

The above conclusion seems obvious enough when, as has been
frequently observed, a single chromosome separated from its neighbors
forms an individual metabolic nucleus and later passes through an
essentially normal series of division stages. The formation of a mitoti-
cally dividing nucleus by a single isolated chromosome, taken together
with what is known of karyomeres and merokinesis, serves to emphasize
the compound nature of the ordinary nucleus and leads to the view that
the usual mitotic figure is essentially a group of associated chromosomes
undergoing division and separation in unison. That the same inter-
pretation is to be placed upon the chromosome when it is a member of a
group, whether as a karyomere (Fig. 75) or an indistinguishable portion
of a metabolic nucleus, is now required by the evidence. That something
essential in the characteristic structural and functional organization of
each chromosome persists through the metabolic as well as other stages
of the cycle is practically proved in recent investigations on the effects of
X-ray treatments (Chapter XVIII). The results of treatments during
the metabolic stage indicate that even at this time the peculiar linear
organization of certain elements of the chromosome is normally main-
tained. In other words, the genes are somehow held to their character-
istic linear order at all times. No other plausible explanation of the
facts has been suggested. Only our limited vision prevents us from seeing
directly that a given chromosome has as characteristic an organization
in the metabolic stage as it has in other stages. This being the case,
less direct but none the less cogent evidence must be relied upon. What
persists as a chromosome through the nuclear cycle is evidently a group
of substances held together in a characteristic pattern (in a chromonema
or "chromonema axis") and accompanied at certain periods by additional
materials, the whole system undergoing a recurrent cycle of physico-
chemical transformations in successive nuclear generations. To what
extent the achromatic materials remain individualized is not known.

The chromosome, therefore, stands out as a persistent individual
reproducing by division. It does not follow, however, that this individ-
ual necessarily remains rigidly fixed and unaltered in character in succes-
sive generations. It will be shown in subsequent chapters that a portion

148 INTRODUCTION TO CYTOLOGY

of a chromosome is occasionally lost or transferred to another chromo-
some. Under the proper conditions such altered chromosomes continue
as individuals of new types. Since such alterations evidently have
occurred with some frequency in the past, a given chromosome should be
looked upon as a member of a long series of generations in which structural
and functional alterations occur from time to time: it is an assemblage
of elements which may remain relatively constant for a long period or
perhaps through only a limited number of generations. It may be likened
to a persisting society whose membership occasionally changes through
losses, additions, and the alteration of personal action. Its persistence
as an individual distinct from its neighbors in spite of all such alterations
is insured by the spindle-attachment region, a definite "organ" with
which the other chromosomal elements are associated. The precise
nature of the chromosomal substances which persist and of the chemical
transformations which they undergo remains for future investigators to
determine.

CHAPTER XI
THE ACHROMATIC FIGURE

The separation of the longitudinally divided chromosomes into two
daughter groups involves the action of the achromatic figure. In many
cells, notably those of vascular plants, this consists solely of the spindle,
a bipolar structure formed chiefly by achromatic constituents of the
nucleus. In other cases, including most animal cells and those of certain
lower plants, the figure has in addition at each pole a system of cytoplas-
mic radiations known as the aster, often with a centrosome at its focus.
Achromatic figures of the latter type are known as "amphiastral"
figures, while those without asters are called "anastral" figures.

Anastral Figures. — All vascular plant cells, with the exception
of certain spermatogenous cells of species with motile spermatozoids, have
anastral achromatic figures. A typical example is seen in the root-tip
cell, where the development occurs in the following manner.

According to an interpretation set forth in the preceding chapter,
the metabolic nucleus contains within its membrane three easily dis-
tinguishable components: a reticulum made up of anastomosed chromo-
nemata, a nucleolus (or nucleoli), and karyolymph. As the prophase of
mitosis advances, each chromonema becomes more or less free from its
neighbors and is seen to be surrounded by a distinct mass of matrix
substance. The karyolymph, in which the developing chromosomes lie,
is to form the spindle; hence it may be termed ''spindle substance."^
In the root-tip cell (Fig. 81) the nucleus commonly enlarges during the
prophase. Its membrane then gradually shrinks inward from the two
poles, leaving behind two "polar caps" of spindle substance, which seems
to have filtered through the membrane. As the membrane shrinks more
closely about the crowded chromosomes, the caps become larger and
gradually form a more definitely spindle-shaped figure. Eventually the
membrane disappears and the double chromosomes become arranged
with their spindle-attachment regions in the equator of the spindle.
Through all these changes the appearance of the cytoplasm remains
essentially unchanged (Robyns, 1924, 1929).

The spindle usually terminates in rather sharp points at its poles,
but cases are known in which the polar regions are nearly or quite as
wide as the equator. In the living condition the spindle is optically

' It is called "parachromosomic substance" by Koerperich (1930) and the "para-
genoplast" by Bleier (1930c).

149

150

INTRODUCTION TO CYTOLOGY

homogeneous, but for reasons which will be given later it is evident that
its substance has a definite longitudinal orientation of some kind. The
fine "fibrils" or ''lamellae" seen running from pole to pole in fixed
preparations are a visible modification of this oriented structure. In
addition to these fine fibrils, there are coarser ones which begin to develop
at the attachment regions of the chromosomes and extend poleward
along the spindle; these have often been called "tractile fibers."

In the anaphase the halves of each split chromosome begin to move
apart at the spindle-attachment region. The tractile fibers are very
prominent (in fixed preparations) at this time, but when the chromosomes
reach the poles they soon disappear. The spindle substance extending
between the two chromosome groups still shows its characteristic fine

.^•i7-

.->

;-;^^Q^;-

:• ••^*' )Vy

1 2 3 4

Fig. 81. — Development of achromatic figure in root tip of Hyacinthus orientalis.
1, nucleus after reaching its maximum size in prophase. 2, nuclear membrane shrunken,
leaving polar caps. S, membrane partly gone; caps about to become spindle cones. 4<
spindle established; metaphase. Note that chondriosomes do not invade the spindle.
(After Robyns, 1924.)

striations. As the two groups develop into telophase nuclei, this mass
of substance widens in the equatorial region to form a barrel-shaped
phragmoplast, which usually continues to extend laterally until it comes
in contact with the wall at one or more sides of the cell. It seems prob-
able that a portion of the spindle substance or some constituent of it
reenters the growing daughter nuclei while the remainder is functioning
as the phragmoplast.

While the above changes are taking place, the partition which is to
divide the original cell into two begins to develop. There is first formed
a delicate membrane known as the cell-plate through the equator of the
phragmoplast. The time at which it appears with reference to the
nuclear changes varies considerably in different cases. Commonly it
appears first in the middle region and extends laterally as the phragmo-
plast widens. The phragmoplast, or spindle substance, soon disappears

THE ACHROMATIC FIGURE 151

near the nuclei but continues to be evident for some time at the margin
of the growing cell-plate (Fig. 101). When a cell contains a large central
vacuole the parietal cytoplasm may form a broad strand through it, the
mitotic figure occupying this strand. In some cases the figure has been
reported to move across a broad cell as the cell-plate develops from one
side to the other. In all these examples, therefore, the achromatic figure
is not only concerned with nuclear division, but it is also involved in the
process of cytokinesis, which here follows very closely upon mitosis.
Cytokinesis and the development of the cell w^all about the cell-plate
will be described in the next chapter.

In microsporocytes, which at the time of their division are usually
suspended more or less free from one another in sporangial fluid, the
development of the achromatic figure is essentially like that described
above, but owing to the shape and polarity of such cells the figure ordi-
narily presents a somewhat different aspect in its earlier stages. In Larix,
for example (Fig. 82), the cytoplasm when adequately fixed appears rather
homogeneous and contains many rod-shaped chondriosomes. During
the late prophase the chondriosomes move endwise toward the nucleus
and lie parallel with its membrane, forming a dense "perinuclear chon-
driosomal mantle." Improper fixation here gives the "radial" and
"felted" aspects so often described. The chondriosomal mantle remains
intact throughout mitosis, its inner boundary marking the limit of the
nuclear region. As the nuclear membrane shrinks and disappears, the
chromosomes become grouped at the center of the nucleus, whose periph-
eral region is then occupied by the intranuclear spindle substance.
The cytoplasm contributes no formed element to the figure. The "trac-
tile fibers" appear first at the chromosomes and develop centrifugally
until the completed spindle extends across the nuclear region with its
poles at the chondriosomal mantle and the remaining intranuclear sub-
stance surrounding it on the sides. The figure is bipolar from the begin-
ning; multipolar appearances and extra fibers surrounding the spindle
proper are held to be due to inadequate fixation. In the telophase the
terminal portions of the spindle and much of the remaining intranuclear
substance become two masses of hyaline fluid in which the daughter
nuclei are reconstituted; hence the hyaline substance of these nuclei is
continuous with that of the original nucleus. The chondriosomes form
mantles about the two nuclei (Devise, 1914, 1922). In the peculiar four-
lobed sporocytes of certain liverworts the developing spindle passes
through a definitely quadripolar stage. ^

Many variations of the processes described above are known in
somatic cells and sporocytes. Among these the most instructive are
certain cases in which there is little or no shrinkage of the nuclear
membrane before the spindle differentiates. Frequently in sporocytes

2 Farmer (1894, 1895), B. M. Davis (1899, 1901), A. C. Moore (1903).

152

INTRODUCTION TO CYTOLOGY

and even in root cells occasionally (Fig. 73, 10) the late prophasic karyo-
lymph assumes the orientation characteristic of the spindle, and the
attachment regions of the chromosomes move to the equator as the
membrane disappears without shrinking inward. Cases are also known
in which the partially shrunken membrane disappears when in some inter-

wmm.

\' '" " • •■■■ ■

• m'.-' ' :^' /*,' I...

'7

>■

D

k1 w*#

-■, mji /v:>o'./- .\ (•■•' i/'-'ft^;^-?^'®-'^^. ■i^:.\ .(fe ::.--'■■■".-.-••. .-.1

■^

^

^■■^^ ■ ■

v-;':>

\/

Fig. 82. — Development of achromatic figure in microsporocyte of Larix europcea.
A-H, after fixation in Benda's fluid. I-L, after fixation in Flemming's fluid. L and H
show two successive stages in cytokinesis. {After Devise, 1922.)

mediate position. Hence it becomes easy to reconcile the many early
accounts in which the spindle was variously stated to arise from the cyto-
plasm, from the nucleus, or from both. What was being observed in all
these cases was a progressive transformation of the late prophasic karyo-
lymph, or nuclear "spindle substance," into a polarized spindle, with or
without a shrinkage of the nuclear membrane before its disappearance.
The reactions involved in this transformation are unknown, but it has

THE ACHROMATIC FIGURE 153

been thought probable that the karyolymph is allowed to react with some
cytoplasmic constituent at this time by the disappearance of the nuclear
membrane or by alterations in its permeability, the reaction occurring
inside or outside the membrane in different cases. ^

It seems proper, then, to regard the complete anastral mitotic figure
in the metaphase simply as the nucleus in a stage of division, its several
chromonemata being doubled and surrounded by condensed matrices
and its prophasic karyolymph being organized as the spindle. The
division is carried out in a cytoplasmic medium, but the structures con-
cerned are primarily those of the nucleus. That mitosis in an ordinary
nucleus is in a sense a cooperative undertaking on the part of its several
chromosomes is suggested by cases in which each chromosome of the
group begins by developing an individual spindle more or less independ-
ently of the others.

Amphiastral Figures. — Achromatic figures of the amphiastral type
are characterized by the presence of a system of radiations known as the
aster about each pole in the metaphase and a centrosome at the focus of
each aster. Such figures are the rule in animals; relatively few cells,
notably certain oocytes, are devoid of centrosomes and asters during
mitosis. They are also found in certain algae and fungi, as well as in
the spermatogenous cells of bryophytes and those vascular plants having
motile male gametes. Since the asters are cytoplasmic, the amphiastral
figure, unlike the anastral type, is not composed wholly of nuclear
materials.

The centrosome varies widely in structure in different tissues.'* What
may be called a "typical" centrosome lies in the cytoplasm (centrosomes
rarely occupy the nucleus) and consists of a deeply staining granule
known as the centriole together with a surrounding mass of substance
called the centrosphere. Either of these elements may be present alone.
The centriole may be single, but more commonly it is double as a result
of division during the later phases of the previous mitosis. Occasionally
there are several centrioles, constituting together a "microcentrum."
The centrosphere substance is often fairly abundant in resting cells
(Fig. 83).

In 1887 van Beneden and Boveri observed in Ascaris that the cen-
trosome, prior to cell-division, divides to form two daughter centrosomes,
which move apart to opposite sides of the cell and form the poles between
which the mitotic figure is established; and further, that after cell-
division is completed the centrosome included in each daughter cell does

3 Nothnagel (1916), Tischler (1921-1922).

* An exhaustive account of centrosomal differentiations is given by Heidenhain
(1907). The terminology of the subject has long been in a confused state (see Wilson,
1900, 1925). In the present account we have chosen more or less arbitrarily a termi-
nology which seems to have found favor with a number of writers.

154

INTRODUCTION TO CYTOLOGY

not disappear but remains visible in the cytoplasm through the ensuing
metabolic stage. They concluded that the centrosome, like the nucleus,
is a permanent organ maintaining its individuality throughout successive
cell generations. This conclusion is supported by the conditions observ-
able in many tissues, but it is evidently not valid for all. In certain
instances it disappears at the close of cell-division, a new one appearing
just before the next mitosis. Moreover, the formation of numerous
asters with centrosomes can be induced in the cytoplasm of certain
animal eggs, notably those of echinoderms, by treating them with solu-

W»

<??=

Fig. 83. — Centrosomes in epi-
thelium of cornea of monkey (A)
and of human gastric gland (B).
{After A. Zimmermann.)

Fia.

84. — Artificial cytasters in egg of Arhacia.
{After Morgan, 1899.)

tion of various chlorides^ (Fig. 84). Such "artificial cytasters" were
thought by some to be quite distinct from normal ones in lacking the
ability to function in mitosis, but it now seems clear that they do have
this ability, and hence that functional centrosomes can be differentiated
independently of preexisting ones.^ Tharaldsen finds that, although
they may arise anywhere in the cytoplasm in Asterias eggs, the region
near the nucleus is "most susceptible," and that cytasters arising here are
usually dominant in the mitotic activity which follows. This recalls
Yatsu's observation that in Cerebratulus the cytasters do not appear
unless the nuclear boundary has begun to break down in late prophase.

6 Mead (1898), Morgan (1896, 1899), Wilson (1901), Yatsu (1905), and later
workers. See Wilson (1925; p. 684).

« Tharaldsen (1926), Bataillon (1929), Fankhauser (1929).

THE ACHROMATIC FIGURE

155

Such facts, taken together with the frequent reports of the appearance
of a normal centrosome only after the aster has become partly developed,
suggest that the centrosome is a result of activity in this region rather
than its cause. Moreover, cases are on record in which bodies described
as centrosomes have turned out to be effects of microtechnical treatment.
Such an interpretation of the phenomena at mitotic centers in cleaving
animal eggs has recently been advanced by Fry (1928, 1929, 1932),

Fig. 85. — First meiotic mitosis in the spermatocyte of Salamandra. I, prophase:
centrioles in centrosphere substance, which is spread out on nucleus. II, prophase:
bivalent chromosomes formed; centrioles beginning to diverge; central spindle and asters
developed. Ill, late prophase: nuclear membrane gone; centrioles moving apart; "fibrils
attaching to chromosomes." IV, anaphase: connecting fibers prominent. V, telophase
cytokinesis by constriction nearly completed; mid-body forming at equator. (After
Meves, 1897.)

but its general validity is strongly opposed by other observers.^ Centro-
somes have been seen in living spermatocytes (Johnson, Pollister, Belaf).
In animal cells the amphiastral figure commonly develops essentially
as follows. The centriole, with or without centrosphere substance, is
usually double as the result of a division during the course of the preceding
mitosis. As mitosis begins, the daughter centrioles begin to move apart,
and as they do so they are seen to be connected by a small "central
spindle." About each of them an aster develops (Fig. 85). The result-

7 Wilson (19306), Pollister (1930, 1932), Belaf (1929c), Wilson and Huettner
(1931), H. H. Johnson (1931).

156

INTRODUCTION TO CYTOLOGY

ing achromatic figure is known at this stage and later as an amphiaster.
As the divergence of the centrioles continues, the asters and central

Fig. 86. — Achromatic figure with large asters in oocyte of Pisciola. {After M. Jorgensen

1913.)

r-

fj-f\,,

r---...^

p., -^ - ..i

l?^fH^vA-l*?J

t4*'

6

^1

"^ k

2

{U,

.■*■!

*%'

• »-

%L^^ -_.^^J

^>

1

^

8

9

•^

•

10

Fig. 87. — First meiotic mitosis in the ascus of Pustularia bolarioides. (After Bagchee,

1925.)

spindle increase in prominence. In some cases the nuclear membrane
disappears while the centrioles are still diverging, while in others it

THE ACHROMATIC FIGURE

157

persists until they have reached opposite sides of the cell. In either
event it may fade out in its original position or first shrink inward before
the enlarging asters. In the literature are many reports of "a growth
of the astral rays into the nucleus" and "a lateral movement of the
central spindle into the nucleus." To what extent this may involve
a progressive alteration of extruded karyolymph beginning in the region
near the amphiaster is not clear, but the spindle figure in such cases at
least appears to incorporate structures not originally nuclear.^

With regard to the asters, it was shown by Chambers (192 1&, 1924)
that in living echinoderm eggs they are regions which are somewhat more

•■C

-;<•:■'

'■J^:.

^fS

"f^:m

Fig. 88. — Development of spores after last mitosis in ascus of Pustularia bolarioides.

{After Bagchee, 1925.)

solid than the rest of the protoplasm, but that their rays, instead of
being firm fibers as some had thought, are actually streams of fluid
passing inward through the more gel-like granular cytoplasm. This con-
firmed a widespread view that the aster is primarily an expression of
streaming movements in the cytoplasm. The rays merge into a central
mass of hyaline fluid which may in some cases begin to accumulate before
the cytoplasm becomes sufficiently gelated to reveal the centripetal
channels. The aster may sometimes show rather well-marked concentric
zones (Fig. 86) as well as one or more concentric series of granules about
the centriole. It is questionable how far these are normal appearances,
for Chambers (19176) asserts that some of them may be produced by
subjecting eggs to abnormal environmental conditions.

During the anaphase the astral radiations remain conspicuous, but,
as the telophase progresses, they gradually fade from view, except in

* See the discussion of these cases by Bleier (1931a).

158 INTRODUCTION TO CYTOLOGY

those forms with more or less permanent asters. The centriole at each
pole divides, usually before the anaphase begins and often even earlier.
In case the aster about it does not disappear at the close of mitosis, a
new amphiaster may differentiate about the daughter centrioles in the
midst of the old aster. The latter rarely divides but usually degenerates
as the new amphiaster develops within it.^

A mass of spindle substance, sometimes surrounded by chondriosomes
in the cytoplasm, remains for some time between the chromosome groups
and the young nuclei w^hich they form. In animals this substance plays
no very conspicuous part in cytokinesis. Granules may be differentiated
at the equatorial region, forming the so-called "mid-body," but the
division of the cytoplasm is ordinarily brought about by the development
of a cleavage furrow, as will be described in the next chapter.

Very characteristic amphiastral figures are developed in the ascomy-
cetes^" (Figs. 87, 88). The centrosome, which in some ascomycetes is
discoid, lies against the nuclear membrane. As mitosis begins, an aster
usually develops in the cytoplasm about the centrosome, and the latter
divides to form two daughter centrosomes. The central spindle, if
formed at all, does not persist. From each of the daughter centrosomes,
which begin to move apart along the nuclear membrane, a group of
"fibers" extends into the nucleus. This appearance may be due to the
fact that the centrosomes here mark regions where there is an active
material interchange between nucleus and cytoplasm (Harper, 1919),
the result being the orientation of prophasic karyolymph to form the
spindle structure. The centrosomes finally reach opposite sides of the
nucleus, and the two groups of fibers become arranged in the form of a
spindle extending through the nucleus with the chromosomes at the
equator. The spindle may occupy nearly all of the nuclear volume or
only a small portion of it. The nuclear membrane commonly remains
intact until the chromosomes approach the poles at anaphase. It may
then disappear, allowing the nucleolus, which has remained visibly
unchanged, to escape into the cytoplasm. Between the two densely
packed daughter chromosome groups there extends a long strand of
spindle substance; this disappears as the daughter nuclei reorganize.

Cytokinesis in fungi is commonly brought about by a cleavage furrow
which is independent of the achromatic figure. After the final mitosis in
the ascus the astral rays curve around and in some way become involved
in the formation of the ascospore membrane. According to Harper, the

9 See Wilson (1925, p. 680).

'« Harper (1895, 1897, 1899, 1905), Faull (1905, 1912), Maire (1905a), Guillier-
mond (1904, 1905, 1911), Fraser (1908), Eraser and Brooks (1909), Fraser and Wels-
ford (1908), Claussen (1912), W. H. Brown (1909, 1910a, 19116), Bagchee (1925),
Carruthers (1911), Schultz (1927), Tandy (1927), Eftimiu (1927, 1929), Gwynne-
Vaughan and Williamson (1930, 1931, 1932).

THE ACHROMATIC FIGURE

159

rays actually fuse laterally to form the membrane, an interpretation
which has been disputed by Faull and others.

Very similar to the amphiastral figures just described are those in
certain algse (Fig. 89). In Dictyota, for example, a curved rod-shaped
centrosome lying against the nuclear membrane divides as mitosis begins.
The daughter centrosomes, each with an aster, separate and occupy the
poles of the intranuclear spindle. In Fucus the two centrosomes are
said to arise independently. In Polysiphonia the centriole-like bodies
seen in the prophase give way later to larger centrosphere-like masses.
In living cells of Sphacelaria, according to W. Zimmermann (1923), the
conspicuous rays about the centrioles before the metaphase are made up

Fig. 89. — Centrosomes in algse. A, B, Stypocaulon. (After W. T. Swingle, 1897,
and Escoyez, 1909.) C, centrosphere-like bodies in Polysiphonia. {After Yamanouchi,
1906.) D, E, Dictyota dichotoma. {After Mottier, 1900.)

of the oriented boundaries of large vacuoles, with fucosan globules and
chromatophores lying along them.

Amphiastral figures in the spermatogenous cells of bryophytes and
those vascular plants having motile male gametes are described in Chapter
XIV (Fig. 122).

The Mechanism of Mitosis. — It has always been tempting to specu-
late upon the mechanical factors involved in the remarkable process of
mitosis. Although the problem is still very far from solution, it is of
interest to consider briefly some of the suggestions which have been
made."

One of the simplest and most widely accepted theories was that of
fibrillar contractility proposed by Klein (1878) and van Beneden (1883,
1887), according to which the chromosomes were supposed to be dragged
apart by the contraction of two opposed groups of spindle fibers. Many
observations were cited in its favor, and elastic models were made to illus-

^1 See the reviews by Wilson (1900, 1925) and Tischler (1921-1922).

160 INTRODUCTION TO CYTOLOGY

trate the supposed contraction and its results (Heidenhain) ; but evidence
subsequently brought forward ^^ led to the general restriction of the role
of contractility, until it became apparent that this factor must be one of
minor importance.

The striking resemblance between the achromatic figure and the lines
of force in an electromagnetic field naturally led to attempts to account
for mitosis on the basis of electrical principles. Several investigators,
working with various chemical substances, succeeded in modeling fields of
force that illustrated graphically the changes supposed to take place in
mitosis. In later years the electromagnetic interpretation was again
brought into prominence by Gallardo, Hartog, and Prenant. At first
Gallardo (1896) believed the two spindle poles to be of unlike sign, but
later (1906), as the result of the researches of R. S. Lillie (1903) on the
behavior of nucleus and cytoplasm in the electromagnetic field, he con-
cluded that they are of like sign, the centrosomes moving apart because of
their similar charge. The movement of the chromosomes to the poles he
held to be due to the combined action to two forces: a mutual repulsion of
the similarly charged daughter chromosomes and an attraction between
the oppositely charged centrosome and chromosome. It has also been
thought that the chromosomes may assume their equatorial position
because they are repelled by both poles, and that a later weakening of
the repelling force relative to the mutual repulsion of the chromosome
halves allows the latter to move poleward.

The fact that the two centrosomes and hence the two spindle poles are
electrically homopolar (Lillie) at once made it apparent that the mitotic
figure does not represent an ordinary electromagnetic field, for in the
latter the poles are of unlike sign — the field is heteropolar. It was conse-
quently suggested by Prenant (1910) and Hartog (1905, 1914) that the
mitotic figure is the seat of a special force peculiar to living organisms.
This force they called "mitokinetism. " It can scarcely be doubted that
electrical forces are in some measure concerned in the mitotic changes, but
it is impossible at present to state how they act.^^ Any theory involving
such forces must be applicable not only to ordinary bipolar mitosis but
to occasional tripolar, quadripolar, and unipolar (p. 163) mitotic figures as
well.

Special significance has been attached to streaming by students of

mitosis ever since Biitschli, Fol, and others showed many years ago that

currents usually exist in the protoplast. That streams passing poleward

within the spindle play a role in chromosome movement was suggested by

many of the aspects observed, and the subsequent discovery that the

astral rays are such streams lent further plausibility to the view\ That

the "spindle fibers" are such streams was, however, not proved.

'2 Hermann (1891), Druner (1894, 1895), Calkins (1898), and others.
i^See WUson (1925, pp. 184-189).

THE ACHROMATIC FIGURE 161

All such hypotheses regarding the mechanism of mitosis must be recon-
sidered in the light of what has recently been learned about the achromatic
figure in living cells. As stated above, the aster has been found to be a
semisolid region of the cytoplasm with centripetal fluid paths, but, since
many achromatic figures have no asters, the causes of mitotic chromosome
movement obviously lie primarily in the spindle and the chromosomes.

It is a notable fact that in uninjured living cells the metaphase spindle
appears to be optically homogeneous, no "fibers" being visible. ^^ Its
density is such that it can be moved bodily through the cytoplasm with
the micromanipulator (Chambers) or the centrifuge, ^^ but the micro-
needles reveal no fibrous structure. In tissue cultures it is observed that
when the medium is made acid the fibers appear and the mitotic process
ceases; when it is made neutral again the fibers disappear and the process
is resumed (Lewis). The fibers can be made to appear by dehydration
and by various agents which bring about gelation or coagulation. Hence
the coarsely fibrous appearance of the spindle in many fixed preparations
is an unnatural one.

It is not to be concluded from these facts that the striations and trac-
tile fibers observed in such preparations have no structural basis what-
ever in the living cell. We are now forced to view the untreated spindle
as a body with a longitudinally oriented finer structure in spite of its
optical homogeneity.^^ In support of this view Belaf cites the following
facts: the distal portions of long chromosomes in the spindle tend to
become arranged parallel to its axis; the Brownian movement of occasional
included granules is greater in amplitude lengthwise of the spindle than in
other directions; mitochondria which sometimes enter an artificially
swollen spindle tend to be arranged longitudinally; the spindle has a
pronounced axial resistance to contraction; certain agencies cause the
spindle to split longitudinally (Fig. 90, c). Hence the spindle may be
likened to a crystal w^hich appears homogeneous to the eye but can be
shown to have an oriented structure by suitable treatment, or to a block
of wood whose splitting and differential swelling indicate the presence of
parallel elements.

The exact nature of the invisible local modifications which appear
upon fixation in definitely localized positions (notably near the spindle-
attachment regions of the chromosomes) is not yet known. The fixed
images often suggest that they are streams moving in harmony with the
cytoplasmic streaming frequently observed during these stages (Fig. 97) ;
but Belaf has shown that the movement of the chromosomes may con-

1* Chambers (1914, 1915, 1917, 1924), Chambers and Sands (1923), Sands (1923),
M. R. Lewis (1923), Lewis and Lewis (1924), Martens (1927c, 1929), Robyns (1929),
Belaf (1927, 1929a6).

i*F. M. Andrews (1915), Nemec (1927).

1" Robyns (1926, 1929), Belaf (1927, 1929afc), Martens (1929), Nemec (1927,
1929e), Bleier (19306), Jungers (1931).

162

INTRODUCTION TO CYTOLOGY

tinue after cytoplasmic streaming has been stopped, and also that the
streaming may continue when mitosis is arrested. The appearances in
living and fixed cells also suggest a longitudinal tension of some kind in the
figure, or even a bundle of tubes through which the chromosomes move
(Reuter, Schrader).

As a result of his investigations on the living spermatocytes of Chort-
hippus (Stenobothrus) and stamen hairs and leaf-cells of Tradescantia,
Belaf advanced the following hypothesis, which is a modification of an
earlier one advocated by Drliner (1895) and others, to account for chromo-
some movement (Fig. 91). The spindle,
which develops progressively from the two
poles to the equator, is composed of relatively
firm fibers (which are aggregates of micellae)
and a less viscous substance between them.

Fig. 90. Fig. 91.

Fig. 90. — Modifications of living anaphase spindles in Chorthippus induced by immers-
ing the spermatocytes in hypertonic Ringer's solution, a, b, elongation and contortion,
c, splitting. The white areas represent the chromosomes. (After Belaf, 1929a.)

Fig. 91. — Diagram illustrating Belaf's hypothesis of interaction of chromosomes and
spindle. See text for explanation. {After Belaf, 1929a.)

The double chromosomes become fixed in or on the spindle at its
equator by their attachment regions. From this region in each half-
chromosome there is exuded a fluid droplet which spreads poleward along
the spindle; this is the "tractile fiber" of other authors and it does not
grow toward the chromosome from outside the nucleus as often supposed.
The separation of the daughter chromosomes (or of synaptic mates) is
initiated by the chromosomes themselves, the tractile fiber mechanism
assisting in some unknown manner, perhaps through forces of adhesion
acting between fiber and spindle; but after this the continued separation
is due mainly to the elongation of the mass of spindle substance ("Stemm-
korper") lying between the diverging groups of chromosomes. In
spermatocytes immersed in hypertonic media this elongation may be
caused to continue until the mitotic figure is far beyond its natural length
and lies folded together within the confining cytoplasm (Fig. 90, a, b).

THE ACHROMATIC FIGURE 163

Meanwhile the polar regions of the spindle undergo little change. Long
chromosomes like those in Tradescantia undergo a marked shortening
during late anaphase.

Although the normal spindle is frequently longer at the end of the
anaphase than in the metaphase, a number of workers ^^ object to the
emphasis on elongation as a major factor in mitosis. As urged by Bleier,
such an interpretation does not apply well to the mitotic phenomena in
many hybrids, where double chromosomes of different origin and con-
stitution (bivalents formed by synapsis and univalents which have split)
pass poleward at different times in the same spindle (Figs. 207, 208).
In Bleier's opinion, all hypotheses postulating only a passive movement
of the chromosomes, whether caused by streaming, a contraction of
fibers, or a "Stemmkorper," fail in such cases. It is rather to some force
resident in the chromosomes themselves that the movement is due
primarily; it is provisionally assumed that this is a repulsion force of
some kind. It is a suggestive fact that the chromosomes exhibit fully
their characteristic reactions in the spindle (attachment at its equator
and subsequent separation) only after they have reached a certain stage
in the development of their doubleness. The delayed attachment of the
univalents may be related to their late splitting, especially at their
attachment regions. The repelling force thus comes into play only when
the chromosome is properly constituted, and it is accordingly possible
to look upon the spindle as a structure which guides the chromosomes
instead of actively moving them. The existence of some such force is
further rendered plausible by certain other phenomena of synapsis and
disjunction to be considered in later chapters, as well as by the successful
distribution of daughter chromosomes in narrow root cells and pollen
tubes, where limitations of space often prevent the arrangement of the
chromosomes in a regular equatorial plane.

Further evidence that the movement of the chromosome is not a
passive one is afforded by the remarkable monocentric mitosis discovered
in spermatocytes of flies of the genus Sciara by Metz.^* In the first
meiotic division, although all of the chromosomes show fibers extending
from their spindle-attachment regions toward the single pole, four of them
move backward away from the pole until they reach the cell boundary,
where they move into a compact group and are extruded in a bud from
the cell. The behavior of these chromosomes when their extrusion is
inhibited shows that they are not merely degenerated material of which
the cell is ridding itself. During their backward movement their shapes
suggest that a poleward force acting at the spindle-attachment region
is overcome by another force acting in the opposite direction. The

1^ Martens (1929), Schaede (1929), Bleier (19306c). See also Schrader (1932).
18 See Metz (1925, 1926c, 1933) and Metz, Moses, and Hoppe (1926). See also
Huth's (1933) account of Belaf's work on monasters in Urechis eggs.

164 INTRODUCTION TO CYTOLOGY

arrangement of materials about the chromosome suggests further that
the latter force is not resident in them but in the chromosome itself.
A hypothesis involving a progressive alteration at one or both ends of the
chromosome is advanced.

Evidence for an active participation by the spindle is afforded by the
occasional division of nucleoli in normal bipolar mitosis. ^^ Ordinarily
the nucleolus has disappeared by the time the metaphase figure is estab-
lished in root cells, but frequently a portion of it may remain. In such
cases it tends to occupy the equator of the figure with the chromosomes.
It may then elongate and divide by constriction, the halves passing
toward the spindle poles, sometimes in advance of the chromosomes. A
similar behavior is manifested regularly by the ''karyosome" in the
nuclei of certain lower plants and animals (see Chapter XIII). In the
ascus of Pustularia the nucleolus is usually left outside the spindle, but
when it lies in the equator it divides. In sea-urchin eggs in hypertonic
media Konopacki (1911) observed that a whole nucleus might be sepa-
rated into two portions if caught between two cytasters.

The foregoing facts seem to show that anaphasic chromosome migra-
tion is a process in which more than one of the nuclear constituents play
active roles. As the metaphase approaches, the prophasic karyolymph-''
becomes organized as a spindle which is the visible expression of a field
of forces tending to divide and carry poleward any sufficiently fluid body
lying in the equator. The chromosomes, which are less fluid at this
stage, are specially adapted to reaction with these forces in being already
doubled when they enter the equator and in having specialized attach-
ment regions. Moreover, evidence cited above suggests an active force
resident in the chromosomes themselves. To the extent that the spindle
substance is actually a constituent of the chromosome {i.e., combined
with its matrix) during the metabolic stage, the mitotic division of the
nucleus may be regarded as a simultaneous and cooperative division of
its several individual chromosomes. In amphiastral figures the process
is closely correlated with the multiplication of centrioles and a series
of structural alterations in the surrounding cytoplasm, such figures
comprising both nuclear and cytoplasmic elements. ^^ The nature and
relative importance of the forces involved are still obscure. It seems prob-
able that mitosis involves the action of many factors, including alterations
in viscosity, 22 surface tension, and permeability, as well as streaming,
tension, and electrical attractions and repulsions. In no one of these
factors alone will the entire solution of the problem of mitosis be found.

" Nemec (1901) on Alnus, Yamaha and Sinoto (1925) on Glycine and other genera,
Zirkle (19286) on Zea, Frew and Bowen (1929) on Cucurbita and Pustularia, Ghimpu
(1930) on Acacia.

2" The "parachromosomic substance" of Koerperich (1930); the "paragenoplast"
of Bleier (1930c). See discussion by Wilson (1932).

21 See Wilson (1925, pp. 174-178).

22 Chambers (1917), Heilbrunn (1920a, 1921).

CHAPTER XII
CYTOKINESIS AND THE CELL WALL

The division of the cytosome, or extra-nuclear portion of the proto-
plast, is known as cytokinesis. It may occur more or less independently
of karyokinesis (mitotic nuclear division), or the two processes may be
very intimately associated. Cytokinesis is accomplished in a variety of
ways in growing and differentiating masses of protoplasm. The prin-
cipal types are included in the following description.'^

Furrowing in Plants. — The cleavage of plasmodial masses is most
commonly brought about by the formation of furrows, with or without
the cooperation of vacuoles. It is well illustrated in the sporangia of
myxomycetes and certain fungi. ^ In Fuligo, cleavage furrows begin to
develop at the peripheral membrane of the young sporangium and
gradually extend inward, cutting out multinucleate blocks which are
subdivided by further furrowing into uninucleate spores. In Didymium
the spores are delimited in a similar way by furrows which begin to
develop both at the periphery and along the young capillitium filaments
in the midst of the protoplasm. In Rhizopus the furrows develop from
the peripheral membrane (Fig. 92, A) and from the columella. In the
sporangia of Achlya, Saprolegnia, and Olpidiopsis the furrows start from
a large central vacuole. In Phycomyces, vacuoles appear in the proto-
plasm, become stellate in form, and cut out spore masses with from one
to about twelve nuclei each (Fig. 92, B). Such vacuoles function together
with peripheral furrows in Piloholus and Circinella. In the sporangia of
the phycomycetes the columella is separated from the rest of the sporan-
gium by a dome-shaped layer of vacuoles which coalesce and form a
continuous partition between the two regions. Such cleavage is inter-
preted by Scarth (1927) as an extension and swelling of kinoplasm present
at the protoplasmic surfaces.

Similar forms of cytokinesis are found in certain algae. ^ In Hydro-
dictyon, for example, the multinucleate protoplasm, lining the wall of the

1 A classification of types of cytokinesis, with examples, is given by Yamaha
(1926a).

2 Harper (1899, 1900a, 1914) on Synchytrium, Piloholus, Sporodinia, Fuligo, and
Didymium; D. B. Swingle (1903) and Moreau (1913) on Rhizopus and Phycomyces;
Rothert (1892) and Schwarze (1922) on Saprolegnia, Circinella, and Achlya; B. M.
Davis (1903) on Saprolegnia; Rytz (1907) on Synchytrium.

3 Klebs (1891) and Timberlake (1902) on Hrjdrodictyon, Yamanouchi (1906) on
Polysiphonia, Brand (1908) on Cladophora. For an extensive account of the algae, see
Oltmanns (1922-1923).

165

166

INTRODUCTION TO CYTOLOGY

large cell, is divided into uninucleate swarmers by cleavage furrows.
These appear to begin their development from the cell and vacuole
membranes and from cleft-like vacuoles. Often the furrows thus
developing inward from the cell membrane are very narrow. In some

,:^^^H:^M

Fig. 92. Fig. 93.

Fig. 92. — Cytokinesis by furrowing in sporangia of fungi. A, Rhizopus nigricans. B,
Phycomyces nitens. {After D. B. Swingle, 1903.)

Fig. 93. — Cytokinesis by furrowing in Closterium. {After Lutman, 1911.)

instances, the wall substance seems to be active in developing the furrow ;
in such cases a "girdle wall" develops centripetally as a ring-like ingrowth
from the sides of the cell (Fig. 94). In Cladophora an accumulation
of slimy material, seen against the lateral wall as the process begins,
appears to be swollen wall substance. The formation of the girdle wall

Fig. 94. — A, girdle wall developing in Spirogyra. {After Nathansohn, 1900a.) B-F, five
stages in the development of the girdle wall in Cladophora. {After Brand, 1908.)

is probably independent of the division of the several nuclei, but in
Spirogyra such a wall develops immediately after the single nucleus
divides and involves the activity of the achromatic figure (McAllister,
1931). The "division by constriction" seen in unicellular alga?, the

CYTOKINESIS AND THE CELL WALL

167

"budding" of yeast cells, and the abstriction of eonidia and basidiospores
may be regarded as special cases of cytokinesis by furrowing.

The microspore quartets of most vascular plants fall into two classes
as regards the shape and arrangement of the spores. If no permanent
partition is formed after the first meiotic mitosis, the four spores are
delimited by partitions appearing simultaneously after the second mitosis.
Such spores, when first formed, commonly,
though not always, have the tetrahedral form.
If the first mitosis is followed immediately by
the formation of a permanent partition through
the equator of the sporocyte, each hemisphere
being divided by another partition after the
second mitosis, the quartet is said to be of the
"bilateral" type.'*

Although the partitions delimiting the four
microspores in angiosperms are sometimes formed
by the cell-plate method, it has been shown^ that
furrows developing inward from the periphery
are chiefly responsible for cytokinesis here, at
least in cases of simultaneous division (quadripar-
tition) to form tetrahedral spores. In Nicotiana,
for example, the four microspore nuclei present
after the second mitosis all become connected by
achromatic "fibers" (Fig. 95). The two sets of
connecting fibers of the second mitosis may
persist, four new sets being added, or the two
may disappear, six sets being developed anew.
These fibers have nothing to do with the forma-
tion of the partitions; no cell-plates are devel-
oped. Furrows appear at the periphery and grow inward until they
meet at the center, dividing the protoplast simultaneously into four
spores. In Nelumbo the furrows are exceedingly narrow, appearing
much like cell-plates. As they grow inward they seem simply to cut
through any fibers which they may encounter (Farr).

Meanwhile there develops within the original sporocyte wall a mass of
callose known as the "special wall." This increases in thickness and
follows the furrows inward, forming a sort of matrix in which the young
spores lie while their elaborate coats are being differentiated (p. 180).

■* Although either the "simultaneous" or the "successive" mode of division may
tend strongly to predominate in certain groups of plants, there are so many exceptions
to rules and so much variation that the character is of very restricted taxonomic
value. See Tackholm and Soderberg (1917, 1918), Soderberg (1919), Palm (1920),
Suessenguth (1921), Stenar (1925), and Coulter and Chamberlain (1903).

^C. H. Farr (1916, 1918, 1922a6), W. K. Farr (1920), Castetter (1925), Gates
(1925), W6ycicki (1932).

Fig. 95. — Cytokinesis by
furrowing in the microsporo-
cyte of Nicotiana. {After
Farr, 1916.)

168

INTRODUCTION TO CYTOLOGY

By some observers the special wall has been thought to arise through a
swelling of the secondary layers of the sporocyte wall, but it now seems
evident that it is secreted directly by the protoplast (Gates, Castetter,
Woycicki), which may undergo a distinct contraction at this time.
Eventually the sporocyte wall and the material separating the four
microspores disappear, leaving the spores free from one another.

Cytokinesis in the microsporocyte of Melilotus alba is of interest in
that vacuoles appear to play a conspicuous part in the process (Fig. 96).
After the second mitosis small vacuoles develop in the regions between
the four nuclei and fuse to form larger ones which nearly separate the
protoplasm into four masses. Furrows originating at the surface then

Fig. 96. — Cytokinesis in the microsporocyte of Melilotus. 1, prophase of first meiotic
mitosis; callose (uniformly stippled) being secreted by the protoplast. 2, telophase of
second mitosis. 3, special wall (black) and furrows appearing. 4, 5, vacuoles forming
between nuclei. 6, special wall extending inward. 7, special wall extensions have met at
center. 8, thickened special wall complete. {After Castetter, 1925.)

grow inward, meet the vacuoles, and complete the cleavage of the proto-
plast (Castetter). A similar process occurs in Gentiana (Woycicki).

In Magnolia, Farr finds a case in which bilateral quartets are formed
by furrowing, rather than by cell-plates as might be expected. Although
a transitory cell-plate may be differentiated, it plays no part in cyto-
kinesis. After the first mitosis a cleavage furrow starts to form, but its
development is arrested until after the second mitosis, when it resumes
its growth and forms a partition through the equator of the sporocyte.
At the same time additional furrows subdivide the two hemispheres, thus
delimiting the four microspores.

Furrowing in Animals. — Cytokinesis, which in animals is most
commonly accomplished by furrowing, has been studied with special
care in segmenting eggs. In the case of small eggs, such as those of

CYTOKINESIS AND THE CELL WALL

169

worms, the daughter cells (blastomeres) round up and become more or
less spherical, whereas in larger eggs, such as those of frogs, a narrow
cleavage furrow appears at one pole and develops through the egg without
altering greatly the shape of the latter, so that the first two blastomeres
have the form of hemispheres. In many animals, notably birds, the
cleavage is superficial, not extending entirely through the yolk-laden egg.

So far as known, no animal cells are divided by cell-plates of the type
found so commonly in plants. As noted previously, there is often a
slight differentiation (the "mid-body") at the equator of the achromatic
figure in the telophase, but it plays no part in cytokinesis. In the
spermatogonia of certain insects Janssens (1924) finds a cell-plate-like
differentiation which appears to represent a region of protoplasmic
continuity rather than a structure concerned in cytokinesis.

Experiments with dividing eggs have led to the identification of some
of the factors involved in the development of cleavage furrows. Many

Fig. 97. — Diagram of streaming and furrowing in the egg of Rhabditis pellio (A) and an oil

droplet (S). {After Spek, 1918a.)

years ago Biitschli (1876) advanced the view that cytoplasmic currents
flowing toward the centrosomes lead to the production of a relatively
high surface tension at the equator of the cell, this in turn bringing about
furrowing through this region. Evidence favoring this interpretation
has been contributed by several later investigators.^ Spek imitated
furrowing and division with oil and mercury droplets in water and showed
that by lowering the surface tension at two poles of the droplet the rela-
tively high surface tension at the equatorial region could be made to
bring about the constriction and fission of the droplet. In both droplet
and dividing nematode egg he found streamings such as Erlanger (1897)
had described in the egg: an inner movement poleward to the region of
low surface tension and a superficial streaming toward the equatorial
region of higher surface tension, the streams turning inward at the furrow
(Fig. 97). Belaf (1927) has observed such cytoplasmic streams in the
furrowing spermatocyte of Chorthippus (Fig. 59).

Closely associated with such streaming and surface-tension phe-
nomena are certain periodic alterations in the viscosity of the egg sub-

sMcClendon (1910, 1913), Spek (1918a, 19206), Just (1922), Cannon (1923),
Bancroft and Gurchot (1927).

170

INTRODUCTION TO CYTOLOGY

stance.^ In the living echinoderm egg it is found that the two asters
developed at the first cleavage division are regions in which the proto-
plasm has become decidedly more viscous, the peripheral and equatorial
regions at the same time showing a high degree of fluidity and active
streaming like that mentioned above. The growth of the two semisolid
masses results in a slight elongation of the egg and a cleavage furrow
develops in the more fluid region separating them, after which the asters
revert to a less viscous state. In a number of interesting experiments
Chambers has shown the dependence of the location of furrows on these
local differences in viscosity. When a dividing egg is cut in two obliquely
through the two asters, the pieces will continue to cleave along the

Fig. 98. — Diagrams showing effect of bisecting cleaving echinoderm eggs. First row:
without disappearance of asters. Second row: with disappearance of asters. {After
Chambers, 1919.)

fluid equatorial plane if the asters persist in the semisolid state; but if the
asters revert to the fluid condition, as often happens as the result of
rough handling, the cleavage furrow is obliterated, and the pieces pro-
duced by the cut divide symmetrically at the next cleavage (Fig. 98).
When the formation of a furrow at the first mitosis is prevented by
mechanical means, furrows develop between all four asters in the second
mitosis, cleaving the egg simultaneously into four blastomeres. Accord-
ing to Heilbrunn, "all agents which stimulate egg cells to segment cause a
gelatin or coagulation and ... all agents which prevent such gelation
prevent the division of the egg." In the plant cells mentioned in the
preceding section, it is probable that the furrows separate regions of
relatively high viscosity even though no asters in the ordinary sense are
present.

7 Heilbrunn (1915, 1920a, 1921, 1925c), Chambers (1917, 1919). See Gray (1931).

CYTOKINESIS AND THE CELL WALL 171

Alterations in surface tension and viscosity, together with proto-
plasmic streaming, are obviously important factors in cytokinesis of
certain types, but comparatively little is known about the initial causes
of these phenomena. That they are in some way associated with changes
in the permeability of protoplasmic membranes seems clear from the
work of Spek and others on animal eggs and of Stalfelt (1921) on plant
cells. Little more than a promising beginning has been made on the
problem of the mechanism of cytokinesis.

Closely allied to the process of furrowing is the type of cytokinesis
seen in certain tissues which are more or less plasmodial in their early
stages of development. In some forms of cartilage and epithelium, for
example, vacuole-like masses of material appear in the cytoplasm and
gradually subdivide the Plasmodium into cells which, however, remain
connected as a syncytium (Fig. 10). In certain cases such masses are
metaplasmic in nature (Rohde, see p. 45).

Cjrtokinesis by Cell-plates. — In the bryophytes and vascular plants
cytokinesis in somatic cells commonly begins with the formation of a
cell-plate through the equatorial plane of the spindle substance lying
between the young sister nuclei. The same process occurs in some sporo-
cytes also. The precise manner in which the cell-plate is formed and
becomes involved in the developing cell wall has long been a subject of
dispute. According to many of the earlier accounts,* the cell-plate is
formed by the fusion of swellings on the middle portions of persisting
spindle fibers, the plate then splitting to form the plasma membranes of
the two daughter protoplasts, the primary wall layer, or "middle lamella,"
then being secreted between them.

In a series of more recent papers^ it is emphasized that after adequate
fixation (Bouin, Benda) the cell-plate first appears as a continuous film
in the midst of the oriented "spindle of cytokinesis" and not as a series
of swellings or granules. This film proceeds to thicken, often unevenly
at first. The "splitting of the plate" so often observed is held to be due
to improper fixation, for it is said to appear only after the use of certain
fluids and not in unfixed cells (Robyns, 1929). Belaf (19296), in his
ingenious experimental studies on living cells of young Tradescantia
leaves, finds that the young cell-plate is a fluid layer offering less resistance
to shrinking agents than the spindle, so that the halves of the cell can
be made to round up and separate along this plane before a primary cell
membrane is present. Hence he concludes that the cell-plate is really a
transverse cleft in the spindle, the membrane substance being deposited

^ E.g., Strasburger (1898), Timberlake (1900), and C. E. Allen (1901).

9 Devise (1922) on the sporocytes of Larix; Robyns (1924, 1926, 1929) on the root
cells of Hyacinthus, Viola, and other plants; Martens (1927c, 19296) on stigma cells
of Arrhenatherum and stamen hairs of Tradescantia; Jungers (1931) on the endosperm
of Iris.

172

INTRODUCTION TO CYTOLOGY

later in this cleft. In living stamen hairs of Tradescantia, W. Becker
(1932) observes that the cell-plate material appears first in the form
of minute droplets which then unite to form a continuous plate (Fig. 99).
This may be a more adequate description of what was formerly inter-
preted as "swellings of the spindle fibers." On the basis of such observa-
tions the supposed "splitting of the cell-plate to form the plasma
membranes" of the two protoplasts could be regarded as merely the
widening of the fluid layer as its substance increases in amount and receives
deposits of the primary wall materials. The plasma membranes would
be the protoplasmic surfaces lying against the fluid layer. The origin of
the fluid which collects thus at the equator to form the cell-plate is
unknown, but it has been claimed that a stainable substance migrates to

Fig. 99. — Formation of cell-plate by coalescence of droplets in stamen hair of Trade-
scantia. The changes shown occupied 27 minutes. {After W. A. Becker, 1932c.)

this region from the two young nuclei. ^° The observations of Becker
point rather to the conclusion that there is a local dissociation of two
protoplasmic phases, one of these forming the cell-plate while the other
remains as the plasma membranes. Such a dissociation ("Entmis-
chung"), often reversible, of more and less fluid phases has been induced
in the living protoplasm of Didymium and Tradescantia by Belaf (1930).
There are many facts which suggest that the processes of cytokinesis
by furrowing, by vacuoles, by membranes, and by cell-plates are not
wholly distinct from one another. The formation of the fluid cell-plate
from the center outward suggests the cleaving action of vacuoles in the
sporangium of Phycomyces; whereas, when spores begin to separate at
the periphery after cytokinesis by cell-plates, the appearance is that of
furrowing. It may be helpful to think of cytokinesis by cell-plates in
vascular plants as a process whose peculiarities are due in large measure
to its close association with the mechanism of karyokinesis.

1" Dembowski and Ziegenspeck (1929), Dannehl and Ziegenspeck (1929).

CYTOKINESIS AND THE CELL WALL

173

The spindle of cytokinesis with its cell-plate commonly extends
laterally as a phragmoplast until it reaches the walls of the cell. In wide
cells with large vacuoles this may involve the formation of cytoplasmic
bridges (p. 151). As multinuclear endosperm becomes cellular, the
recently formed pairs of nuclei are connected by spindles on the flanks of
which additional spindles arise and so connect all the nuclei. This
involves a lateral extension of the spindle substance and apparently
also the use of any such substance remaining from the preceding mitosis.
Cell-plates appear in all the spindles and so subdivide the multinucleate
mass into uninucleate cells (Fig. 100). The development of the cellular

-.-:.'^'

v..

7 i N0.-;'

U /; y

r#

if/

^'

,..-^"

\

V r .'4'

Fig. 100. — Formation of cell partitions in endosperm of Iris. (After Jungers, 1931.)

stage in cycad embryos occurs in a similar manner (Chamberlain, 1910,
1916).

When one of the two telophase nuclei lies near the side of a large cell,
as in the angiosperm embryo sac or microspore, the phragmoplast may
curve sharply so that the cell-plate and subsequently formed membrane
cut off a small cell against the side of the large one (Fig. 125). In extreme
cases it may form a complete sphere about one nucleus and so cut out a
small cell which lies free in the cytoplasm of the original cell (Fig. 102).
Other modes of "free cell formation" are seen in ascospore development
(Fig. 88), in the delimitation of the egg in certain phycomycetes and of
embryo cells in certain gymnosperms (Fig. 103), and in certain animal
tissues (Rohde, 1923). In some cases, notably certain algse,^^ partition
membranes are reported to form between sister nuclei after the complete
disappearance of the achromatic figure.

11 Strasburger (1892), W. T. Swingle (1897), Mottier (1900).

174

INTRODUCTION TO CYTOLOGY

The Cell Wall. — Probably the most striking difference which meets
the eye in comparing animal and plant tissues is the degree of distinctness
with which the limits of the individual cells can be made out. Animal
cells, as a rule, are separated only by very thin membranes, which in
many tissues are so delicate as to be scarcely discernible; whereas the
cells of plants usually possess conspicuous firm walls, which, in the case
of woody plants, become greatly thickened and afford mechanical support
to large bodies.

i^USi

) % ^

t^.

n

Fig. 101. Fig. 102. Fig. 103.

Fig. 101. — Continued extension of partition wall after completion of mitosis in endosperm
of Physostegia virginiana. (After Sharp, 1911.)

Fig. 102. — Delimitation of generative cell in pollen grain of Scirpus. (The dark
bodies are degenerating nuclei of grains which fail to develop.) (After Piech, 1928.)

Fig. 103. — Embryonic cells in Ephedra, developed by "free cell-formation" in a com-
mon mass of protoplasm. (After Land, 1907.)

As shown in the foregoing section, the development of the cell wall in
vascular plants ordinarily begins with the formation of a fluid cell-plate
at the close of mitosis. Cytologists are not yet in agreement regarding
the exact relation of this layer to the primary wall layer, or middle lamella
(the "intercellular substance" and "cement" of early waiters). For
some time it was thought^' that the cell-plate became the middle lamella
directly, secondary and tertiary layers being deposited upon it by the
protoplasts on either side. Soon it was suggested, ^^ as already stated,
that the cell-plate splits, the middle lamella then being deposited between
its halves. As we have indicated (p. 171), the young cell-plate has been

12 E.g., by Strasburger (1875, 18826, 18846).

" Treub (1878). Strasburger adopted this view in 1898. It was supported by
the work of Timberlake (1900), C. E. Allen (1901), and a number of later writers.

CYTOKINESIS AND THE CELL WALL 175

shown to be a fluid film, and it now seems evident that the deposition of
salts and other matter in this film transforms it into the middle lamella.
Whatever its origin, the middle lamella may increase somewhat in thick-
ness before distinct secondary layers appear. The finer structure of the
middle lamella is not adequately known, but there is much to suggest
that it consists in reality of two or three differentiated layers, through
one of which the lamella splits when intercellular spaces are developed
by a rounding up of the cells.

It is probable that the deposition of the secondary layer begins after
the cell has reached nearly or quite its full size, though to this there are
apparently certain exceptions. The secondary layer, which seems to be
formed with considerable rapidity, differs from the primary layer chemi-
cally and in structure. There are circular or elongated areas in which
no secondary substance is deposited, so that the cells at these places are
separated only by the delicate primary membrane. Such a wall is said
to be "pitted," the primary layer extending across the pit being termed
the closing membrane. The central portion of this membrane (vascular
cells of gymnosperms chiefly) has sometimes a more or less conspicuous
thickening known as the torus. The portion of the membrane around
the torus is pierced by fine pores. In some cases these may become so
large and numerous that the torus appears to be suspended on a mesh-
work, while extreme cases are known in which it is held in place only
by a few strands. In bordered pits the secondary wall overarches the
margins of the closing membrane. In this type of pit, characteristic
chiefly of water-conducting cells of the gymnosperms, the closing mem-
brane is of such a nature that its position in the center of the pit is
readily altered. Probably because of changes in pressure it swings to the
side of the pit; the torus then lies against the pit opening, or "mouth,"
and the pit is blocked except for slow diffusion through the rather thick
torus.

The secondary wall layer may be even more limited in extent, only a

small portion of the primary wall being covered. Such is the case in

protoxylem cells, where the secondary layer is deposited in the form of

rings and spirals (Fig. 8, B, C). This form of thickening, together with

the peculiarly extensible character of their primary walls, permits the

great increase in length of these cells necessitated by the continued

growth of the young organs in which they chiefly function. In some

cells, notably the tracheids of certain gymnosperms and the vessels of

many angiosperms, a tertiary layer is deposited upon the secondary one.

This tertiary layer takes the form of slender spirals, rings, and other

figures resembling the secondary thickenings of protoxylem cells. ^^ It

has been shown in the protoxylem and metaxylem cells of the gourd

1* For a more complete account of such differentiations, see Eames and Mac-
Daniels (1925).

176 INTRODUCTION TO CYTOLOGY

Trichosanthes anguina that the position of the spiral and annular thicken-
ings is determined by peripheral bands of cytoplasm separated by more
vacuolate regions (Barkley, 1927).

Composition of the Cell Wall. — The principal constituents of the
completed cell walls of vascular plants are polysaccharides: cellulose,
hemicelluloses, and pectins. With these are often associated other
substances, notably lignin, suberin, and cutin.^^ The distribution of
these components in the various layers of the wall has been the subject
of many investigations.^" The earlier workers, who relied chiefly on
staining reactions, concluded that the middle lamella consists of pectic
compounds, while the secondary and tertiary layers are composed chiefly
of cellulose with or without lignin, pectin, and other additional materials.
Subsequent studies with chemical methods have shown that the middle
lamella, although it consists chiefly of pectin in one or more of its forms in
parenchyma, is principally lignin in woody tissues, and that staining
reactions cannot be safely relied upon as criteria of chemical composition.
What becomes of the original pectins in the young wall during its lignifi-
cation is still somewhat uncertain. Harlow finds that the secondary
layers of softwoods are appreciably lignified, while those of hardwoods,
with few exceptions, have practically no lignin. Tertiary layers are
often lignified.

The secondary and tertiary layers are made up of numerous thin
lamellae which appear to differ in the relative amounts of cellulose and
pectin present (van Wisselingh) as well as in physical properties. In the
wall of the flax fiber the layers have been shown to consist of spirally
arranged fibrils, the fibrils in contiguous layers running in opposite
directions (D. B. Anderson, 1927). In cotton the direction of coiling
changes at intervals along the fiber (Balls, 1923).

Suberin and cutin are varying mixtures of certain organic acids
present in part in the form of fats (Priestley, 1921). They are distin-
guished more by location than by composition, suberin appearing in
the walls of periderm cells (cork), while cutin occurs as a cuticle on the
epidermis and often in patches in the walls of subepidermal cells. In
the resin canals of conifer leaves the suberin is said to be deposited on the
primary layer and rarely on the secondary one (Gauba, 1926). Lee and
Priestley (1924) have ascribed the formation of plant cuticle to certain

^^ For an extensive account of walls and their constituents, see van Wisselingh
(1924). See also Czapek (1913), Molisch (1913), von Wettstein (1921o), Gleisberg
(1921), Grafe (1911, 1922), and Gortner (1929). Among the earlier papers on this
subject are those of Payen (1842), Fremy (1859), Kabsch (18636), Wiesner (1864,
1886), Mangin (1888-1893), Schulze (1890-1894), Gilson (1890), van Wissehngh
(1888, 1892, 1895), and Allen (1901).

1^ Among recent works, see especially Tupper-Carey and Priestley (1923), Ritter
(1925, 1928), Harlow (1927, 1928a6c, 1931), D. B. Anderson (1926, 1927, 1928), and
Scarth, Gibbs, and Spier (1929).

CYTOKINESIS AND THE CELL WALL 177

alterations in fatty substances which are produced in the protoplasts and
then migrate into and along the cell walls to the outer surface of the
epidermis. D. B. Anderson (1928) finds the outer wall of the epidermal
cell of Clivia to consist of (1) an inner layer of cellulose and pectin;
(2) a thin layer consisting mostly or wholly of pectin; (3) a cuticular
layer composed of (a) a region of cellulose and pectin lamellae containing
cutin and (6) a region of cutin and cellulose with little or no pectin;
and (4) a cuticle of pure cutin. In Aloe new cutin is secreted below the
old cuticle (Ziegenspeck, 1928).

A variety of mineral substances, such as silica, calcium carbonate,
and calcium oxalate, as well as more complex organic compounds, includ-
ing tannins, oils, and resins, are often deposited in the walls of old cells.
The heartwood of trees owes many of its qualities, such as color and
density, to the presence of these additional materials in the walls and
cell cavities.

Among the thallophytes many species have walls essentially like those
of higher plants, cellulose being the chief constituent. Others are
characterized by the predominance of other compounds, notably chitin in
zygomycetes, ascomycetes, basidiomycetes, and certain algae; pectins in
the bacteria; and keratin in myxomycetes. In many specific cases the
results of various workers do not agree. ^^

That the cell wall is not wholly an ergastic secretion, but contains
protoplasm in some form, is a view which has frequently been main-
tained.^^ Wiesner supposed the growing wall to be made up of regularly
arranged particles ("dermatosomes") connected by protoplasmic fibrils,
growth involving an intercalation of new particles between the old ones.
Hansteen-Cranner believes the wall to be a colloidal network of celluloses
and hemicelluloses with extensions of the plasma membrane in the
meshes. In the cellulose walls of a number of meristems Wood (1926)
found no more than 0.001 per cent of protein matter, which is less than
would be expected if the wall contained significant amounts of protoplasm.

Ultramicroscopic Structure of the Wall. — In connection with this
subject, which has recently come into prominence anew, it is of interest
to note the prophetic nature of certain early theories.'^ Von Mohl
advanced the view that the cell wall grows by the deposition of material
in successive laminae ("apposition theory"). On the other hand, Niigeli,
as a result of his researches on starch grains and the wall, concluded that
the wall is composed of molecular complexes called viicellce surrounded by
water films and that growth involves the intercalation of new micellae

'^ See van Wisselingh (1924) and literature there cited; also Mameli (1920),
Tiffany (1923), Wurdack (1923), and Thomas (1928).

18 Wiesner (1886 et seq.), Molisch (1888), Hansteen-Cranner (1919, 1922, 1926).

"Von Mohl (1853, 1858), Nageli (1858, 1863, 1864), Dippel (1879), Krabbe
(1887), Strasburger (1882, 1889), Wiesner (1886, 1890, 1892), Correns (1889, 1892,
1893).

178 INTRODUCTION TO CYTOLOGY

between the old ones ("intussusception theory"). Similar to this was
the later view of Wiesner, mentioned in the preceding paragraph. Stras-
burger held that the units are not micellse but single molecules linked
together in a reticular framework by their chemical affinities. He
attributed growth in area to simple stretching without intercalation of
particles, and growth in thickness to apposition of small "microsomes."
The longitudinal or spiral striations observed in many walls were thought
by some to indicate a linear arrangement of particles, while the fine
lamination of the wall was attributed either to unlike orientations in
contiguous lamina or to differences in water content.

The recent advances in our knowledge of the finer structure of the
cell wall have been made largely through studies of diffraction patterns
produced when X-rays^° are passed through cellulose and of the effects
obtained with polarized light. ^^ These studies, notably those of Sponsler
taken together with the chemical researches of Irvine, have shown that
the primary structural unit in the wall is an anhydrous glucose residue
with the formula CeHioOs. Such units are bound together in cellulose
chains by primary valencies, while the chains are in turn linked laterally
by secondary valencies in such a way that the units form a regular
three-dimensional space lattice (Fig. 104). In other words, the wall has
a crystalline structure. In the fibers of ramie {Boehmeria nivea) and the
Valonia cell wall, the distance between the centers of adjacent units is

o o

calculated to be about 5.15 A. longitudinally, 6.1 A. tangentially, and

o

5.4 A. radially (Sponsler). There is also evidence that the chains are
aggregated into bundles, or colloidal micellcB, these probably being
between 100 and 600 A. (0.01 to 0.06^) long and between 20 and 50 A.
(0.002 to 0.005/x) thick. The nature of the matter between these micellse,
or "crystallites," is unknown.

In a given visible layer of the wall there are many layers of primary
units, and the chains they form may be arranged parallel to the longitu-
dinal axis of the cell (ramie), or more or less obliquely (cotton). In
Valonia there are two main sets of chains which usually cross each other
at an angle of about 80°. This structure extends through the many-
layered wall. The chains are found to be parallel to the fine striae visible
on the surface of the wall. There are many facts which indicate that
it is not the surface upon which a layer is deposited that determines the
arrangement of its elements. It is reported that in the cotton fiber the
crystalline pattern becomes more perfect as the fiber matures (Clark
et al.). The micellse evidently come to be much closer together when a

20Herzog and Jancke (1919-1920), Sponsler (1925a6, 1926, 1928a6, 1929, 1931;
general account, 1933), Sponsler and Dore (1926, 1928), Bragg (1930), Clark, Pickett,
and Farr (1930), Astbury, Marwick, and Bernal (1932). See Frey (1926a), Meyer
and Mark (1928), and Seifriz (19296).

21 Balls (1923), Frey (19266, 1927, 1928), Preston (1931), D. B. Anderson (1927),
Mitchell (1930), M. Shaw (1929).

CYTOKINESIS AND THE CELL WALL

179

fiber is dried and farther apart when it is swollen (Frey). Presumably
the valencies binding the units into chains offer greater resistance to
swelling forces than do those uniting the chains laterally; hence a cellulose
fiber swells unequally in different directions. Sponsler and Dore have
shown that mercerization involves a lateral shift of the chains in the
wall and a partial rotation of their units, together with certain other
changes. The precise nature of the structural changes occurring as the

^^-S.40—^^

•^^^ •%)• •^J*

Aa^* SAt* •%?•

Fig. 104. — Diagrams of cell-wall structure as indicated by X-ray analysis. A, large
micellse with chains of glucose residue units showing in one of them, a, primary valence
forces; 6, secondary association forces; c, tertiary micellar forces. {After Scifriz, 19296.)
B, minute portion of cell wall in perspective, showing portions of six chains, each consisting
of three glucose residues (large circles) and their connecting oxygen atoms (small circles).
(After Spo?isler, 1931.) C, inner surface of wall; four chain molecules with four glucose
units shown in each. Black circles and white circles represent oxygen atoms and carbon
atoms, respectively; hydrogen atoms not shown. {After Sponsler, 1929.)

wall grows in area and becomes impregnated with other substances,
such as lignin, remains to be determined.

It is a suggestive fact, as pointed out by Sponsler, that about the only
solid materials deposited in large amounts by plant protoplasm, namely,
cellulose and starch, consist of CeHioOa units arranged in patterns.
There is similar evidence that certain animal products, such as chitin,
hair, and silk, have their molecules arranged in regular patterns. -^ It is
possible that this is due not only to the chemical properties of protoplasm
and the forces of crystallization but also to certain structural features in
protoplasm itself. Seifriz (19296) has emphasized the idea that the
contractility, cohesiveness, elasticity, and tensile strength of protoplasm,

" Herzog and Jancke (1921), Brill (1923), Astbury and Street (1931), Astbury and
Woods (1932).

180 INTRODUCTION TO CYTOLOGY

as well as such phenomena as conductance and polarity, are best explained
on the assumption that protoplasm itself possesses structural units
arranged in linear series, especially since certain other materials exhibiting
such properties are known to have such a structure (see Beutner, 1933).

The Walls of Spores. — In bryophytes and vascular plants the walls of
spores are developed in two general ways: (1) by the successive formation
of layers within the original membrane by the protoplast, often with the
addition of material from the anther fluid, and (2) by the deposition of
material on the outside of the original membrane by a Plasmodium
formed by tapetal cells.

In the first method a more or less temporary gelatinous layer is ordi-
narily developed around each of the young spores, either before or after
these have separated from one another (Fig. 96). Upon the inner surface
of this special layer the protoplast deposits the exine, or outer wall layer.^^
In many cases this is at first a homogeneous layer that soon differentiates
into an outer lamella and an inner zone with net-like thickenings and
spines (the ''mesospore"). Finally, there is deposited an inner layer, or
intine. This mode of development is widely prevalent, the walls of most
spores showing two principal layers, or "coats": an intine, which later
becomes greatly extended to form the pollen tube in seed plants, and an
exine, which is characteristically thickened and sculptured. In angio-
sperm pollen the exine has one or more definitely differentiated germ
pores through which pollen tubes are to emerge. The characters of the
resistant exine are of much value in determining the relationships of
living and fossil plants. ^^ The exine, although it begins to differentiate
in contact with the protoplast, may continue to thicken and develop its
peculiar markings after it has been separated from the protoplast by
other layers.-^ In an extensive study of the composition of pollen-grain
walls Biourge (1892) showed that they contain cutin, callose, cellulose,
and pectic substances, singly or in various combinations.

The highly specialized coats of the megaspore of Selaginella have been
repeatedly studied. In Selaginella rupestris^^ the coats begin to differ-
entiate in the midst of a thick gelatinous layer developed at the close of
the divisions delimiting the spores. The exospore first appears as a
double zone, the outer part of which becomes the perinium (Fig. 105)
The small protoplast now expands and pushes outward the undifferen-
tiated inner portion of the gelatinous layer, and, as it does so, a second
coat, the endospore, is formed at its surface. In *S. emiliana the exospore
and endospore develop simultaneously. Lyon finds two coats in place

^^ E.g., Ipomoea purpurea (Beer, 1911).

2^ E.g., Wodehouse (1928 et seq.) on living plants. For references on fossil pollen,
see Erdtnian (1927, 1930) and Sears (1932).

"Beer (1905, 1911), Tischler (1908).

2«Lyon (1905). The accounts of Fitting (1900, 1906) differ from this in certain
details.

CYTOKINESIS AND THE CELL WALL

181

of the three reported by Fitting but points out that a portion of the
gelatinous layer may remain undifferentiated until a late stage and thus
appear like a third coat.

In vascular plants the sporangium (the anther in angiosperms) is
lined by a layer of special nutritive cells known as the tapetum. In
many known cases, including Equisetum, Botrychium, Marsilia, and a
number of angiosperms, the boundaries of these cells break down, allowing
the protoplasts to coalesce and form a "tapetal Plasmodium," or "peri-
plasmodium." This flows in among the immature spores and contributes
to the development of their coats (Fig. 106). In Equisetum the spore
has three coats: an endospore, an exospore, and a perispore, the last being
formed by the Plasmodium and consisting of several layers. Upon the

Fig. 105. Fig. 106.

Fig. 105.— Developing megaspore coats of Selagindla rupestris. p, protoplast with nu-
cleus; en, endospore; s.m., undifferentiated portion of gelatinous layer; ex., exospore, of
which the denser portion is the "perinium." (After Lyon, 1905.)

Fig. 106. — Exine of microspore (right) developing in contact with tapetal Plasmodium
(left) in Commelina. (After Tischler, 1915.)

original membrane the Plasmodium deposits successively an inner
gelatinous layer, a second layer, an outer gelatinous layer, and finally a
layer which later splits up to form the characteristic appendages of the
spore. These four layers together constitute the perispore. While they
are in the process of formation the original spore membrane becomes
transformed into the exospore, and within it the endospore is developed
last of all."

In the ascomycete Hydnotrya Tulasnei each spore, after its delimita-
tion from the cytoplasm of the ascus (p. 158), is surrounded by a thin
endospore. In the ascus cytoplasm near each spore there appears a
rounded mass of fluid, which enlarges, gradually surrounds the spore, and
develops into the elaborate exospore. In this case, therefore, the wall
material is visible before its deposition on the spore (Nemec, 1929d).

The Cell Membranes of Animals. — The problem of the intimate
relation of protoplasm to partitions which subdivide it into cells is encoun-

27 Beer (190%), Hannig (1911).

182 INTRODUCTION TO CYTOLOGY

tered in animals as well as in plants. Zoologists have differed widely in
their interpretations of the "intercellular substance" composing such
membranes in animal tissues. Heidenhain and Rohde have emphasized
the view that this substance is metaplasm, a special form of living sub-
stance which differentiates in protoplasm in connection with special
functions and which is capable of growth, response to certain stimuli, and
further differentiation. A. Meyer has strongly opposed this conception,
holding that the albuminous intercellular substance of animals, like the
carbohydrate wall of plants, is ergastic in nature and not to be classed
with metaplasmic (alloplasmatic; Meyer) differentiations. The fibrils
frequently observed in the intercellular substance, which many have taken
as indications of its metaplasmic nature, Meyer regards as modifications
of the ergastic material or as substances which have arisen in protoplasmic
connections.^^

The membranes of animal cells differ from those of most plants in
consisting largely of such substances as chitin, elastin, keratin, and gelatin
rather than cellulose and related carbohydrates. Cellulose has been
found only rarely among animals. In the ascidians, as has long been
known, the outer layer of the body wall consists largely of cellulose. A
cellulose-like substance has recently been found in the skeletal plates
of an infusorian (Dogiel, 1923a).

28 Heidenhain (1902, 1907), Rohde (1908, 1914, 1923), Meyer (1896, 1920); see
also p. 45. See the general account by Studnicka (1925).

CHAPTER XIII
ATYPICAL MITOSIS AND OTHER NUCLEAR PHENOMENA

In the foregoing chapters attention has been restricted largely to
typical nuclei and nuclear division as these are observed in the great
majority of plant and animal tissues. In this chapter will be reviewed
briefly certain additional modes of division and other phenomena which,
though in many instances abnormal, have served to broaden our knowl-
edge of the nucleus and its significance.

Amitosis.^ — In amitotic, or direct, nuclear division the nucleus
simply constricts and separates into two portions while in the metabolic
condition, no condensed chromosomes or achromatic
figure being formed (Fig. 107). When the portions are
very unequal in size, the process is called "nuclear bud-
ding"; when they are more than two in number it is
referred to as "nuclear fragmentation." Such nuclear
divisions are not followed by cytokinesis; the cells thus
come to have two or more nuclei. Amitosis was at one
time looked upon as the prevailing mode of nuclear divi-
sion, mitosis even being somewhat exceptional, but the
true state of affairs, so far as higher organisms are con-
cerned, has turned out to be quite the reverse, mitosis
occurring almost universally and true amitosis in com-
paratively few well-authenticated cases. It is now
evident that binucleate cells, constricted or fusing nuclei,
and especially the results of aberrant mitosis have often Amitosis in inter-
been hastily construed as amitotic division, and it is in ^°^® °^ Chara.
the light of this fact that many reports of amitosis should be read.^

The amitotic phenomena so frequently reported in cells with a dis-
tinctly nutritive function, such as certain gland cells of animals and
tapetal, antipodal, and endosperm cells of angiosperms, have been
thought to substantiate the widely adopted hypothesis that amitosis
aids in metabolism by increasing the nuclear surface. The supposed
amitosis in tapetal cells has been shown in a number of instances to be
aberrant mitosis (Bonnet), but Tischler considers it probable that true

1 Bonnet (1912), Beer and Arber (1919), Schtirhoff (1920), Kater (1927a). For
reviews of the literature pertaining to amitosis and irregular mitosis in plants, see
Tischler (1921-1922, Chap. VII) and Schurhoff (1926). For the literature on amitosis
in animals, see Conklin (1917), Nakahara (19186), and Wilson (1925, p. 214).

183

Fig. 107.—

184 INTRODUCTION TO CYTOLOGY

amitosis as well as deranged mitosis and nuclear fusion may sometimes
occur in such cells and the periplasmodia they form.

Another very prevalent opinion regarding the significance of amitosis
is that expressed by Flemming (1891), namely, that the process is
primarily a degenerative phenomenon, since it is so frequently observed
in pathological tissues. In the words of vom Rath (1891), "when once
a cell [nucleus] has undergone amitotic division it may indeed continue
to divide for a time by amitosis, but inevitably perishes in the end."
That this interpretation cannot be of universal application has been
contended by those who have found amitosis or amitosis-like appearances
in cells which show no other sign of degeneration. ^ It is probably
significant, however, that most if not all of the observed cases of amitosis
in living tissues have occurred in cultures which were growing old or
showing distinct signs of degeneration, or in which the medium was
unfavorable for normal growth.^ It is the opinion of Kofoid (1923) that
the supposed amitosis in Protozoa is a degenerative or pathological
phenomenon, or in some cases a special form of mitosis which has been
incorrectly interpreted. Conklin (1917) was able to show that the
amitosis-like appearances in Crepidula eggs and embryos were all instances
of abnormal mitosis and cytokinesis. He observed that the chromosomes
might scatter and fail to unite in a single nucleus; or mitosis might occur
without cytokinesis, giving cells with two or more nuclei; or certain
chromosomes might fail to separate in the anaphase, leaving a bridge
between the sister nuclei; or the nuclear membrane might persist through-
out mitosis and finally constrict at the middle. As a result of his many
observations and an examination of the evidence offered by others he
concluded that there is not a single case of true amitosis known in nor-
mally differentiating cells.

The literature contains conflicting opinions on the question of whether
or not a portion of a nucleus resulting from amitosis can subsequently
divide by mitosis. The observation of amitosis under abnormal con-
ditions followed by mitosis after the tissue has been restored to a normal
environment is not conclusive evidence on this point unless it is shown
that the mitotically dividing nucleus is actually a product of amitosis.
Chambers (1917a) observed that after a nucleus is pinched in two with
the micromanipulator the parts may reunite and undergo mitosis. In
wound tissue of the stem of Tradescantia, Conard (1926a, 1928) has
shown that markedly lobed nuclei may enter mitosis while in this form,
also that they sometimes become constricted into two separate portions
while in the metabolic or prophase stage. Two such portions may then

2 Des Cilleuls (1914) on rabbit cells; Saguchi (1917) and Helvestine (1921) on
ciliated cells of animals; Bast (1921) on bone; Kisser (1922), Conard (1926rt, 1928) and
others on vegetative tissues of plants; F. E. V. Smith (1923) on Saprolegnia.

3 Lewis and Lewis (1924), Drew (1923).

ATYPICAL MITOSIS AND OTHER NUCLEAR PHENOMENA 185

undergo mitosis side by side, the two spindles often uniting to form only
two daughter nuclei. Examination of the chromosomes in such pairs of
mitotic figures shows that each nuclear portion after amitosis has only a
portion of the full complement, and that certain chromosomes have been
fragmented in the amitotic division. The two portions together con-
stitute a complete complement. Since some fragments may pass to the
poles along with the unbroken chromosomes, the union of the mitotic figures
brings about a partial restoration of the original nuclear organization.

These phenomena suggest that the common failure of amitotic nuclear
fragments to undergo mitosis is due not so much to the effects of amitosis
itself as to a persistence of the abnormal conditions which originally
induced amitotic division. Were such nuclei to continue dividing in a
growing and differentiating tissue, derangements in their nuclear organi-
zation might well be reflected in abnormalities in the results of differen-
tiation; and were descendants of such nuclei to be transmitted through
gametes to the next generation, abnormalities in development would be
expected there also. The basis for such an expectation is seen in the
known results of chromosome fragmentation and translocation to be
described in Chapter XVIII. At present it has not been shown in any
case that the descendants of true amitotic nuclei ever become the nuclei
of functional gametes.

Induced Aberrations of Mitosis. — Aberrations of mitosis like those
so often mistaken for amitosis may be induced by a considerable variety
of means. For example, when root tips and other plant tissues are
subjected to the action of chloral hydrate and other anesthetizing agents,*
the normal course of mitosis is disturbed in various degrees, depending
on the strength of the dose. As a rule the achromatic figure develops
poorly or not at all, and the chromosomes become irregularly scattered
in the cell (Fig. 108). They may form one or more groups and reorganize
nuclei which often remain connected by bridges or undergo fusion.
Hence it is not uncommon to find in such tissues all gradations between
normal mitosis and what looks like amitosis. The latter condition is
known as " pseudoamitosis" (Haecker). Nemec and Sakamura attribute
such scattering of chromosomes to protoplasmic streaming induced by
the experimental agency; this is in harmony with G. Ritter's (1911)
observation that the nucleus may sometimes be displaced by streaming
induced by the wounding of near-by cells. The experiments of Van
Regemorter indicate that the failure of the spindle substance to develop
a regular figure in chloralized tissue is due to a destruction or impairment
of the cell's polarity, the recovery from the effect of the reagent involving
a return to the properly polarized condition.

* Pfeffer (1899), Nathansohn (1900a), NSmec (1904, 1910a, 1929c), Kemp (1910),
Sakamura (1920), Van Regemorter (1926). The effects of many other agents are
described by Yamaha (1927o6).

186

INTRODUCTION TO CYTOLOGY

Abnormal temperatures, either high or low, are known to cause
aberrations of mitosis in somatic cells and microsporocytes.^ Such effects
are responsible for the origin of certain races of plants with altered
chromosome numbers, as will be shown in Chapter XX.

Wounding, such as that occasioned by grafting or decapitation, often
disturbs the mitotic process, cells or even branches with altered chromo-

FiG. 108. — Abnormal mitosis in chloralized root cells of Vicia. A, irregular distribution
of chromosomes. B, scattered chromosomes beginning to assume nuclear form. C,
nucleus reconstructed by scattered chromosomes. D, chromosomes reconstructing three
separate nuclei instead of one. E, chromosomes reconstructing two nuclei connected by a
bridge. F, amitosis-like appearance resulting from condition shown in E. {After Saka-
mura, 1920.)

some numbers sometimes resulting.^ Abnormalities also occur in the
presence of parasites in gall tissue.^

The effects produced by radiations of high frequency^ are of special
interest in view of their employment in attempts to analyze the functional
differentiations of the chromosomes (Chapters XVIII and XX). Among
such radiations the X-rays have been studied most. The cytoplasm of
cells treated with these rays may show alterations in viscosity^ and rate of
streaming, ^° as well as certain degenerative aspects, such as turbidity and

^ Borgenstam (1922) on Syringa, Belling (1925a) on Uvularia, Sakamura and Stow
(1926) on Gagea, Stow (1926, 1927) and Fukuda (1927) on Solanum, de Mol (1927c,
1928a-c?) on Hyacinthus and Tulipa, Rybin (19276) on Nicotiana, Shimotomai (1927)
on Scilla, Michaelis (1926, 1928) on Epilohium and (Enothera, Bleier (19306) on
Triticum, Koshuchow (1928) on Zea and Cucumis. Bleier (1931c) questions the
evidence for the role of temperature in cau.sing natural sterility in Solarium.

« Winkler (1916) and J0rgensen (1928) on Solanum, Kostoff (1930c, 193 Ice) and
Kostoff and Kendall (1931a) on Nicotiana, Lindstrom and Koos (1931) on tomato.

^ Winge (1927d) on crown gall of Beta; Nemec (1924, 1926) and Kostoff and Kendall
(1929a6, 1930a6) on galls of other types.

^ Certain biological effects of such radiations are reviewed by Packard (1931).
Bersa (1926) gives a bibliography. See Popoff (1931) on cell stimulation.

9 Fairbrother (1928), Wels (1924), Jansson (1927), Nadson (1925).

»» M. Williams (1923, 1925a), Zuelzer and Philipp (1925).

ATYPICAL MITOSIS AND OTHER NUCLEAR PHENOMENA 187

vacuolation.'i The chromatic matter of the nucleus may contract into a
deeply staining mass (pyknosis), diffuse in the karyolymph (karyolysis),
or adhere to the membrane. Nuclei about to divide are prevented from
doing so, but those in division usually continue or complete the process.
Mitosis is often very aberrant, ^^ in many respects resembling that seen
in chloralized cells (Fig. 109). The chromosomes are irregularly dis-

D

Fig. 109. — The effect of Rontgen rays on mitosis in cornea cells of Salamandra. A,
chromatic bridge. B, " pseudoamitosis." C, distribution of chromosomes to three cen-
ters. D, partial pyknosis; some of the chromosomes have passed to the poles. {After
Alberti and Politzer, 1923.)

tributed, hence nuclei and cells with polyploid or otherwise altered
chromosome complements are frequently observed in irradiated tissues.
The reported occurrence of just such phenomena in ordinary and arti-
ficially induced tumors^^ has excited much interest in connection with the
cancer problem, i"* but at present very little can be said concerning causal
relationships.

Of great interest are the more definitely localized effects produced
by irradiation with X-rays. ^^ It is found that with proper dosages a

11 Nadson (1925), Bisceglie and Bucciardi (1929).

12 E.g., Komuro (1917 et seq.), Pekarek (1927), and Patten and Wigoder (1930) on
Vicia roots; Alberti and Politzer (1923, 1924) and Politzer (1925) on cornea cells;
Strangeways and Oakley (1923), Strangeways and Hopwood (1926), and Kemp and
Juul (1930) on tissue cultures; Pauli and Hartmann (1924) and Pauli and Politzer
(1929) on cathode rays; and Bersa (1927) on Zea roots.

13 In animals: Howard and Schultz (1910), Boveri (1914a), Bichler (1914), Yama-
giwa and Ichikawa (1915 et seq.), Lewis and Lockwood (1929), Winge (1930a), Levine
(1931, good bibliography), and others.

In plants: Komuro (1922, 1924f/e, 1925a6c, 1928a6c, 1930ac), Winge (1927^),
Levine (1929), Goldschmidt and Fisher (1929).

" See the reviews by Ludford (1925) and Levine (1931).

15 H. J. MuUer (1926, 1927, 1928a6c, 19296c, 1930a6c), Muller and Painter (1929),
Painter and Muller (1929), Muller and Altenburg (1930), J. T. Patterson (1928, 1929,
1930a6, 1931a), Patterson and Painter (1931), Mavor (1921, 1922, 1923o6c, 1925),
Hanson (1928), Dobzhansky (1929a6cd, IdSOad, 1931a6). The foregoing are on
Drosophila. For general accounts, see Muller (1929c, 19306). In plants: Stadler
(1928a6c, 1929, 1930a5c, 1931a6, 1932), Goodspeed and Olson (1928a6), Goodspeed
(1929o6, 1930a6c, 1932), Goodspeed and Avery (1930), de Mol (19306, 1931a6c),
M. Nawaschin (1931c), Delaunay (1930), Randolph (1932), Lewitsky and Araratian
(1931). For a general statement, see Stadler (19306).

188 INTRODUCTION TO CYTOLOGY

single chromosome only, or even but a small portion of it, may be elimi-
nated or changed. Often a portion of a chromosome becomes detached
from the remainder {Jragmentation) , or attached to another chromosome
{translocation), or reversed in position {inversion), or rendered functionless
{inactivation) , or removed altogether {deletion). These and other altera-
tions, including changes in individual genes, may be brought about not
only during certain phases of mitosis but also when the nuclei are in the
metabolic condition, as in pollen and dormant seeds. This affords strong
support to the view that some characteristic organization is maintained
by each chromosome at all stages of the mitotic cycle. Treatments with
ultra-violet radiations^^ and the rays emitted from radium ^^ have also
been found to cause alterations of the protoplasm and of nuclear behavior,
some of which are comparable to those produced by X-rays. As will
appear in later chapters, it is such specific effects of irradiation, partic-
ularly those obtained with X-rays, which give the method a high value in
modern cytogenetic analysis.

The discovery of "mitogenetic rays" emitted by growing tissues was
announced in 1923 by Gurwitsch,^^ who reported that when a growing
onion root (as "sender" of the rays) is pointed directly at the region of
cell-division in another root (as "detector") and left for some hours,
the detector shows more mitoses in the side toward the sender, the excess
over the other side being as much as 50 per cent. Metabolically active
tissues in considerable variety have since been reported to emit such rays,
and growing yeast cultures have come to be favorite detectors. Attempts
to determine the nature of the rays have led to the belief that they are
ultra-violet radiations of very low energy content, and that they may
possibly be associated with oxidation.

The value of the evidence for the existence of such rays, or for a
causal relation between them and the effects observed, has been adversely
criticized by a number of investigators.^^ Reasons for discrepancies in
the results of various trials are beginning to be apparent in differences
in technique and in the condition of the materials used. At present it
appears probable that radiations produced by processes occurring in

i« Takamine (1923), Schleip (1923), Addoms (1927), Just (1933), Heilbrunn and
Young (1930), Bucholtz (1931).

1' Mohr (1919), M. Williams (1925a), Gager and Blakeslee (1927), Canti and Spear
(1927, 1929), Hanson and Heys (1928, 1929), Hanson and Winkleman (1929), Levine
(1929), Stein (1929), Stadler (19286, 19316), Stoel (1928), Goodspeed (19295), Good-
speed and Avery (1930).

18 For general accounts, see Gurwitsch (1925, 1926, 1929, 1932), Reiter and Gdbor
(1928), and Hollaender and Schoeffel (1931). See also Wagner (1927, 1928), Magrou
and Magrou (1927), Baron (1928, 1930), Reiter and Gdbor (1929), Frank (1929),
Siebert (1928), Borodin (1930), Kisliak-Statkewitsch (1927), Loos (1930), Ferguson and
Rahn (1933), Tuthill and Rahn (1933).

19 Guttenberg (1928), W. Schwarz (1928), Rossmann (1929), Taylor and Harvey
(1931), Richards and Taylor (1932), Moissejewa (1931).

ATYPICAL MITOSIS AND OTHER NUCLEAR PHENOMENA 189

tissues are an important cause of certain phenomena of cell growth and
multiplication.

Karyosome Nuclei. — Numerous peculiar types of nuclear organi-
zation and behavior are known in the lower organisms, notably among
flagellates and Protozoa.-" Of these types one of the most prevalent is

%•'

^"-4-^

Fig. 110. — Mitosis in Oxyrrhis marina. 1, living individual, showing two flagella and
two food bodies. 2, 3, and 4 show the paradesmose between the diverging centrioles.
6, endosome elongated and about to divide. 6, early telophase. 7, 8, fission in progress.
{After Hall, 1925a.)

that in which the nucleus contains a large, deeply staining body known as
the karyosome, or endosome ^^ It may contain the only highly chromatic
substance in the nucleus at certain stages, but critical studies have shown
that the chromosomes, like those in ordinary nuclei, develop in the
surrounding region (Figs. 110, 111). The karyosome usually reacts
negatively in the Feulgen test,-^ but it may still be concerned in the
changes in chromaticity of the chromosomes (c/. p. 119). Ordinarily

20 Pqj. general accounts of the nuclei of Protista, see M. Hartmann (1911), Minchin
(1912), Doflein (1916), Calkins (1926) and Belaf (1926).

^^ Minchin's term endosome is probably used more widely now than karyosome
(Hartmann). Other terms are Binnenkorper (Doflein) and nucleolo-centrosome
(Keuten). Much of the confusion in the older literature on this subject has been
clarified by recent work; see especially Belaf (1926), Hall (1925a) and Hall and
Powell (1928).

22Reichenow (1928), Roskin and Romanova (1928).

190

INTRODUCTION TO CYTOLOGY

the karyosome elongates and divides by constriction at the time of
nuclear division. Often it forms a dumb-bell-shaped structure, about
the middle of which the chromatic granules or chromosomes are grouped
and separated into two masses as the nuclear membrane remains intact
(Fig. 111). Frequently it does not divide until the elongated chromo-
somes have reached the poles. The chromosomes lying parallel to
the axis of the division figure may appear to break in two at the middle,
but it has been shown by Hall and others that in the prophase they
are split and opened out from one end, the supposed transverse division

I

Fig. 111. — Mitosis in Heteronema acus. (After Loefer, 1931.)

being merely the completion of the separation at the other end.^^ It is
claimed that in Euglena the split is present in the preceding telophase.^*
While these changes are in progress the centrosome and motor elements,
if present, become doubled in number in various ways to form the cor-
responding elements of the daughter cells^^ (see p. 223).

In the Plasmodiophorales^^ the chromosomes form a ring at the equa-
tor of the mitotic figure; as this ring divides and separates to the two poles,
the karyosome it encompasses does likewise. In the green alga Clado-
phora glomerata, the nucleolus elongates and divides as the split chromo-
somes separate (Fig. 112). The nuclear membrane remains intact
throughout mitosis, and at certain stages the whole figure bears a striking
resemblance to those described above." The behavior of the nucleolus

23 R. P. Hall on Menoidium (1923), Oxyrrhis (1925a) and Ceratium (1925fc); Hall
and Powell (1928) on Peranema; Loefer (1931) on Heteronema.

24Tschenzoff (1916), Tannreuther (1923), Ratcliffe (1927).

2^ Kofoid and Christiansen (1915), Kofoid and Swezy (1915 et seq.), Swezy (1915,
1916, 1922), Wenrich (1921), Boeck (1917), Hall (1923, 1925a6), Bunting and Wenrich
(1929), Kater (1929).

26 S. Nawaschin (18996), Winge (1912) on Sorodiscus, Cook (1928) on Ldgniera,
Home (1930) on Spongospora, Milovidov (1931) on Plasmodiophora. For other
accounts of mitosis in myxomycetes, see Strasburger (1884a), Harper (1900a), Jahn
(1904, 1908, 1911), Olive (1907), Prowazek (1905), Kranzlin (1907), and Skupieiiski
(1928).

2^ T'Serclaes (1922). For other recent accounts of mitosis in green algse, see
Czurda (1922a6) and Geitler (1930) on Spirogyra, Foyn (1929) on Cladophora and
Ulva, Hartmann (1921) on Eudorina, Higgins (1930) and Schussnig (1930) on Clado-
phora, Kretschmer (1930) and Ohashi (1930) on (Edogoniu7n, Mundie (1929) on Vauch-
eria, Peterschilka (1922) on Mougeotia, Schussnig (1928a6) on Caulerpa, and M.
Williams (19256, 1926) on C odium and Vaucheria.

ATYPICAL MITOSIS AND OTHER NUCLEAR PHENOMENA 191

here tends to be somewhat irregular; in related types it disappears in the
prophase, as in higher plants.'^

Such a range of structural conditions as that reviewed in the foregoing
paragraphs suggests that karyosome nuclei differ from the ordinary nuclei
of higher organisms chiefly in the amount of nucleolar matter present and
in its tendency to be associated with other elements, notably centrosomes.
In higher plants the nucleolar matter, which has some structural and
functional relationship with the chromosomes (p. 118), ordinarily dis-
appears before the metaphase, but, if any remains, it may sometimes
undergo division in the mitotic figure (p. 164). In such forms as Clado-
phora the latter mode of behavior occurs with some regularity. In still

.«-'

Fig. 112. — Mitosis
in Cladophora glomerata.
(After T'Serclaes, 1922.)

Fig. 113. — Stages of cell-division
in Anaboena circinalis. {After Haupt,
1923.)

other forms centrosomal elements are present also. How such conditions
have come about is entirely a matter of conjecture. It is not to be
assumed, however, that all the cytological differentiations in Protista
can be fully explained by reference to those in higher organisms.

With regard to their chromosomal mechanism, it becomes increasingly
evident as critical researches multiply that many of the Protista are in
certain essential features like higher forms. Both Metcalf (1915) and
Kofoid (1915, 1923) have emphasized the fundamental similarity of
protozoan and metazoan nuclei. In some representatives of all the main
groups of Protozoa, elongated chromosomes, which split and show evi-
dence of being made up like those of Metazoa, have been found. Kofoid
states that the chromosomes are constant in number and differ in size
and shape in certain flagellates. There are genetic data which indicate
that, so far as their life cycles show agreement. Protozoa and Metazoa
exhibit similar modes of inheritance (see Jennings, 1920). In many
Protista, on the contrary, this high degree of nuclear differentiation seems

28 Nemec (19106) on the variety simplicior; Carter (1919c) on Rhizoclonium.

192 INTRODUCTION TO CYTOLOGY

not to have been reached. To what extent the apparently simpler types
of nuclear organization and of division ("promitosis") represent stages
in the evolution of more complex types must remain for the future to
determine.

Blue-green Algae. — The structure of the cell in the Cyanophycese
has long been a subject of controversy. ^^ The chief question at issue has
been the nature of the central region, which appears relatively colorless
and ill defined in living material. By some observers it has been denied
that this in any way corresponds to a nucleus, the contention being that
blue-green algse, like bacteria, have a cell organization fundamentally
different from that of other organisms. Others have maintained that
the central region, although it is not sharply delimited, may be viewed
as a "primitive nucleus," since it is occupied by a material which often
stains like "chromatin" and tends to be distributed rather equally to
the daughter cells during cell-division'^" (Fig. 113). It is reported
that in some genera it contains a material reacting positively to the Feul-
gen test, also that in Nostoc no nucleic acid can be demonstrated
although its radicles are present. ^^ The degree of distinctness with
which such "nuclear" materials are aggregated in the central region
varies widely.

At present it is difficult to place a proper evaluation on the conflicting
claims made in this field. Many have provisionally concluded with
Guilliermond that in at least some blue-green algae there is a primitive
nucleus consisting mainly of chromatic matter often arranged in strands,
that such strands are broken as the whole mass divides by a process some-
what intermediate between amitosis and mitosis, and that no distinct
membrane appears about the mass because the latter is almost constantly
in process of division. Definite chromosomes and longitudinal division
of chromatic strands have not been demonstrated.

The peripheral cytoplasm in such cells with a central body contains
chlorophyll, together with phycocyanin or phycoerythrin. The exact
manner in which these pigments are borne is uncertain,^- but it is thought
probable that they occur in numerous minute droplets which may some-

23 Among cytological works on the Cyanophyceae are those of Biitschh (1896),
Fischer (1897, 1905), Hegler (1901), Kohl (1903), Olive (1904), Phillips (1904), Gard-
ner (1906), Guilliermond (1906, 19256, 1926), W. H. Brown (1911a), Acton (1914),
Baumgartel (1920), Haupt (1923), S. Lee (1927), Pascher (1929), and Prat (1925).
Convenient resumes are given by Olive and Haupt. Lloyd (1924) has given special
attention to the pigments.

™Kohl (1903) on Tohjpothrix; Olive (1904) on Oscillatoria; W. H. Brown (1911)
on Lyngbya; Guilliermond (1906) on Phormidium, Nostoc, and Rivularia; Haupt
(1923) on Anabcena and Gloeocapsa.

^' Poljansky and Petruschewsky (1929) on Oscillatoria, Tolypothrix, Spirulina, and
Gloeotrichia ; Mockeridge (1927) on Nostoc.

^^ See the discussion of fluorescent colors by Lloyd (1924).

• ATYPICAL MITOSIS AND OTHER NUCLEAR PHENOMENA 193

times aggregate to form groups with a plastid-like appearance. Ergastic
substances, such as glycogen, fat globules, and "cyanophycin granules,"
also occur and vary in abundance under different nutritive conditions.
Although the cytoplasm is rich in lipides, no chondriosomes are present,
according to Guilliermond. This author describes a vacuome consisting
of small vacuoles containing metachromatin, the precipitation of this
substance giving the granules mistaken for nuclear matter by certain
observers.

It is tempting to search among lowly organized plants for light on
the origin of structures and modes of behavior seen in more complex
types. Although it is improbable that the Cyanophycese had anything
to do with the evolution of higher plants, the organization they exhibit
affords a hint as to stages which may have occurred in the evolution of
the typical nucleus and its elaborate mode of division. The view has
long been entertained that certain leading constituents of primitive
protoplasm may gradually have aggregated to form a definite organ, the
nucleus, thus securing the advantages of more consistent interaction and
orderly distribution during growth and differentiation. By arranging
various blue-green and other algse in a suitable series, one can at least
illustrate "the conception of cell structure which implies differentiated
regions of a colloidal system in which special processes have become
localized and tend to remain fixed" (Harper, 1919).

Bacteria. — The bacterial cell presents many obstacles to cytological
study. It is extraordinarily small and is often surrounded by a layer of
material which interferes with fixation; moreover, it contains ergastic
substances which vary in amount and present a great variety of aspects in
different preparations. Opinion has ranged all the way from the view
that the whole bacterium is a naked nucleus to the idea that it is wholly
cytoplasm with inclusions. Most prevalent has been the view that
scattered nucleo-proteins are present but not aggregated into a definite
nucleus, the cell thus illustrating a primitive stage in the evolution of the
nucleus-and-cytoplasm type of organization.^^

The literature contains many descriptions of small granules supposed

to be nuclei or at least granules of "nuclear matter," and the aggregation

of such granules to form peculiar spiral masses has frequently been

reported. The spiral masses seem to be modifications of the cytoplasm

about the vacuoles (Meyer), while the nature of the supposed nuclei

has been rendered doubtful in most cases by the presence of ergastic

masses which may simulate nuclei. In Bacillus pasteurianus, Meyer

regarded as nuclei certain minute bodies which he was able to distinguish

from the globules of fat, volutin, and glycogen. The frequently paired

arrangement of such small bodies was suggestive of division, and their

33 See the accounts by Meyer (1912), Dobell (19116), Frost (1917), Lohnis (1922),
Kirchensteins (1922a), Enderlein (1925), Petit (1927), and Wdmoscher (1930).

194 INTRODUCTION TO CYTOLOGY

position at the center of developing spores recalled the behavior of nuclei
elsewhere.

That certain bacteria may contain definite nuclei in spite of the above
uncertainties has been rendered more probable by the recent work of
Stoughton (1929) on Bacterium (Pseudomonas) malvacearum. By
employing the methods of Enderlein (1925) and Nakanishi (1901), in
which obscuring nutritive materials are removed and the cells are stained
without drying, this investigator has been able to differentiate a central
body about 0.5^1 in diameter which shows an affinity for basic dyes and
passes through a definite division cycle correlated with that of the cell.
In some cases this central body elongates and becomes divided with the
cell as the latter constricts, w^hile in others it becomes dumb-bell shaped
and completes its division before the cell divides by forming a transverse
wall. It can be seen in living cells under dark-field illumination. It is
Stoughton's conclusion that this central body is in all probability either a
nucleus or possibly (following Enderlein's theory) a nucleus imbedded in a
mass of chromatic food-reserve substance. Appearances very suggestive
of nuclear fusion and division have been reported for the avian tubercle
bacillus (Lindegren and Mellon, 1932).

Chromidia. — In 1902 R. Hertwig described in Actinospharium and
certain other rhizopods what appeared to be an emission of chromatic
granules from the nucleus into the cytoplasm. The nucleus might even
break up completely into such granules. He called these granules
chromidia and set forth a "chromidia hypothesis." According to those
who developed this hypothesis, ^^ there are in an ordinary nucleus two
kinds of "chromatin": idiochromatin, concerned in reproduction; and
trophochromatin, concerned in nutrition. The chromidia are granules
of trophochromatin which pass into the cytoplasm where they degenerate
(Hertwig) or play a role in the differentiation of specialized structures
(Goldschmidt). In certain rhizopods they may consist of idiochromatin
and give rise to gamete nuclei. It was further suggested that in the
infusoria the micronucleus contains the idiochromatin and the macro-
nucleus the trophochromatin, and that the ordinary nucleus of higher
forms is thus a duplex "amphinucleus." This " binuclearity hypothesis"
has now fallen into disfavor.

Chromidia were described in many animal tissues by other investi-
gators,^° some of whom did not, however, subscribe to the above views
regarding their origin and significance. They were particularly con-
spicuous in oocytes and spermatocytes, where a mass of them developed

34 R. Hertwig (1902, 1904), Goldschmidt (1904 et seq.), Goldschmidt and Popoff
(1907), Popoff (1906 et seq.), Schaudinn (1903), Schaxel (1910 et seq.).

^' Marcus (1907), Wassilief (1907), Reichenow (1908), Nowikoff (1909), Buchner
(1909), Moroff (1909, 1911), M. Jorgensen (1910, 1913), Nussbaum (1913), Hirschler
(1913), van Herwerden (1913).

ATYPICAL MITOSIS AND OTHER NUCLEAR PHENOMENA 195

near the nucleus during the growth period. When special methods for
the study of chondriosomes and Golgi material developed, however, it
became apparent that chondriosomes, chromidia, secretion droplets,
and other ergastic bodies had been hopelessly confused and that many of
the elements which had passed as chromidia were, in reality, chondrio-
somes and other materials for which there was no evidence of nuclear
origin. ^^ Cowdry points out that " ... in practice, under the heading
of chromidia, we have therefore to deal with a variety of substances
which have been hastily grouped together on account of their general
affinity for 'basic' stains and their supposed relation to nuclear chromatin
and for which no special methods of fixation are required. It is a branch
of cytology which has developed almost wholly apart from methods for the
study of living cells."

At present it seems best to reserve the term "chromidia" for the
scattered chromatic matter in Protista with no formed nuclei, and in
other organisms for the small bodies in the cytoplasm which resemble
nuclear matter in composition and chromaticity more closely than do
the chondriosomes and other ergastic substances. The view that chro-
matic granules are transferred bodily through the nuclear membrane has
not been well substantiated, but that a nucleic acid compound passes the
membrane in solution, takes the form of granular "chromidia" as it
reaches the cytoplasm, and is transformed into strands and clumps on
fixation is probable (van Herwerden). Such manifestations of nucleo-
cytoplasmic interchange have been clearly shown in echinoderm eggs,"
although their full significance and their relation to the general problem
of chromidia are not yet apparent. ^^

36Duesberg (1911), Faure-Fremiet (1910), Hirschler (1913), Nussbaum (1913),
Jorgensen (1913c), E. V. Cowdry (1924a). The chromidia of Adinosphcerium are
ergastic, according to Rumjantzew and Wermel (1925).

^ Danchakoff (1916), Tennent (1920).

^ See further on the subject of chromidia Kofoid (1921), Agar (1920a), E. V. Cow-
dry (1924a), and Wilson (1925, p. 700).

CHAPTER XIV

GAMETOGENESIS AND SPOROGENESIS

In plants there are two principal kinds of specialized reproductive
cells: spores, which develop singly, and gametes, which undergo sexual
fusion and form a zygote, this in turn developing into a new individual.
As already pointed out (p. 122), gametogenesis and sporogenesis are
commonly associated with the alternation of two generations in the life
cycle of plants, the gametophyte producing gametes and the sporophyte
spores. In some of the thallophytes, however, both spores and gametes
may be produced rather freely by the same individual, no clear alternation
of generations being present. ^ In the higher animals there are reproduc-
tive cells of but one principal kind, namely, the gametes.

The present chapter deals with a few sample cases from among the
many diverse types of reproductive phenomena exhibited by different
organisms. Discussion of the actual fusion of the gametes and of the
behavior of chromosomes in sporogenesis is deferred to the following two
chapters.

Algae. — The two gametes which fuse sexually may be morphologically
similar or dissimilar, and motile or non-motile. In Ulothrix and Ecio-
carpus they are similar and motile, the two cilia of each gamete being
equal and terminal in the former but unequal and lateral in the latter
(Fig. 138, A, B). In Spirogyra the gametes are but little-modified vege-
tative cells with no special motile apparatus aside from contractile
vacuoles (p. 228).

Examples of unlike male and female gametes are afforded by (Edo-
gonium, Fucus, Vaucheria, and Polysiphonia. In no two of these genera
are the male gametes of the same morphological type. In (Edogonium
certain small cells of the filament produce two ovoid, green spermatozoids,
each with a ring of cilia around one end, while other cells enlarge and
become eggs (Fig. 138, C). The egg contains plastids and reserve food
materials, while a more or less clear "receptive spot" may often be made
out at the point where the spermatozoid is to enter. In Fucus the pri-

1 For general accounts of the life cycles of plants, see general textbooks of botany,
especially Holman and Robbins (1928), Smith, Overton et al. (1928), Gager (1926),
Robbins and Rickett (1929), and Fitting, Sierp, Harder, and Karsten (1930). For
algae, see Oltmanns (1922-1923), Bonnet (1914), West (1927), and G. M. Smith
(1933); for fungi, Gaumann-Dodge (1928) and Fitzpatrick (1930); for seed plants,
Coulter and Chamberlain (1903, 1910). For the cytology of bryophytes, see Motte
(1932) and Hoefer (1932).

196

GAMETOGENESIS AND SPOROGENESIS

197

mary nucleus of the antheridium initiates a series of mitoses giving rise
to a large number of nuclei. About each of these is organized a laterally
biciliate spermatozoid. In the oogonium the primary nucleus initiates
a series of three mitoses, the protoplasm then subdividing to form eight
large eggs. In related genera only four, two, or one egg may be produced,
the remaining nuclei degenerating. ^ In Vaucheria, which is coenocytic,
many colorless, elongated spermatozoids with two cilia near one end are
organized about the nuclei in the antheridium. In the maturing oogo-

l''^'a"

Fig. 114. — Gametogenesis and syngamy in Vaucheria sessilis. A-C, differentiation of
spermatozoids in coenocytic antheridium. D, early stage in development of oogonium.
E, mature egg with one nucleus and many plastids. F, gametic nuclei uniting in egg c,
chloroplast; n, nucleus; r, receptive papilla; s, spermatozoids. {After Oltmanns, 1895.)

nium all but one of the many nuclei retreat to the main thread in a mass
of " Wanderplasm " or degenerate, that one remaining as the nucleus of
the single large egg^ (Fig. 114), In Polysiphonia, non-motile male
gametes, or spermatia, are budded off successively from the antheridial
cell, each of them being supplied with a nucleus formed by a division of
the antheridial nucleus. The female nucleus lies in the enlarged base
of the carpogonium, a cell which elongates to form a receptive trichogyne
above.

The most characteristic spores in algae are the zoospores, which swim
about actively by means of cilia. Except for their larger size they
resemble the male gametes of their respective genera, being terminally

^ For recent accounts, see Tahara (1927, 1929).

3 Oltmanns (1895), Heidinger (1908), and Couch (19326) report retreat; B. M.
Davis (1904), M. Williams (1926), and Mundie (1929) report degeneration.

198

INTRODUCTION TO CYTOLOGY

biciliate in Ulothrix, laterally biciliate in Ectocarpus, and crowned with a
ring of many cilia in (Edogonium. Non-motile spores (aplanospores)
also occur in some genera. In Polysiphonia, carpospores are budded off
from the carpogonium and tetraspores are formed in groups of four in
the tetrasporangium. In some algae, notably Spirogyra and its relatives,
the product of gametic fusion is a resting zygospore.

The cytological phenomena appear to be about the same in the devel-
opment of motile gametes and spores of a given type. The protoplasm
of the antheridium or the sporangium, as the case may be, is often not
entirely used up in the formation of the spermatozoids or zoospores.
The chromatophores, if large and continuous, ordinarily break up into
numerous smaller ones, while the pyrenoids and starch tend to disappear
as the gamete or spore primordia are delimited. In each primordium

I 'I I iinrrrrnfTiriniroriiirTrTrn ij II ^ miiii i,i ^^

'^i:.-'

liiii ii['inriiTrfl-^-

FiG. 115. — Development of blepharoplast in (Edogonium. (After Kretschmer, 1930.)

there are differentiated an eyespot and a motor apparatus, the latter
consisting of a blepharoplast with its attached cilia.

The development of the blepharoplast, or cilia-bearing organ, has
attracted much attention in these and other organisms. In CEdogonium
(Fig. 115) the nucleus moves against the cell membrane, which there
forms a convex thickening. In the plane of contact there appears a
ring of granules. As the nucleus loses contact with the thickening the
ring becomes double, and from its outer half a crown of cilia grows out,*
Each of the many pairs of cilia on the coenocytic Vaucheria swarm spore
is in some way associated with a nucleus lying near the cell membrane.
In Eudorina the pointed end of the nucleus, to which a centriole is
attached, touches the membrane and then retreats to the center of the
cell, leaving behind a double body (centrioles?) from which the cilia grow
out (Hartmann, 1921). Such blepharoplasts as that of CEdogonium are
called " plasmodermal blepharoplasts" to distinguish them from the
"centrosomal blepharoplasts" of pteridophytes, bryophytes, and some
of the lower forms.

* Strasburger (1892, 1900a), Kretschmer (1930).

GAMETOGENESIS AND SPOROGENESIS

199

The mature spermatozoids of the algae are usually described as having
a considerable amount of cytoplasm, but evidently this is not always
the case. In Fucus serratus the figures of Guignard (1889) and Kylin
(1916) represent the cytoplasm as equaling or exceeding the nucleus in
volume, whereas in 7^. Areschougii Kylin (1920) has shown that the main
portion of the spermatozoid is nuclear, the cytoplasm being very small in
amount (Fig. 116, yl). At one side is the eyespot, which is derived from
the chromatophore of the antheridial cell through an intermediate color-

FiG. 116. — Spermatozoids of plants. A, Fucus Areschougii; b, blepharoplast; c,
chromatophore; 7i, nucleus; p, plastomere. (After Kylin, 1920.) B, Chara. (After
Belajeff.) C, QiJdogonium. D., Zamia. (After Webber.) E, Onoclea. (After Steil,
1918a.) F, Riccardia. (After Steil, 1923.) G, Marsilia; spermatozoid extended as it
enters gelatinous material about the archegonium. (After Sharp, 1914.)

less stage. Connected with it is the blepharoplast, which arises from the
centrioles, according to Meves (1918c). Farther back are one or more
"plastomeres," which appear to be chondriosomal in nature.

Fungi. — In their reproductive processes the fungi show many interest-
ing parallels with the algae, at least among the largely coenocytic phy-
comycetes. In Synchytrium the zoospores and gametes are uniciliate,
the gametes being morphologically alike. In Allomyces javanicus the
gametes are unlike in size. In Monoblepharis the zoospores are uniciliate
also, while the gametes are differentiated into large eggs borne in oogonia
and small uniciliate sperms. In the other oomycetes^ the male element is

6 Trow (1895-1904), Wager (1896, 19006), F. L. Stevens (1901), B. M. Davis
(1900, 1903, 19055), Miyake (1901), P. Claussen (1908), Murphy (1918), P. M. Patter-
son (1927a), Nishimura (1926), Carlson (1929), G. O. Cooper (1929a6), Couch (1932a).

200

INTRODUCTION TO CYTOLOGY

represented by the uninucleate or multinucleate contents of the anther-
idium, some or all of which is discharged into the oogonium through a
copulating tube. In Albugo Candida and Pyihium Debaryanum all but
one of the nuclei originally present in the young oogonium retreat to the
periplasm, which becomes sharply set off from the central ooplasm with
the single functional nucleus (Fig. 117). A dense cytoplasmic mass
known as the "ccenocentrum" may appear about the nucleus or in its
vicinity. In Saprolegnia the multinucleate protoplasm of the oogonium
becomes divided up by one or more vacuoles into several eggs, each of
which is at first multinucleate and finally uninucleate. In Mucor
and the other zygomycetes the multinucleate contents of two gametangia
behave as gametes.

Fig. 117. — Gametogenesis and syngamy in Pythium Debaryanum. 1, formation of
oogonium at end of hypha. 2, oogonium and antheridium in contact. 3, egg mature;
degenerating nuclei in periplasm; antheridium above, with one functional and several
non-functional nuclei. 4> sexual nuclei in contact. {After Miyake, 1901.)

The zoospores and motile male gametes in the phycomycetes are
formed by the subdivision of multinucleate protplasm. In Saprolegnia,
for example, the protoplasm in the swollen tip of a hypha rounds up into
uninucleate portions by an extension of the vacuole system. These units
become terminally biciliate zoospores. At a later stage of the cycle,
Saprolegnia produces also reniform, laterally biciliate zoospores. Con-
nection of the cilia with a granule (centrosome?) at the apex of a top-
shaped central body in the nucleus has been described for Leptolegnia
(A. C. Mathews, 1932).

In the large sporangia of the zygomycetes the non-motile spores are
formed by a progressive furrowing of the multinucleate mass, as already
described (p. 165).

The formation of spores exogenously is illustrated by conidia and
basidiospores. The former are cut off successively by constriction from
the ends of certain hyphae, each of them receiving one or more nuclei
derived by division from the nuclei of these hyphae. The basidiospores
are budded off in quartets from the basidium, whose nucleus by two

GAMETOGENESIS AND SPOROGENESIS

201

divisions provides them with one nucleus each (Fig, 164). Development
of spores by free cell formation occurs in the ascomycetes. After the
primary ascus nucleus has divided to eight, a portion of the ascus cyto-
plasm is cut out about each of these nuclei, the astral rays curving around
from the centrosome having some part in the process (p. 158). Finally,
resting spores are often formed as a result of a sexual fusion. Examples
of this are the zygospore of Mucor and the oospore of Albugo.

Bryophytes. — In bryophytes, which show a well-marked alternation
of generations, the eggs and spermatozoids are borne by the gametophyte
in archegonia and antheridia, respectively. The egg
is the innermost cell of the axial row in the arche-
gonium (Fig. 118). Commonly it enlarges, rounds
up, and lies more or less free in the slimy fluid of the
venter, the other axial cells meanwhile breaking
down. In some genera (Anthoceros, Sphagnum) the
ventral canal cell also is sometimes organized as a
functional egg, and there are other facts which sug-
gest that the other cells of the axial row were gametes
historically. Besides a large nucleus, the egg may
contain plastid primordia and chrondriosomes. In
mosses Motte (1928) reports that the egg contains
practically no food reserves. In many cases a fairly
distinct hyaline receptive spot is present at the ^j^ ^^g Arc he-
side of the egg directed toward the neck of the gonium of RebouHa,

nrrhpp-nniiim showing egg, ventral

arcnegonmm. ^.^^^^i ^^^j ^^^ ^^^j.

Spermatogenesis has been studied in both liver- neck canal cells.
worts and mosses.^ In Marchantia, according to the '^^ '^^^ '
early account of Ikeno, a minute centrosome comes out of the nucleus
before each spermatogenous cell-division in the antheridium and divides
into two; these pass to opposite sides of the cell and occupy the spindle
poles during mitosis. After the last (diagonal) cell-division the centro-
some passes to one corner of the cell (spermatid) and there elongates
to form the blepharoplast, from which two long cilia grow out (Fig. 119).
Meanwhile the nucleus becomes altered in shape and forms the main por-
tion of the body of the spermatozoid. In the cytoplasm of the spermatid
was seen another chromatic body of uncertain fate. Later accounts of
other liverworts present essentially the same story except that the nuclear
origin of the centrosome, which is usually seen only in the last mitosis,
has not been substantiated. In Blasia the blepharoplast divides into

6 On liverworts: Ikeno (1903), Miyake (19055), C. E. Lewis (1906), Bolleter (1905),
Escoyez (19076), Schaffner (1908), Woodburn (1911, 1913), Sharp (19205), Motte
(1928), Yazawa (1931). On mosses: M. Wilson (1911), Woodburn (1915), C. E. Allen
(1912, 1917a), Bowen (1926/, 19276), Motte (1928), Weier (1930, 19316). See
Miihldorf (1930, 1931) on the mature spermatozoid.

202

INTRODUCTION TO CYTOLOGY

Fig. 119. — Spermatogenesis in Marchantia. h, blepharoplast; c, centrosome; n, nucleus.

{After Ikeno, 1903.)

Fig. 120. — Spermatogenesis in Polytrichum. A-D, mitosis in androgones, showing
appearance of plastid material (k). E-H, behavior of centrosome in last division; each
androcyte (spermatid) has one centrosome, which acts as a blepharoplast {b). I-K,
transformation of androcyte into spermatozoid: a, apical body; I, limosphere; n, nucleus;
p, percnosome. L, mature biciliate spermatozoid. {After C. E. Allen, 1912, 1917a.)

GAMETOGENESIS AND SPOROGENESIS

203

fragments which together form the ciha-bearing rod, as in certain vascular
plants (Sharp, 19206). In the spermatozoids of i^zccardza (Fig. 116, i^),
Pellia, and certain other genera the two cilia spring from different points,^
at which basal granules may be seen.

Recent studies on spermatogenesis in mosses have revealed a remark-
able parallelism between the behavior of cell elements here and that in
animal spermatogenesis. In the multiplying spermatogenous cells
("androgones") of Polytrichum the plastids form one or two masses,

Fig. 121. — Diagram of spermatogenesis in Polytrichum. In 1 the apical body {A) is
separating from the limosphere remnant (L). B, blepharoplast. C, cilia. A'^, nucleus.
{After Weier, 19316.)

which appear after certain fixations like clumps of granules and as large
plates, or, after other procedures, like a series of chromophilic plates in a
chromophobic substance (see p. 80). In each cell generation these
bodies undergo division (Fig. 120). In each cell of the last generation
but one, a centrosome with radiations in the cytoplasm divides into two.
These move apart and occupy the spindle poles during the last mitosis,
which differentiates the spermatids ("androcytes").

In the androcyte the plastid becomes a body known as the limosphere.
It becomes somewhat oblong and buds off a small differentiated portion
from one end; this is the apical hody^ (Fig. 121). Meanwhile the centro-

' Steil (1923), Showalter (1926a), Mlihldorf (1931).

* The limosphere was named by M. Wilson (1911). Allen (1917a) gave the first
adequate description of it, discovered its division to form the apical body, and pointed
out evident references to it in the earlier literature. Its derivation from plastids was
demonstrated by Weier (1930, 19316, 1932), see page 81. The granules and plates
in the earlier spermatogenous cells were called "kinetosomes" and "kinoplasmic
plates" by Allen (1912). Sapehin's (1915) claim that they are plastids was confirmed
by Bowen (19276) and Weier.

204 INTRODUCTION TO CYTOLOGY

some has elongated to form the blepharoplast, and the nucleus has begun
to elongate also. The blepharoplast comes against the apical body at
one end of the nucleus; this is to be the anterior end of the spermatozoid.
The apical body becomes pointed, while the portion of the blepharoplast
lying beside it somehow gives rise to the two long cilia. Meanwhile the
limosphere remnant takes up a position near the posterior end of the
nucleus where it may eventually disappear along with some of the cyto-
plasm. The mature spermatozoid consists of an elongated body repre-
senting chiefly the nucleus, a little cytoplasm, an apical body, and a
motor apparatus consisting of blepharoplast and cilia.

It will be noted that the behavior of the limosphere and apical body
are almost precisely similar to that of the acroblast and acrosome in
animals (p. 220). The acroblast is known to represent the Golgi material
of the animal spermatid; hence the demonstration that the limosphere is
derived from the plastids of earlier cell generations lends strong support
to the view that of all the cell elements in plants the plastids correspond
most closely to the Golgi material of animals (see p. 80).

The spores in bryophytes are borne by the sporophyte, which develops
from the fertilized egg. In the sporangium certain cells known as
sporocytes round up from one another and each of them undergoes two
successive divisions, thus giving rise to a quartet of spores. In some
liverworts the sporocyte becomes markedly four lobed before it divides.
It is in the course of the two mitoses in the sporocyte that the number of
chromosomes is reduced one half. Meanwhile the plastids also are
divided (at least in some cases) and distributed to the four spores (p. 70).
After their walls become fully developed, the spores are freed from the
sporangium and later grow into new gametophytes.

Pteridophytes. — In pteridophytes, as in bryophytes, quartets of
spores with the reduced, or gametic, chromosome number are produced
by the division of sporocytes in the sporangium. Furthermore, the
spores germinate to produce gametophytes, which bear eggs and sperma-
tozoids in archegonia and antheridia. In location and general charac-
teristics the egg is much like that of bryophytes. Often it is somewhat
flattened on the receptive side at the time of syngamy.

The spermatozoids of all pteridophytes, except Ly co-podium, Phylloglos-
sum, and Selaginella, differ from those of bryophytes in being multiciliate.
Most of the accounts of spermatogenesis^ state that the blepharoplasts
appear first either in the spermatids or as centrosomes during the divi-
sion which differentiates these cells. In Equisetum (Fig. 122) it has
been shown that the blepharoplast appears as a functional centrosome

sfiuchtien (1887), Campbell (1887), Belajeff (1888, 1897, 1898, 1899), Guignard
(1889), Schottlander (1893), Shaw (1898a), Thorn (1899), Yamanouchi (19086),
R. F. Allen (1911), Sharp (1912, 19146). See the recent studies on the mature
spermatozoid by Dracinschi (1930, 1931, 1932) and Yuasa (1932, 1933).

GAMETOGENESIS AND SPOROGENESIS

205

in each cell of the penultimate generation; there it divides to two, which
separate and occupy the poles of the achromatic figure in the manner of
animal centrosomes. At the close of mitosis the blepharoplast in each
spermatid fragments into a number of pieces which later join to form a
continuous chromatic thread. The spirally coiled body of the mature
spermatozoid in pteridophytes consists of the elongated nucleus, a
cytoplasmic band lying along the anterior portion of the nucleus and
containing the chromatic thread at its margin, a posterior globule of
cytoplasm containing starch and other inclusions, and numerous cilia.
Students of spermatozoid development have described the cilia as
growing out from the chromatic thread ("blepharoplast"), though

Fig. 122. — Spermatogenesis in Equisetum arvense, showing the behavior of the blepharo-
plast (centrosome) in the last spermatogenous mitosis and in the transformation of the
spermatid into the spermatozoid. {After Sharp, 1912.)

recent observers of mature spermatozoids report that they appear to
be attached to basal bodies in the cytoplasmic band whose margin is
formed by the thread ("border brim") (Dracinschi, Yuasa).

In Marsilia each of the two primary spermatogenous cells undergoes a
series of four divisions which result in 16 spermatids. No distinct centro-
somes appear during the first mitosis. During the anaphase of the second
mitosis centrosomes develop at the spindle poles. In the telophase they
divide but usually then disappear in the cytoplasm. In the third mitosis
centrosomes again appear at the spindle poles during the anaphase, and in
the telophase they divide. The daughter centrosomes so formed then
move apart and occupy the poles of the spindle through the fourth, or
final, mitosis. They are at all times accompanied by distinct cytoplasmic
radiations, the achromatic figure being strikingly like those in animals and
certain thallophytes. Before the last mitosis is completed, the centro-
some (blepharoplast) becomes vacuolate, and in the spermatid it breaks

206

INTRODUCTION TO CYTOLOGY

up into a number of fragments. These later join to form a cilia-bearing
band which elongates spirally in close union with the nucleus to form
the spermatozoid (Sharp, 1914).

Gymnosperms. — In all seed plants, as well as in certain groups of
pteridophytes, spores of two distinct kinds are produced in quartets:
microspores and megaspores.'^^ Such plants are said to be heterosporous,
while those with only one kind of spore quartet are homosporous. In the
gymnosperms the microspore quartets are developed in a manner essen-
tially like that of the quartets of homosporous ferns, i.e., by the subdivi-
sion of isodiametric sporocytes. The sporocyte which develops the

Fig. 123. — OSgenesis in Dioon edule. A, young archegonium. B, egg nucleus below
and ventral canal nucleus above; two conspicuous neck cells. C, protrusions of the egg
cytoplasm (at right) extending as haustoria through pores in the egg membrane into the
surrounding jacket cells (at left). {After Chamberlain, 1906.)

megaspore quartet in the ovule is commonly elongated, and it divides in
such a manner that the spores form a row. The outer three spores
ordinarily degenerate, while the innermost one develops into a female
gametophyte with archegonia.

The eggs of gymnosperms^^ are very large cells, the nucleus alone in
certain cycads being as much as 0.5 millimeter in diameter. The egg is
borne in an imbedded archegonium, which has an evanescent ventral
canal cell or nucleus (Fig. 123). The egg cytoplasm is in close communi-
cation with surrounding nutritive cells of the gametophyte through pits
in the wall. In most cases these pits are said to be closed by a membrane,
the only direct connection being through minute plasmodesms. In
Dioon, however, Chamberlain has shown that the membrane at first

^^ These standard terms imply a size difference, but the essential difference is one
of sexual tendency; androspore and gijnospore would be more appropriate. "Mega-
spores" are sometimes smaller than "microspores."

11 Goroschankin (1883), Ikeno (1898), Chamberlain (1899, 1906, 1910, 1912, 1916),
I. Smith (1904), Ferguson (1904), Stopes and Fujii (1906), Eames (1913), P. Sedgwick
(1924), Lawson (1907, 1909, 1926), G. Nichols (1910), Shimamura (1928, 1929),
Sm61ska (1927), Wakayama (1929), W6ycicki (1923a6), Herzfeld (1927).

GAMETOGENESIS AND SPOROGENESIS

207

separating the projecting egg haustoriiim eventually ruptures, the
cytoplasm of the egg and nutritive cells then becoming continuous. In
the cycads the egg cytoplasm appears relatively free from conspicuous
nutritive inclusions, but in conifers, such as Pinus and Agathis, there
are often large masses of stainable ergastic material and other substances
of uncertain origin and composition. The nucleus of the gymnosperm
egg resembles that of certain animal eggs in containing an unusually large
amount of material not incorporated in the chromosomes at the time of
mitosis.

D U- . . ^v' . ^Islisjife^j^G^

B

Fig. 124. — Stages in spermatogenesis in Dioon edule. A, "body-cell" with black
granules in cytoplasm. B, two blepharoplasts differentiated. C, body-cell with two
blepharoplasts; prothallial and stalk cells below; all in end of pollen tube. D, fragmenta-
tion of blepharoplast in spermatid as spiral band begins to form. E, portion of edge of
section of spermatozoid (cf. Fig. 116, D) showing spiral blepharoplast cut at two points and
cilia growing from it. {After Chamberlain, 1909.)

In the gymnosperms there are two principal types of spermatogenesis,
some of the orders (Cycadales, Ginkgoales) having ciliated spermato-
zoids^- and the others (Coniferales, Gnetales) non-motile male cells.
In most cycads and Ginkgo a greatly enlarged "body-cell" in the devel-
oping pollen tube gives rise to two spermatozoids. In Dioon, for example
(Fig. 124), numerous "black granules'' appear in the body-cell cytoplasm.
Two blepharoplasts now develop, apparently by the enlargement of two
of the black granules, and take up positions on opposite sides of the
nucleus. Very conspicuous radiations^^ appear about them as the
body-cell divides. The mitotic figure is wholly intranuclear, and,
although the blepharoplasts remain opposite its poles, they appear to
have no direct connections with it. A wall appears between the two
daughter nuclei at the close of mitosis; in each of the resulting cells a

12 Hirase (1894), Ikeno (1898), Fujii (1898, 1899), Webber (1897, 1901), Caldwell
(1907), Miyake (1906), Chamberlain (1909, 1916), Kuwada and Maeda (1929).

13 Hirase (1894), Fujii (1899), and Kuwada and Maeda (1929) report that these
are invisible in living cells.

208

INTRODUCTION TO CYTOLOGY

spermatozoid is organized. Even before the division of the body-cell
nucleus the enlarging blepharoplasts become vacuolate. After the
division is completed, each of them breaks up into a number of small
fragments which then coalesce and begin the formation of the spirally-
coiled band that bears the many cilia. This band-like blepharoplast
continues to elongate just within the cell membrane until it has made
several turns, a prolongation of the nucleus remaining in contact with its
growing end. The mature spermatozoid consists of an enormous
nucleus, which in the living condition can be seen to undergo amoeboid
changes of shape, a cytoplasmic sheath, and the blepharoplast with its
ciha.

Fig. 125. — Microsporogenesis and development of male gametophyte in an angiosperm.
First row: two meiotic mitoses in microsporocyte, followed by cleavage of protoplast into
four microspores, three of which are shown. Second row: formation of male gametophyte
by one microspore, t, tube cell; g, generative cell; cT, male gametes; i, in tine; e, exine;
p, germ pore with plug. Semidiagrammatic.

In the conifers, as in the cycads, the body-cell divides to form two
male gametes, but here they are non-motile. In some genera (Taxodium)
a wall separates the two nuclei after mitosis in the body-cell, but in others
(Pinus) these nuclei lie together in the body-cell cytoplasm. As the
body-cell moves down the pollen tube its outlines may remain distinct,
but in some cases its cytoplasm becomes intermingled with that of the
pollen tube. In the latter event the male gametes are simply nuclei,
rather than complete cells. In some genera the two male gametes are
differentiated in size and apparently in function, a tendency which
reaches its fullest expression in the Podocarpinese.

The theory that the blepharoplasts of bryophytes and vascular plants
are homologous with centrosomes^^ was at one time much disputed, but
its validity is now generally conceded. A survey of the known cases
suggests that centrosomes originally functioning in the ordinary way
through several mitoses have tended to become restricted to one, and
" Belajeff (1897), Ikeno (1898 et seq.). See the review by Sharp (1912).

GAMETOGENESIS AND SPOROGENESIS

209

that their original role has grown less evident as they have been modified
in connection with their other function, namely, the bearing of cilia. In
forms with non-motile gametes they do not appear.

Angiosperms. — In its essential features sporogenesis in angiosperms
is like that in gymnosperms. In the anther the microsporocytes, usually
as they lie in the anther fluid after rounding up, undergo two divisions to
form quartets of microspores (Fig. 125). In some cases a separating wall
is formed after the first mitosis, but more commonly cytokinesis does not
occur until after the second mitosis, when the cell is divided simultane-

—.- 'y^-s^-i'

B

i:s^

;^,:::^

Fig. 126. — Development of male gametes in angiosperm pollen tube. A-D, division of
generative nucleus and delimitation of male cells in Galanthus nivalis. E, male cells in
Hemerocallis flava. The vegetative pollen-tube nucleus (p) may either precede or follow
the generative nucleus through the tube. {After Trankowsky, 19306.)

ously by furrows or otherwise into the four spores (p. 167). Each micro-
spore develops a thick wall and soon forms a very simple male gametophyte.
The microspore nucleus, which has the reduced number of chromosomes,
divides to two, around one of which a membrane cuts out a generative cell.
The other nucleus and the rest of the microspore cytoplasm constitute
the tube cell, which later grows out to form the pollen tube.

The generative cell divides to form two male gametes. This division
sometimes occurs in the pollen grain before it is liberated from the anther,
but probably more often it takes place in the growing pollen tube after

210 INTRODUCTION TO CYTOLOGY

pollination^^ (Fig. 126). It has been shown in many cases^'' that the male
gametes are complete cells, at least while they are in the pollen grain or
tube, and sometimes until they reach the embryo sac (p. 236) ; but it is
also reported ^^ that their membranes sometimes disappear early, leaving
the male nuclei free in the cytoplasm of the pollen grain or tube. The
male nuclei in many species become vermiform, particularly after entering
the embryo sac'^ (Fig. 144). This change may occur more rapidly in one
nucleus than in the other, the two thus being unlike at late stages. It is
questionable whether or not such nuclei have any power of movement
aside from that occasioned by protoplasmic streaming and surface-
tension phenomena.

In the ovule a megasporocyte is developed by the enlargement of a sub-
epidermal cell of the nucellus (Fig. 127). At the close of the first mitosis
a wall is formed between the nuclei, and the two resulting cells (secondary
megasporocytes) divide again, giving thus four megaspores. (In some
cases the outer secondary megasporocyte does not divide.) The outer
megaspores disintegrate, while the innermost one enlarges and develops
the female gametophyte. Its nucleus, which has the reduced number of
chromosomes, initiates a series of three divisions which result in eight
nuclei. Ordinarily four of these lie near each end of the elongated embryo
sac." In the micropylar end membranes are differentiated in the cyto-
plasm about three of the nuclei, forming an egg and two synergids,
while in the opposite end three antipodal cells are similarly formed.
The two remaining free polar nuclei move together and fuse sooner or
later. The angiosperm egg usually shows very little special morphological
differentiation, and except for its size and the position of its nucleus and

1^ This constitutes a systematic character of some value (Schiirhoff, 1926, p. 260);
see this work for a review of the cytology of angiosperms. W6ycicki (19266) attrib-
utes the movement of the generative cell into the pollen tube to the action of vacuoles.

i« E.g., Ishikawa (1918) on (Enothera; Wyhe (1923) on Vallisneria; Piech (19246,
1928) and Kostrioukoff (1930) on Scirpus; Trankowsky (19306) on Hemerocallis;
Madge (1929) on Viola; Finn (1925, 1926a, 1928) on Asclepias, Vincetoxicum, and
Vinca; and Finn and Rudenko (1930) on Orohanche.

^' E.g., Dahlgren (1916) on Primula; Trankowsky (1930) on Convallaria and
Galanthus; Schiirhoff (19196) on Sambucus; and Poddubnaja (1927) on Echinops.

'^E.g., Mottier (1898a), S. Nawaschin (1899, 1900, 1909, 1910), Land (1900),
Guignard (1900), Blackman and Welsford (1913), Welsford (1914), Sax (1916, 1918),
and Heimans (1928).

Fig. 127. — Megasporogenesis, development of female gametophyte, syngamy, and
early embryogeny in an angiosperm. 1-5, division of megasporocyte into linear quartet of
megaspores; meiosis occurs in these two mitoses. 6-12, development of female gameto-
phyte by innermost megaspore, this involving three mitoses. In 13 the largest cell in the
upper end of the embryo sac is the egg, and two polar nuclei are in the center. 13, discharge
of two male nuclei into embryo sac by pollen tube. 14, double fertilization, one male
nucleus fusing with egg nucleus and the other with polar nuclei. 15, embryo in two-cell
stage; endosperm in ccenocytic stage. 16, embryo has developed cotyledons, and endo-
sperm has become cellular. Semidiagrammatic.

GAMETOGENESIS AND SPOROGENESIS

211

Fig. 127.— See p. 210 for legend.

212 INTRODUCTION TO CYTOLOGY

vacuoles it closely resembles the synergids; in fact, cases are known in
which synergids as well as eggs may develop into embryos. Commonly
the egg is somewhat larger than the other cells, has its nucleus in the end
toward the center of the sac, and has one or more large vacuoles. Visible
ergastic materials other than cell sap are usually not conspicuous, but
chondriosomes and plastid primordia are probably present regularly.

Many variations of the process just described have been found in the
angiosperms.^^ Probably the commonest of these is that exemplified in
Lilium: here no walls are formed after either of the two mitoses in the
megasporocyte, the four nuclei lying free in the cytoplasm of the embryo
sac where they undergo one further mitosis to form a typical eight-
nucleate gametophyte (Sargant, 1896). The egg, therefore, is removed
from the product of meiosis by a single mitosis, instead of by three mitoses
as in the usual type of development.

A condition intermediate between this and the usual one is seen in
Smilacina, where the walls form and then disappear, leaving the four
nuclei to divide to eight (McAllister, 1909). Of exceptional interest is the
situation in Plumbagella micrantha, described by Dahlgren (1915). Here
the four nuclei, formed free as in Lilium, divide no further : one of them
becomes directly the nucleus of the egg, two of them fuse like polar
nuclei, and the fourth disintegrates in the base of the sac. This is the
only known case among higher plants in which the gamete nucleus is the
immediate product of meiosis, as in animals.

In several known instances the embryo sac is developed neither from a
single megaspore as in the usual type, nor directly from the primary
megasporocyte as in Lilium and Plumbagella, but from one of the second-
ary megasporocytes. In Cypripedium, for example, the nucleus of this
cell undergoes the second meiotic mitosis, after which another mitosis
occurs, giving four nuclei, one of which becomes the nucleus of the egg
(Pace, 1907). Embryo sacs with more than eight nuclei have also been
found. In Peperomia hispidula no walls are formed after the meiotic
mitoses, the four nuclei dividing twice in succession to give 16. An egg
and one synergid are organized, and the remaining 14 nuclei fuse (D. S.
Johnson, 1907). The attention of the geneticist may be called to the fact
that when all of the embryo-sac nuclei arise from one of the four products
of meiosis in a heterozygous plant, they may be assumed to be of the same
genetic constitution; but when they are derived from more than one, as in
several of the examples cited above, they may differ greatly, so that very
unusual correlations between the characters of the sporophyte and those
of the endosperm may be expected. In several instances two or more of
the described modes of development are known to occur in the same
family and even in the same individual.

'° For the types of embryo sac development, see Rutgers (1923), Stenar (1925),
Schurhoff (1926), Chiarugi (1927), Schnarf (1929), and Modilewski (1929).

GAMETOGENESIS AND SPOROGENESIS

213

Oogenesis in Animals. — The development of the animal egg varies
considerably in detail in the different groups. The general features of the
process as it occurs in typical cases may be briefly sketched as follows. ^°
In the ovary certain cells known as oogonia enlarge somewhat and become
primary oocytes. When first distinguishable the oocyte is relatively
undifferentiated, but it soon passes through a growth period during which
it enlarges greatly and becomes supplied with one or more kinds of yolk
(Fig. 128). A role in the elaboration of these products has been assigned
to the chondriosomes and Golgi material by a number of investigators
(pp. 78 to 88). In some animals the changes during the growth period

Fig. 128. — Differentiation of oocyte in Hydra. A, very young oocyte between ecto-
dermal cells at right. B, oocyte after growth period, with yolk globules. {After Downing,
1909.)

involve the activity of a special follicular epithelium organized about the
oocyte, or a group of "nurse cells." The oocyte at this stage is often
called the "ovarian egg" and its large nucleus the "germinal vesicle."

At the close of the growth period the oocyte nucleus, which is already
in an advanced stage of the prophase, undergoes division near the cell
membrane. One of the daughter nuclei so formed is included in the first
polocyte, or "polar body," a small cell cut off at this point (Fig. 154).
The nucleus remaining in the large cell, now called the secondary oocyte,
quickly undergoes another division, one of the resulting nuclei being
included in a second polocyte, or "polar body," while the other remains in
the now mature ovum, or egg. The first polocyte may divide and thus
complete a quartet of cells, but often this does not occur. Normally the
polocytes are functionless and soon degenerate, sometimes within the

20 See Hegner (19146), Wilson (1925), and Corner (1932). The question of the
origin of the germ cells is reviewed by Harms (1926) and Heys (1931).

214

INTRODUCTION TO CYTOLOGY

egg. The two mitoses in the oocyte are meiotic in character and result in
a reduction from the zygotic to the gametic number of chromosomes.
They are frequently called "maturation divisions."

From the foregoing it is evident that the animal ovum develops most
of the features characterizing it as a gamete before the meiotic divisions
take place. It will be seen later (p. 239) that in some cases the sper-
matozoon enters the egg before these divisions are completed. It is a
further significant fact that in many animals the differentiation of visibly
distinct cytoplasmic regions having a relation to parts of the future

*^

'V

A..

r

*.>■

I- } «;

■..y

I

Fig. 129. — First division of spermatocyte of Euschistus, showing behavior of chondrio-
somes (first row) and Golgi material (second row), ch, chromosomes. {After Bowen,
1920.)

embryo may begin in the oocyte or ovum before the entrance of the
spermatozoon; in other words, embryogeny may actually begin before
fertilization (p. 419).

The ovum is surrounded by a delicate vitelline membrane, which
becomes conspicuous only after fertilization, a thicker layer often showing
radial structure (vertebrates) and sometimes a third layer of structureless
jelly. The surrounding cells may add certain secondary layers, and later
there may be deposited one or more protective envelopes, such as the
albumen, shell membrane, and shell of the bird's egg.

Spermatogenesis in Animals. — In the male animal those cells (sperma-
togonia) in the testis whose ultimate descendants are to become sperma-
tozoa multiply by divisions of the ordinary type until a certain number are
produced. These cells, now called primary spermatocytes, enlarge and

GAMETOGENESIS AND SPOROGENESIS 215

undergo two successive divisions: the first division results in two cells
called secondary spermatocytes; the second divides the two secondary
spermatocytes into four spermatids, each of which then becomes trans-
formed into a spermatozoon. The mitoses in the spermatocyte are meiotic
in character and bring about a reduction in the chromosome number.
Besides the spermatogenous cells, the testis also contains certain accessory
cells, such as the Sertoli cells of mammals and Verson's cells of certain
insects.

The transformation of the spermatid into a spermatozoon (spermio-
genesis) has long been one of the most fascinating and difficult problems
in structural cytology. The several components of the cell undergo an
astonishingly complicated series of transformations, and these, together
with the types of spermatozoa resulting, differ considerably in detail from
group to group. This has naturally led to much confusion in the literature
on the subject, although many points were well covered by the early
investigations. The outstanding researches of Bowen (1920-1926) have
so clarified our conceptions that his descriptions will be used as the princi-
pal basis of the following account. Bowen worked chiefly with insects
(Hemiptera, Orthoptera, Lepidoptera, Coleoptera, Aptera) and amphibia
(Plethodon), but comparisons show that his descriptions, with minor
modifications, will apply to the general features of spermatogenesis in
various other groups. -"^

The Spermatocyte and Its Divisions (Fig. 129). — In the spermatocyte
are the following components: nucleus, cytoplasm, chondriosomes, Golgi
material, a pair (usually) of centrioles, and frequently other formed ele-
ments of questionable nature. The chondriosomes are present in the
form of granules, rods, or threads, and, although these behave variously
in different species, they are usually distributed rather equally to the four
spermatids in the two divisions. This in some cases involves the passive
division of individual chondriosomal threads or an even more precise
distribution (p. 86). The centrioles diverge to opposite sides of the cell
and occupy the poles of the achromatic figure in each mitosis. At the
close of the second mitosis the centriole usually divides, so that the sper-
matid has a pair of them. Much confusion in terminology and diversity of
interpretation have arisen concerning the special differentiations which
may occur about the centrioles and the topographic relation which certain
other cell components, notably the Golgi material, may bear to them.

Two general modes of arrangement of Golgi material in spermatocytes
may be distinguished. In the insects (Bowen) a number of Golgi bodies,

^1 For further general accounts of animal spermatogenesis, see Wilson (1925),
Metz (1932), and the resume by Bowen (1924c). See the extensive researches of
Gatenby (1917 et seq.). Other recent works are those of Voinov (1925, 1927a6), Nath
(1925), Chickering (1927), Sokolow (1926, 1929a6), Payne (1927), Hirschler (1928),
Pollister (1930), and H. H. Johnson (1931).

216

INTRODUCTION TO CYTOLOGY

each composed of two substances differing in chromaticity, are scattered
throughout the cytoplasm. At each of the meiotic divisions they break
up into fragments (dictyosomes) which become arranged around the
nucleus at the equator of the cell and pass as equal groups to the two poles
in advance of the chromosomes. In Gerris Pollister finds that only the
osmiophilic substance forms the dictyosomes, the osmiophobic (and

Fig. 130. — Diagram illustrating principal features of spermiogenesis in animals, a,
acrosome; c, centrioles; g, Golgi material (acrobiast) ; N, nucleus; n, nebenkern; p, perfora-
torium. {Based on diagrams and other figures of Bowen.)

neutral-red staining) substance remaining behind. In another series of
forms (mollusks, amphibia, other vertebrates) the Golgi bodies are closely
aggregated about the centrioles where their lightly staining substance
flows together to form the idiosome, to the surface of which their deeply
staining constituent adheres as separate chromophilic rodlets. This
chromophilic matter often appears as a network or a continuous shell
instead of separate rodlets, but it is uncertain how far such appearances
are due to the action of fixatives. It was formerly thought that the idio-
some substance was related primarily to the centrioles, the Golgi materia]

GAMETOGENESIS AND SPOROGENESIS

217

collecting about it at certain stages, but the situation in insects seems to
show that the real unit is the Golgi body composed of chromophilic
"Golgi matter" and relatively chromophobic "idiosome substance,"
a close topographic relation to the centrioles being assumed only in
certain cases. During the meiotic divisions of the nucleus the Golgi
rodlets (or network or shell) form a number of dictyosomes which pass as
two groups to the poles; whether each divides or not is a question. The
fate of the idiosome substance is difficult to determine, but it is probable
that each dictyosome is a minute Golgi body with its two substances,
which are thus distributed to the four
spermatids.

Each spermatid consists of cytoplasm,
a nucleus with the gametic number of chro-
mosomes, some chondriosomes, a pair of
centrioles, a number (usually) of Golgi
bodies, and often ergastic inclusions.
These various elements will now be followed
through the metamorphosis of the spermatid
into a spermatozoon (Figs. 130 to 134).

Centrioles. — In the Hemiptera the two
centrioles are situated near the anterior
end of the young spermatid, one of them
lying in contact with the nuclear membrane.
From the distal member of the pair the
delicate axial filament of the flagellum
grows out and pierces the cell membrane.
In many insects this filament may appear in spermiogenesis in Piethodon dn-

1 I- IP -i. • • IX ereus. (After Bowen, 1922a.)

much earlier, before mitosis is complete or

even in the primary spermatocyte (moths). The centrioles now
migrate to a position near the posterior pole of the nucleus, where
they take the form of parallel rods lying against the nuclear membrane,
and soon form a V, with the elongating axial filament extending from its
angle. An intranuclear body ("pseudoblepharoplast") present during
these stages has often been confused with the centrioles. The centrioles
eventually constitute the so-called "centrosomal middle piece" at the base
of the sperm head, but in insects this is not a very distinct structure.

The centrioles in certain other animals show curious modifications
into rings and knob-like structures which have been variously interpreted
(Fig. 131). In his accounts of spermatogenesis in the salamander Meves
(1896, 1897) reported that the distal centriole, after the appearance of the
axial filament, transforms itself into a ring. The filament then passes
through this ring and attaches itself to the proximal centriole, which
pushes into the base of the nucleus and enlarges to form the middle piece.
Meanwhile the ring divides into two parts, one of which becomes the

Fig. 131. — Behavior of centrioles

218

INTRODUCTION TO CYTOLOGY

"end-knob" at the posterior end of the middle piece, while the other passes
backward along the axial filament. In mammals (rat, man) Meves
(1898, 1899) found much the same situation: the proximal centriole
remains near the nucleus and does not elongate to form a middle piece.
The distal centriole then divides, one part forming the end-knob and the
other passing back as a ring to the end of the "connecting piece" (which
does not correspond to the middle piece of the salamander). In (Ecanthus
nigricornis, a cricket, the distal centriole, to which the axial filament is
attached, constricts off a portion which encircles the filament and works
backward along it to the end of the tail sheath (H. Johnson, 1922, 1931).

WSSm^

Fig. 132. — Transformation of nebenkern in Brochymena. {After Bowen, 1922cd.)

Chondriosomes. — In insects generally the chondriosomes form a single
more or less compact body, the nebenkern (the mitosome of Gatenby)
(Fig. 132). Globules of a lightly staining fluid appear in the nebenkern,
chiefly near its periphery, giving the "blackberry stage" reported after
certain fixatives. Soon the more deeply staining portion takes the form
of a series of concentric plates alternating with layers of the lighter sub-
stance (the "onion stage"). The platework now becomes a hollow ovoid
mass with a median partition. As the nebenkern elongates, the ovoid
mass shrinks; as it does so, a furrow follows it inward and eventually
cuts the nebenkern in two as the chromatic mass vanishes. Meanwhile
globules of an additional "central substance" appear in the light neben-
kern material, arrange themselves in rows, and coalesce to form beaded
strands. As the nebenkern halves elongate further, these strands
unite until each half finally has a single axial core composed of the central
substance.

GAMETOGENESIS AND SPOROGENESIS

219

The nebenkern halves now come to lie on either side of the axial
filament and rapidly elongate to form the two "filament sheaths" which
become twisted about the axial filament. Their anterior ends appear to
attach themselves to the centrioles at the base of the nucleus. As they
become longer and thinner they show a series of swellings which may
possibly represent accumulations of the central substance. These even-
tually disappear and the uniform sheaths extend nearly, if not quite, to
the tip of the axial filament.

ff

J

B

M^^ I

G - H ^-^ I

Fig. 133. — Behavior of Golgi material in spermatids of certain insects. A, F, Brochymena;
B-E, Euschistus; G-J, Murgantia. Cf. Fig. 130. {After Bowen, 1920, 1922c.)

Golgi Material (Fig. 133). — In the Hemiptera the Golgi constituents

of the spermatid usually behave as follows. At the close of the meiotic

divisions the dictyosomes fuse to form several larger Golgi bodies much

like those of the spermatocyte. The fusion continues until there is

formed a single large acroblast,'^'^ which lies near the base of the nucleus

on the side opposite that to which the centrioles migrate. Ordinarily it

has a heavily staining shell except on the side next to the nucleus. The

acroblast soon begins a migration around to the other side of the nucleus,

passing first to the anterior end of the cell where it pauses for a time. It

^- Often referred to in the literature as the "spermatid idiosome," or "sphere." In
moUusks this mass has frequently been called the "nebenkern."

220 INTRODUCTION TO CYTOLOGY

then continues along the nuclear membrane on the other side, following
the path of the centrioles, and eventually comes to lie near them.

During the migration of the acroblast an acrosome is differentiated
from it. This first appears as a delicate vesicle on the side of the acro-
blast near to the nucleus and seems to consist of a new material, the
formation of which is dependent upon the activity of the substance of the
acroblast.-^ Within it is a small granule. Very rarely the acrosome
itself has the form of a granule rather than a vesicle (mollusks, Gatenby ;
grasshopper. Bo wen). The acroblast becomes somewhat smaller as the
acrosome grows, and together they move again toward the anterior end
of the cell. Either before or after reaching the apex they separate, the
acrosome taking its final position near the apex while the remainder of
the acroblast, known as the "Golgi remnant," passes backward along the
tail and is ultimately cast out of the cell in a protoplasmic ball sloughed
off at the close of spermiogenesis.^^

The acrosome, after reaching its definitive position near the anterior
end, undergoes a further differentiation. Within it appears a deeply
staining mass which may possibly bear some relation to the granule
observed in the vesicular acrosome at earlier stages. It rapidly develops
into the pointed perforatorium at the tip of the spermatozoon, while the
remaining portion of the acrosome grows backward as a band against one
side of the asymmetrical and elongating nucleus, with which it becomes
very intimately united as the spermatozoon matures. It is the view of
Bo wen (19246) that the acrosome or perforatorium is not merely a boring
organ, as commonly thought, but a secretion with a special function in
fertilization, thus corresponding in origin with the secretion droplets
observed to arise in connection with the Golgi material in gland cells
(p. 76). Van Herwerden has shown the presence of an oxidase in the
acrosome region. Certainly the acrosome cannot be a boring organ in the
spermatozoon of Lepisma, in which it lies at the base of the nucleus rather
than anterior to it.

Nucleus. — No conspicuous changes occur within the nucleus until the
acroblast and its differentiated acrosome have completed part or all of

23 In Lepidoptera and grasshoppers the Golgi bodies do not fuse but give rise to a
common acrosome (Bowen, 1922ae). Parat (1928) regards the acrosome as a vacuole,
largely because it stains with neutral red. Pollister (1930) finds no neutral-red stain-
ing substance in Gerris from the close of the first spermatocyte division to the formation
of the acroblast in the spermatid; it then appears as a secretion within the acroblast.
H. Johnson (1932) finds the chondriosomes and the chromophilic rim of the dictyo-
somes in insect spermatocytes to react similarly to Janus green and certain other vital
dyes and questions the complete homology of the dictyosome-acroblast complex with
the somatic Golgi apparatus.

2" Sjovall (1906) on the guinea pig, Terni (1914) on Geotriton, Gatenby (1917) on
mollusks and Lepidoptera. In certain mammals a portion of the Golgi remnant is
said to remain as a part of the middle piece (Weigl, 1912; Gatenby and Woodger,
1921).

GAMETOGENESIS AND SPOROGENESIS

221

their migration around it. The chromatic substance is
then seen to arrange itself in a layer against the inside of
the nuclear membrane, and as spermiogenesis proceeds
it abandons the posterior portion and collects as a com-
pact, deeply staining cap at the anterior side. As the
acrosome begins to form the perforatorium, this chro-
matic cap becomes very asymmetrical and the whole
nucleus elongates and begins its transformation into the
slender sperm head. The "pseudoblepharoplast,"
which has already been mentioned and which may pos-
sibly represent chromosomal material, disappears at
about this stage. The head continues to elongate in the
form of a narrow spoon with the acrosomic band lying
in the hollow; eventually it becomes a slender pointed
body in which nucleus and acrosome can no longer be
distinguished. During these changes the non-chro-
matic constituents of the nucleus gradually diminish
and disappear, so that the nucleus of the spermatozoon
is an extremely concentrated chromatic mass in which
structure can be demonstrated only in rare cases.

Cytoplasm. — As the other components of the sper-
matid undergo the transformation outlined above, the
cytoplasmic cell body elongates and remains visible
around them (with the possible exception of the tip of
the axial filament) until a comparatively late stage.
Toward the close of spermiogenesis in the insects it has
been ascertained that a cytoplasmic ball, containing the
Golgi remnant and other granules of an unknown nature,
is sloughed off and ingested by the nutritive epithelial
cells lining the spermatic cyst. In other animals a cyto-
plasmic mass is likewise eliminated, but the amount of
"active" protoplasm contained in it is uncertain.

The Mature Spermatozoon (Fig. 134). — The mature
spermatozoon has two main parts : the head, which is a
dense chromatic mass comprising the nucleus, the acro-
some, and sometimes a skeletal fiber of uncertain origin;
and a tail, consisting of an axial filament produced as an
outgrowth from the distal centriole, the thread-like
sheaths formed by the chondriosomal derivatives, and
an uncertain amount of residual cytoplasm. It is prob-
able that a thin cytoplasmic membrane exists about
the head also, although this is ordinarily invisible.
Koltzoff (1909) was able to demonstrate a membrane in
this region by using hypotonic solutions. In A rhacia and
Nereis, according to Popa (1927), the sperm head con-

/--

Fig. 134.— Dia-
gram of a typica.
mammalian sper-
matozoon, a, acro-
some; n, nucleus;
c, proximal centri-
ole; c', distal cen-
triole and deriva-
tives; w, cell mem-
brane; d, chondrio-
somes; /, axial fila-
ment of tail; m,
middle piece; p,
principal piece of
tail; e, end piece of
tail. {After Bowen,
1924c.)

222

INTRODUCTION TO CYTOLOGY

sists of a central hydrophilic substance representing the nucleus, a periph-
eral lipochromatic layer consisting of cytoplasm with lipides and lipopro-
teins, and a delicate outer membrane; a fatty layer surrounds the whole
cell. In Sepia, W. J. Schmidt (1928) concludes that the head, which is
anisotropic in polarized light, is composed largely of submicroscopic rod-
shaped micellae arranged parallel to the longitudinal axis.

In many animals, particularly mammals, a ''middle piece" is more
distinctly differentiated than it is in insects, the spermatozoon therefore
appearing to have three main parts. In general it is more convenient to

J

Fig. 135. — Spermatozoa of various animals. A, Triton (salamander). B, Nereis
(annelid). C, guinea pig. D, Phyllopneuste (bird). E, sturgeon. F, Vesperugo (bat).
G, Castrada (turbellarian). H, Pinnotheres (crustacean). I, Homarus (lobster). /,
Ascaris (nematode): a, apical body; n, nucleus; r, "refringent body." (From the works of
Ballowitz, F. R. Lillie, Meves, Luther, Koltzoff, Herrick, and Scheben.)

think of the middle piece as a portion of the tail. The tail of the typical
animal spermatozoon as a rule may be said to have three segments,
though in certain animals all of them may not be differentiated. These
are the "middle piece," in which the axial filament is enclosed in a sheath
of undifferentiated cytoplasm carrying the mitochondrial elements and
the centrioles; a ''principal piece," which has a thin sheath of questionable
origin but no undifferentiated cytoplasm; and an "end piece," which is the
naked posterior end of the axial filament. Many minor variations in
all of these cell elements are known, the spermatozoa of different animals
thus differing widely in appearance (Fig. 135).

GAMETOGENESIS AND SPOROGENESIS

223

In some animals, notably certain arachnids, crustaceans, myriapods,
and nematodes, the spermatozoon has no tail.^^ Although the structures
developed in such bizarre types of sperms are very different from those
of the ordinary flagellate type, Bo wen finds that they are derived from
the same components of the spermatid. For example, the "refringent
body" in nematodes, the "capsule" in decapods, and the ''honeycomb"
and "valves" in myriapods are all derived from the Golgi apparatus and
hence may be compared to the acrosome of other spermatozoa.

The Structure of Other Ciliated Cells. — In addition to zoospores and
gametes, there are other cells which possess special motor
structures. Of particular interest are the motor apparatus
of flagellates and the ciliary mechanism of certain epithe-
lial tissues.

Many types of motor apparatus are known in motile
organisms. 2^ In Menoidium (Fig. 136) the apparatus con-
sists of a single flagellum, a blepharoplast, a centrosome
at the surface of the nucleus, and a rhizoplast connecting
the blepharoplast with the centrosome. At the time of
cell-division the blepharoplast divides, its halves remaining
connected for a time by a slender paradesmose. Similar
in many respects is the mechanism in Peranema (Hall and
Powell; Brown). In Polytoma and other forms with two
flagella (Fig. 110) there are also two blepharoplasts, be-
tween which a paradesmose is usually present, at least dur-
ing division.-^ In some instances a centronema is said to
extend from the centrosome inward to a karyosome. In
Trichomonas niuris there is a single body which acts as
both blepharoplast and centrosome. To this " centroblepharoplast "
are attached three short, free flagella and one long one forming the margin
of the undulating membrane. Along the base of the membrane and
connected with the blepharoplast is a "chromatic basal rod," and
within the cell may be seen certain other peculiar differentiations. As
mitosis begins, the blepharoplast buds off a smaller new one and the
two diverge like centrosomes to opposite poles of the achromatic

2^ See Bowen (19256) and literature there cited; also Sokolow (1929o6).

^^ For accounts of the flagellar apparatus of flagellates and Protozoa, see Minchin
(1912), M. Hartmann (1911), Wilson (1925), Calkins (1926) and the papers by
R. G. Sharp (1914), Yocum (1918), C. V. Taylor (1920), Rees (1921), McDonald'
(1922), Hall (1923, 1925a), Hall and Powell (1928), Kofoid and Swezy (1915-1923),
Kofoid and Christiansen (1915), Entz (1918), Nieschulz (1922), Belaf (1921), Wenrich
(1921), A. S. Campbell (1926, 1927), Bunting and Wenrich (1929), Kater (1929), and
V. E. Brown (1930). For accounts of cilia and their action, see Heidenhain (1911),
Lundeg&rdh (1922), Petersen (1929), Gray (1928, 1931), and Lucas (1932).

'^''Polytoma uvella (Entz, 1918), Chlamydomonas nasuta (Kater, 1929), Oxyrrhis
marina (Hall, 1925a).

Fig. 136.—

Menoidium in-
curvum, showing
motor appara-
tus. See text.
(After Hall,
1923.)

224

INTRODUCTION TO CYTOLOGY

figure, a paradesmose being drawn out between them. Apparently,
one or two of the free fiagella accompany the new blepharoplast, new ones
later growing out to restore the full number. It is also accompanied
by a new chromatic basal rod, which begins to differentiate as a row of
granules even before the division of the original blepharoplast (Wenrich,
1921).

In the trypanosomes, as in the infusoria, there are two nuclei: the
trophonucleus and the kinetonucleus. Motor mechanisms differ con-
siderably within the group, but it seems that the flagellum is usually borne

•te-

A B C

Fig. 137. — A, B, ciliary mechanism in Lampsilis. The cilia (c) are fusrd in pairs at
their tips. Below the basal corpuscles (6) in the cuticle each cilium splits into two strands
which connect with strands from other basal corpuscles. (After Grave and Schmitt, 1924.)
C, diagram of a ciliated epithelial cell based on the figures of Saguchi (1917).

on a basal granule (centrosome?) associated with the kinetonucleus. At
the time of cell-division the trophonucleus, kinetonucleus, and basal
granule all divide. Although it was formerly thought that the flagellum
also split, it now seems clear that it remains attached to one half of the
divided basal granule while a new one arises from the other half.^^

In ciliated epithelial cells each cilium is associated with a basal
corpuscle in or near the cell membrane (Fig. 137). The nature of such
basal granules has been the subject of a long controversy beginning with
the statement of the theory that they, like the granules bearing the axial
filament in the spermatozoon, are modified centrioles or centriole deriva-

28 Rosenbusch (1909), Kuczynski (1917), Hartmann and NoUer (1918).

GAMETOGENESIS AND SPOROGENESIS 225

tives.-^ In ciliated epithelial cells, according to Saguchi, there is a basal
corpuscle at the base of each cilium. The granules and cilia are in parallel
rows. Beneath each row there is a transparent zone in which the rootlets
of the cilia are anchored and through which they pass and become
continuous with strands of a cytoplasmic reticulum. Saguchi regarded
the basal corpuscle as the kinetic center of ciliary movement but not as a
centriole derivative.

In the gill cells of certain mollusks^" the ciliary rootlets below the
basal corpuscles form a continuous system which probably represents the
structural basis for the coordinated action of the cilia of a given cell.
The view of Grave and Schmitt, that the systems of adjacent cells are
continuous, is disputed by Bhatia and by Lucas, who believe the coordi-
nating impulses pass from cell to cell through the general cytoplasm and
the membranes. In any event, the evidence shows clearly that the cilium
or the flagellum is itself an actively contractile element and not merely a
passive element operated by an intracellular mechanism (see Gray, 1931).

-^ Henneguy (1897), Lenhossek (1898). This theory is favored by Helvestine
(1921), Jordan and Helvestine (1923) for certain cells, and Kindred (1927). It was
opposed by Saguchi (1917) and by Erhard (1911), who reviewed the evidence then
available.

^0 Grave and Schmitt (1924, 1925) on Lampsilis and Quadrula, Bhatia (1927) on
Mytilus, Lucas (1931) on Mytilus and other genera.

CHAPTER XV

SYNGAMY

The sexual union of two gametes is known as syngamy. In the case of
organisms having large female gametes and small, more active male
gametes, it is customary to refer to syngamy as the fertilization of the egg
by the sperm ; but it should be borne in mind that the syngamic reaction is
in all cases mutual, and that it is the fusion product of the two gametes
which proceeds with development.

Syngamy has two important results: firstly, it has a pronounced
effect upon the physiological state of the cells concerned and hence upon,
ensuing developmental processes. This may manifest itself in various
ways, commonly in the activation of an egg whose development has
ceased temporarily, or in the onset of a dormant condition, as in the
zygotes of certain lower plants. Secondly, it brings about a significant
alteration in the constitution of the nucleus. Syngamy culminates in the
fusion of two nuclei each of which has a gametic chromosome complement,
typically a single set; hence the zygote nucleus so formed has a zygotic
complement composed typically of two sets. This doubling of the
chromosome number (diplosis) has far-reaching consequences, as will be
emphasized in later chapters.

PLANTS

The general features of gametic fusion in plants are extraordinarily
diversified, notably in algae and fungi. ^

Algae. — Fusions involving gametes of the various types described in
the preceding chapter take place as follows. In Ulothrix two morpholog-
ically similar, motile gametes meet and fuse to form a resting zygospore
(Fig. 138, A). The exact manner of fusion varies greatly in such forms,
but commonly it begins at the ciliated end.^ In Edocarpus, also, the
gametes are morphologically similar, but some of them become relatively
passive and anchor themselves to the substratum by one cilium, while

1 For an extensive account of sexual and asexual cell and nuclear fusions in plants,
see Tischler (1921-1922). For angiosperms, see also Schlirhoff (1926), Dahlgren
(1927a), andSchnarf (1929); for algae, Oltmanns (1922-1923) and G. M. Smith (1933);
for fungi, Guilliermond (1913e), Atkinson (1915), Wager (1920), Giiumann-Dodge
(1928), and Fitzpatrick (1930).

2 That such similar gametes are actually unlike sexually, and secrete charac-
teristically different substances into the medium, is shown by the work of M. Hart-
mann and his associates, chiefly on green algse. See M. Hartmann (1932).

226

SYNGAMY

227

more active ones become attached by a cilium to the anchored ones and
gradually undergo fusion with them (Fig. 138, B). The fusion culminates
in the union of the nuclei. In such gametic fusions the plastids undergo
no fusion, so far as is known. In some cases they have been followed
through into the new individual. In Fucus the large passive eggs and the
small motile spermatozoids are shed from the organs which bear them,
their union occurring in the sea water. Many spermatozoids attach
themselves to each egg by one cilium, but after one of them enters the egg
the others move away. The male nucleus remains relatively small up to
the time it fuses with the egg nucleus, and a centrosome with an aster

Fig. 138. — Syngamy in various alga. A, gamete, union of similar gametes (isogamy),
and zygote of Ulothrix. B, isogamy in Ectocarpus siliculosus. (After Oltmanns, 1897.)
C, portion of filament of CEdogonium; spermatozoids escaping from antheridial cells below;
spermatozoid about to enter egg above. (After Coulter.) D, the formation of eggs by
subdivision of a ccpnocytic protoplast in Spharoplea. E, portion of filament of Sphceroplea
showing several eggs; spermatozoids have entered through pores in filament wall. (D and
E after Klehahn.)

appears near the nuclear membrane at the point where the male nucleus
enters (Yamanouchi, 1909). This latter phenomenon, which is very
suggestive of what occurs in animals, has also been observed in Didyota
(J. Williams, 1904).

In (Edogonium and Vaucheria the egg is not liberated from the
oogonium but is fertilized in situ by a spermatozoid. The latter passes
into the oogonium through a specially differentiated pore and then enters
the egg at a more or less distinct receptive spot. In the mature male
gametes of Vaucheria, Chara, and Coleochcete no plastids have been demon-
strated, the new individual apparently deriving these organs wholly from
the female gamete. This statement, however, may require revision when
male gametes have been more fully studied with methods specially devised
for the investigation of cytoplasmic differentiations. In Polysiphonia the
non-motile male gamete (spermatium) comes in contact with a prolonga-

228 INTRODUCTION TO CYTOLOGY

tion (trichogyne) of the female sex organ (carpogonium). Solution of the
intervening walls allows the nucleus of the spermatium to pass into the
trichogyne and down to the female nucleus in the base of the carpogonium
(Fig. 139, A). The male nucleus, when it reaches the female nucleus,
appears as a group of 20 chromosomes. In this condition it enters the
female nucleus while the latter is yet in the reticular state. Soon the
female reticulum condenses into 20 chromosomes, which arrange them-
selves with the 20 paternal chromosomes in the spindle as the fusion
nucleus divides (Yamanouchi, 1906). The spermatium of the Floridese is
said to carry no plastids.

A special condition is found in the Conjugatse. Here certain vegeta-
tive cells, after little morphological alteration, fuse in pairs to produce
resting zygospores. In Sjnrogyra, for example, the entire protoplast
passes through a conjugating tube to unite with a similar cell, commonly
in another filament. The two nuclei fuse, but the plastids remain distinct
and those introduced by the migrating cell are observed in some species to
degenerate in the zygospore (Fig. 162). In some species the gametes
meet and form the zygospore in the conjugating tube. The movement
of these gametes is accomplished through the remarkable action of
contractile vacuoles, which withdraw water from the central sap vacuole
and discharge it between the protoplast and the wall.^

In the diatoms^ there are two general modes of sexual behavior, with
minor variations in the different species. With rare exceptions these
modes characterize the two main groups, Pennatae and Centricae. In
Rhopalodia gibba, a representative of the former group, two individuals
meet and form a common mass of jelly between them. In each individual
the nucleus undergoes two successive divisions, the protoplast then divid-
ing into two portions, each with a large and a small nucleus. These two
portions now fuse with the two produced by the other individual, forming
two zygotes which develop into large auxospores. In each case the large
nuclei fuse and the small ones degenerate (Klebahn). In some diatoms,
for example, certain forms of Cocconeis, the two uniting individuals show
distinct differences in size and sexual behavior (Geitler, 1927afe). In the
Centricae the auxospores are formed asexually, the sexual act consisting in
the union of small biciliate gametes. In Coscinodiscus these are of
two types: small colorless ones and larger ones with chromatophores
(Pavillard).^

'Lloyd (1925, 1928a). Conard (19Slh) claims that the cytoplasmic portions of
the gametes remain distinct and are separated by the first wall at germination.

4 Klebahn (1896), Lauterborn (1896), Karsten (1897, 1900, 1904, 1912, 1924),
O. Mliller (1906), Bergon (1907), Pavillard (1913), Geitler (1927a6c, 1928a6c, 19296),
von Cholnoky (1927, 1928, 1929), P. Schmidt (1923, 1927a6). See Pavillard (1910)
and Oltmanns (1922).

^ These small cells are termed "microspores" in the literature. The rarely
observed "microspores" in Pennatae seem to be asexual.

SYNGAMY

229

Fungi. — The fusion of the sexual elements described in the preceding
chapter (p. 199) proceeds as follows. In Synchytrium the morphologically
similar uniciliate gametes unite to form a zygote which penetrates into a
host plant. In Monohlepharis the uniciliate male gamete creeps along the
surface of the oogonium to its opening, where, after loss of its cilium,
it unites with the egg to form a resting oospore ; this matures either inside
or outside the oogonium. In Albugo Candida and Pythium Deharyanum
the egg is entered by a single male nucleus through a conjugating tube
from the antheridium (Fig. 139, B). The nuclear fusion in Pythium
and Achlya occurs in association with a cytoplasmic "coenocentrum"
(P. Patterson). In Saj)rolegnia, which has several eggs in the oogonium,

y^ >i

A B C

Fig. 139. — A, Syngamy in Polysiphonia; group of paternal chromosomes about to enter
female nucleus. {After Yamanouchi, 1906.) B, Syngamy in Albugo Candida; female
nucleus in ooplasm near coenocentrum (larger dark body) ; antheridial tube about to dis-
charge male nucleus. {After Davis, 1900.) C, Syngamy in Lygodium palmatum. The
coiled nucleus of the functional spermatozoid lies against the right end of the egg nucleus,
while its cilia lie in the cytoplasm near by. Outside the egg are other spermatozoids.
Arrow indicates neck canal. (After Rogers, 1926.)

the antheridium sends in a branching tube which delivers a male nucleus
to each egg.

In the zygomycetes® the contents of the multinucleate gametangia do
not subdivide into small gametes but meet and fuse in their entirety.
The product is a heavy-walled zygospore. The extreme minuteness of
the nuclei and the abundance of metabolic products in the protoplasm
have so far made it impossible to clear up the matter of nuclear behavior
in this group.

In the higher ascomycetes the sex organs are typically antheridia and
ascogonia. Some species have both organs, some have one or the other,
and some have neither. In some cases the organs are uninucleate and in
others multinucleate. After an ascogonium has been entered by the con-
tents of an antheridium the nuclei do not fuse (according to one prevalent
view) but associate and divide repeatedly in pairs ("conjugate division"

« P. A. Dangeard (1906), Moreau (1911, 1913, 1915), Keene (1914), Burgeff (1915),
Macormick (1912), Baird (1924).

230 INTRODUCTION TO CYTOLOGY

of a "dikaryon") in the ascogenous hyphse which grow out from the asco-
gonium. In each ascus the two associated nuclei finally fuse. Accord-
ing to this interpretation/ therefore, the nuclear fusion is merely delayed :
instead of occurring in the ascogonium, it takes place in the ends of
branches produced by the latter, namely, in the asci; and this fusion may
be regarded as sexual in nature, as originally stated by Dangeard (1894).

Other observers have claimed that there are two nuclear fusions in
the ascomycete life cycle : in addition to the fusion easily observable in the
ascus, it is contended that an earlier fusion occurs in the ascogonium after
the entrance of the contents of the antheridium,^ or in the ascogonium
when the antheridium is functionless or absent,^ or in vegetative cells
when the ascogonium is functionless or absent. ^^ In the ascomycetes
generally the fusion nucleus, or ''primary ascus nucleus," initiates three
successive mitoses to form the eight ascospore nuclei. A reduction in
chromosome number occurs in the course of these mitoses. Adherents of
the view that there are two nuclear fusions in the life cycle claim that
there is a "double reduction" in the ascus (p. 281). In certain yeasts it
has been shown that the production of ascospores is preceded by a union
of two cells and a fusion of their nuclei, the fusion nucleus dividing to form
the spore nuclei (see Guilliermond, 1920n).

In the hymenomycetes it has long been known that a fusion of two
nuclei occurs in the basidium, itself the terminal cell of a hypha with
binucleate cells, prior to the formation of the four basidiospore nuclei
(Fig. 164). The discovery of the origin of the binucleate condition is
more recent. ^^

In certain species of several genera, including Co'prinus, Aleurodiscus,
PanoBolus, and Schizophyllum, it has been shown that carpophores,
although they will sometimes develop on a mycelium from a single
spore, appear freely only when mycelia from different spores are inter-
mingled. Unions then occur between uninucleate hyphae of different
strains and initiate the binucleate dikaryophase. According to Buller, the
migrating nucleus divides after entering the adjacent hypha, one of the
daughter nuclei then moving on to the next cell to repeat the process. In
this way the originally uninucleate mycelium becomes progressively
"diplodized. " In the resulting binucleate mycelium the paired nuclei

' P. Claussen (1907, 1912), W. H. Brown (1909, 1910a, 19116), Faull (1911, 1912),
Nienburg (1914), Ramlow (1914), F. Brooks (1910), McCiibbin (1910), H. B. Brown
(1913), Fitzpatrick (1918a), Frey (1924), S. G. Jones (1925), Delitsch (1926).

* Harper (1895-1905), Blackman and Fraser (1905), Gwynne-Vaughan and
Williamson (1931, 1932).

9 Blackman and Fraser (1906a), Fraser (1907), Welsford (1907), Dale (1909),
Gwynne-Vaughan and Williamson (1930).

i» Fraser (1907, 1908), Carruthers (1911), Blackman and Welsford (1912).

11 Kniep (1915 el seq.), Bensaude (1918), Lehfeldt (1922), Mounce (1921, 1922),
Hanna (1925, 1928), Sass (1929), Buller (1930, 1931).

SYNGAMY 231

divide in unison before each cell division, their descendants eventually
fusing in the basidium. Here the nuclear fusion ("karyogamy") is
delayed until some time after cytoplasmic union ("plasmogamy"), these
two events being separated by a binucleate phase in the life cycle.

In the rust fungi there are life cycles of several kinds, these differing
in the presence or absence of various spore types and of cell and nuclear
fusions. ^2 Some forms have uninucleate cells throughout the cycle, some
are entirely binucleate, and some have uninucleate and binucleate, or even
short plurinucleate, phases. In a number of forms, including Puccinia
graminis, the common wheat rust, each cell of the young teliospore is
binucleate. These two nuclei eventually fuse, and as the teliospore
germinates to form a promycelium, which is homologous with the basidium
of the hymenomycetes, the fusion nucleus divides to four which enter the
sporidia. Beginning with the work of Blackman (19046) and Christman
(1905) on Phragmidium and certain other genera, it was thought that the
binucleate condition originated by nuclear migration between cells or by
cell fusions, particularly in the basal region of the secial sorus. Evidence
recently brought forward ^^ indicates that in certain species of Puccinia
a mycelium developing from a single sporidium, or basidiospore, pro-
duces as a rule only sterile secia, and that chains of aeciospores develop
only when pycniospores of a different strain are added to the infec-
tion or when "plus" and "minus" mycelia develop close together.
Some of the cytological changes involved here have been ascertained.
Andrus (1931) has announced that in Uromyces appendiculatus the spore-
forming cells in the base of the secium are not formed by fusion but are
enlarged female cells which send elongated trichogyne-like hyphaj through
the opposite side of the leaf, where they meet and fuse with spermatia
(pycniospores) from infections of opposite strain. Nuclei apparently
pass through the septa of the trichogynes into the female cells, which
then proliferate and produce chains of binucleate seciospores. Similar in
many respects is R. F. Allen's (1932a) interpretation of the phenomena in
Puccinia triticina. Here the mycelium formed by a single sporidium
produces spermatia, receptive hyphee, and the primordia of aecia. After
nuclei from spermatia of the opposite strain enter the receptive hyphse,
the resulting binucleate (or plurinucleate) hyphae extend into young
secia and develop seciospores.

In the smut fungi, as exemplified by species of Ustilago, the binucleate
condition arises as the result of a union of promycelial cells, sporidia, or
mycelial cells which they produce, the . two nuclei fusing later when
chlamydospores are differentiated. ^^ It is known further that the sporidia

12 See Arthur (1929), Gaumann-C. Dodge (1928), B. O. Dodge (1929a), and
Jackson (1931).

i^Craigie {I927ab, 1928, 1931), R. F. Allen (1929, 1930, 1932), Hanna (1929a).
1* P. A. Dangeard (1893), Lutman (1910), Rawitscher (1912), Kniep (1919, 1920).

232

INTRODUCTION TO CYTOLOGY

and the mycelia developing from them are of two kinds, only those of
unlike strain ("plus" and "minus") uniting when brought together.^^

The significance of the hyphal and sporidial fusions which lead to
the binucleate condition of the cells in the dikaryophase of ascomycetes
and basidiomycetes is a matter of debate among mycologists. The view

V»-

M

,M7:^^

fir

■4.:':

FiG. 140. — Syngamy in Riccardia. 1, sections of spermatozoids in archegonium; one
male nucleus applied to egg. 2, male nucleus in egg cytoplasm. 3-7, passage of male
nucleus into egg nucleus and its development of a distinct reticulum. 8, 9, first mitosis in
zygote; paternal and maternal chromosomes intermingled. {After Showalter, 19266.)

that they represent a sexual act is disputed by those who hold that they
are primarily nutritive in character ("nutritive heterothahism"),
although they may be followed by some of the beneficial effects of true
sexuality. Comparisons with other plants strongly suggest that sexual
differences in fungus nuclei and mycelia, as well as other conditions
affecting their interaction, are often related to meiotic factor segregation
in sporogenesis. This topic is discussed further at page 386.
15 Kniep (1919, 1920), Stakman and Christensen (1927), Hanna (19296).

SYNGAMY

233

Bryophytes and Pteridophytes. — The cytological details of the union
of the motile spermatozoid with the egg in bryophytes are best known in
certain liverworts, owing especially to the researches of Showalter
(1926a6, 1927 ab, 1929). In Riccardia pinguis (Fig. 140) the elongated
body of the spermatozoid applies itself to the surface of the egg, becomes
more slender, and gradually sinks through the membrane into the cyto-
plasm. The chromatic matter of the egg nucleus contracts, and one end
of the sperm nucleus extends through the membrane of the egg nucleus,
where it becomes considerably swollen. The female nuclear matter then
loosens up, and the swollen end of the penetrating male nucleus is seen to
lose its definite outline and differentiate a chromatic reticulum and a
nucleolus. After penetration is complete the
female and male reticula remain distinguish-
able for some time, but in the late prophase
and the metaphase of the first embryonal
mitosis the chromosomes of the two parents
form a single group. The fate of the cyto-
plasm, blepharoplast, and cilia of the male
gamete is uncertain, but in view of what has
been observed in other species it is highly
probable that they are absorbed in the egg
cytoplasm.

In a number of other liverworts^*^ the male
nucleus does not enter the egg nucleus in the
compact form but becomes vesicular and
reticulate in some degree before the fusion
occurs (Fig. 141). In Sphoerocarpos it ap-
pears that the nuclei do not undergo fusion while in this state but
develop separately their chromosomes, which then take their places in a
common mitotic spindle, as in many animals. In Preissia, centrosomes
are reported in the egg cytoplasm during the fertilization period. This,
together with observations on certain algae (p. 227), suggests that in
certain plants, as in animals, the differentiation of division centers in
the egg cytoplasm may be induced in some manner by the entrance of the
spermatozoid. The fate of the non-nuclear portions of the spermatozoid
may prove to be of interest in this connection.

In the pteridophytes^^ the multiciliate spermatozoid enters the egg
cytoplasm. It has been stated that it continues into the egg nucleus in
its entirety, but in Lygodium it has been clearly shown that the cilia (and

^^Pellia Fahbroniana (Showalter, 19276); Riccia (Garber, 1904; Black, 1913);
Corsinia (K. Meyer, 1911); Preissia quadrata (Graham, 1918; Haupt, 1926); Rehoulia
(Woodburn, 1920); Sphcerocarpos (Rickett, 1923). In Funaria flavicans (moss) the
male nucleus enters rounded up but still compact (Beardsley, 1931).

" Pilularia (Campbell, 1888); Onoclea (Shaw, 18986); Nephrodium (Yamanouchi,
1908b); Lygodiu7n (Rogers, 1926); Equisetum (Sethi, 1928).

Fig. 141. — Syngamy in
Anthoceros. Male and female
nuclei about to fuse in lower
part of egg in venter of archego-
nium; elongated plastid above
them. Gametophyte cells show
one nucleus and one plastid each.

234

INTRODUCTION TO CYTOLOGY

presumably the blepharoplast and most of the cytoplasm) are left in the
cytoplasm as the compact and coiled male nucleus enters the egg nucleus
(Fig. 139, C). The male nucleus then gradually becomes reticulate, and
eventually the materials contributed by the two gametes become
indistinguishable.

The behavior of the plastids during gametogenesis and syngamy in
ferns is not well known. Plastids may frequently be seen in the develop-
ing egg, and presumably they play a role in
spermatogenesis somewhat like that in bryophytes
(p. 203). At present it seems probable that the
plastids of the sporophyte are derived chiefly if
not wholly from the female gamete.

Gymnosperms. — In the cycads and Ginkgo the
pollen tube discharges two motile spermatozoids
near the archegonium, into which one of them
passes by squeezing between the neck cells. The
nucleus of the spermatozoid then becomes free
from its cytoplasmic sheath, blepharoplast, and
cilia and advances alone to the egg nucleus, with
which it fuses^^ (Fig- 142). In Ginkgo the cyto-
plasm and motor apparatus are left in a "receptive
spot" formed by vacuoles in the upper part of the
egg. In Bowenia the paternal and maternal
chromosomes can be distinguished in the first few
mitoses preceding wall formation in the embryo.
In the Coniferales and Gnetales the male cells
have no motile apparatus. Each consists of a
nucleus surrounded by a more or less sharply
matozoid above; another dehmited mass of cytoplasm. In most cases this
spermatozoid at surface of cytoplasm remains intact until after the male
egg. {After Wehher, 1901.) ^^^^ ^^^ entered the egg, but in other forms it

mingles with the cytoplasm of the pollen tube, so that only male nuclei,
rather than completely organized male cells, are delivered to the egg.
All the nuclei present in the pollen tube — stalk nucleus, tube nucleus,
the two male nuclei, and, in certain species, free prothallial nuclei — may
be discharged into the egg. All but the functioning male nucleus usually
degenerate at once, but in some cases they have been observed to undergo
division.

Male cells of conifers show two general modes of behavior after their
entrance into the egg. In some instances the male's cytoplasm is left
in the peripheral region of the egg while the nucleus advances alone to

i«Hirase (1895, 1898, 1918), Ikeno (1901), Shimamura (1928) and Herzfeld
(1927) on Ginkgo; Ikeno (1898) and Kuwada (1925o, 19266) on Cycas; Chamberlain
(1910, 1912, 1916) on Dioon, Ceratozamia, and Stangeria; Lawson (1926) on Bowenia.

Fig. 142. — Syngamy in
Zamia. Male and female
nuclei uniting at center;
cytoplasmic sheath and spi
ral blepharoplast of sper

SYNGAMY

235

the centrally placed egg nucleus. ^^ In other cases^" the male cytoplasm
remains intact and surrounds the fusing sexual nuclei. The pollen-tube
cytoplasm often plays a conspicuous part in the formation of this
"mantle."

The behavior of the chromosomes during the fusion of the gametic
nuclei and the first embryonal division has been described in a number of
conifers ; similar data for the cycads are as yet comparatively few. As a
general rule the chromatic elements of the two nuclei, although in the
reticular condition when the nuclei unite, do not become very intimately
associated in the fusion nucleus but remain distinguishable until the first
embryonal mitosis occurs. They then develop two groups of chromo-
somes which become arranged in a common achromatic figure-' (Fig. 143).

I^Cv^ssT^JmS.' ^l^^

Fig. 143. — Syngamy in conifers. A, male nucleus pressing into female nucleus in
Pinus. B, first mitosis in zygote, showing parental chromosome groups. {After Ferguson,
1904.) C, parental chromosome groups in Larix. {After Wdycicki, 1899.)

In Sequoia the male nuclei escape from their cytoplasm before their
discharge from the pollen tube, and after the nuclear fusion in the egg the
contributions of the two gametes cannot be distinguished (Lawson,
1904a). In gymnosperms, as in other organisms, all of the chromosomes,
paternal and maternal, divide longitudinally in the first embryonal
mitosis, the daughter chromosomes being distributed to the daughter
nuclei.

Angiosperms. — The pollen tube, which is the elongated tube cell
bounded by the greatly extended intine, grows from the pollen grain on
the stigma through the style to the ovarian cavity and then by way of the
micropyle of the ovule through the nucellus and into the embryo sac
(Fig. 127). Usually the tube makes its way between the cells of the
style by means of enzymes which dissolve the middle lamellae of their
walls (Paton, 1921). After entering the sac the tube ruptures at its

^^ Pinus (Ferguson, 1901, 1904), Thuja (Land, 1902), Juniperus (Norcn, 1904),
Cryptomeria (Lawson, 19046), Libocedrus (Lawson, 1907), Ephedra (Berridge and
Sanday, 1907).

2" Taxodium (Coker, 1903), Torreya (A. Robertson, 1904; Coulter and Land,
1905), Cephalotaxus (Coker, 1907), Phyllocladus (Kildahl, 1908), Juniperus (Nichols,
1910), Agathis (Eames, 1913), Taxus (Dupler, 1917).

^^ Pinus (Blackman, 1898; Chamberlain, 1899; Ferguson, 1901, 1904), Larix
(W6ycicki, 1899; Sm61ska, 1927), Tsuga (Murrill, 1900), Juniperus (Noren, 1907),
Cunninghamia (Miyake, 1910), Abies (Hutchinson, 1915), Bowenia (Lawson, 1926).

236 INTRODUCTION TO CYTOLOGY

end, discharging the two male gametes, together with a certain amount
of pollen-tube cytoplasm and sometimes the tube nucleus. Frequently
the tube appears to pass directly through a synergid. It has been
suggested that the synergids produce enzymes which swell and rupture
the membrane of the pollen tube (Goebel; Haberlandt, 1927). As they
appear in the embryo sac, the male gametes may be complete cells or
only nuclei with no specially delimited cytoplasm (see p. 210). Fre-
quently the nuclei are markedly vermiform. Double fertilization, a
process peculiar to angiosperms, now takes place: one male gamete fuses
with the egg, while the other unites with the two polar nuclei or their
fusion product^^ (Fig. 144).

The Gametic Fusion. — The nucleus of one of the male gametes enters
the egg — through a sort of rift, according to Heimans. In cases where
the male gamete is a complete cell in the pollen tube, its nucleus may
become free from its cytoplasm before reaching the egg.^^ In other cases,
however, the male cytoplasm remains distinct from that of the pollen
tube and embryo sac until the surface of the egg is reached. 2"* It has not
yet been demonstrated cytologically in any case that male cytoplasm
enters the egg along with the nucleus. Wylie thinks it probable that
it does so in Vallisneria, and there is genetic evidence that it may enter
in certain other cases (Chapter XXV). It would obviously be difficult
to identify male cytoplasm during the passage of the nucleus through the
egg membrane, or to show that the nucleus is absolutely freed of all
adhering matter previously associated with it. It is expected that
refinements in technique will shed light on this question. Occasional
differences in chromaticity between male and female nuclei are reported,-^
so that one may hope for similar evidence for the cytoplasm.

The fusion of the two gamete nuclei probably occurs in most cases very
soon after they come in contact, though in certain forms it is known to be
considerably delayed. The chromatic matter of the two nuclei at the
time they unite may be in the reticular condition, the male and female
elements becoming indistinguishable in the fusion nucleus. In other
cases^^ it has already reached the condition characteristic of the prophase,
the paternal and maternal elements often being distinguishable in the
spindle in the ensuing division of the zygote. That the same species may
show considerable variation in this respect is indicated by the situation in

22 For reviews of the features of fertilization in angiosperms, see Dahlgren (1927a),
Schurhoflf (1926), Schnarf (1929), and Coulter and Chamberlain (1903).

" E.g., Lilium (S. Nawaschin, 1910; Welsford, 1914), Viola (Madge, 1929), and
Melandrium (Breslawetz, 19306). See Tischler (1921-1922, p. 486).

2^ Vallisneria (Wylie, 1922, 1923), (Enothera (Ishikawa, 1918), Asclejjias (Finn,
1925).

2^ E.g., Heimans (1928; on Lilium) and Kuwada (1925a, 19266; on Cycas).

^^ E.g., Lilium (Guignard, 1891; Weniger, 1918), Calopogon (Pace, 1909), and
Trillium (Nothnagel, 1918).

SYNGAMY

237

Fritillaria, in which Sax (1916, 1918) finds that fusion, though it usually
occurs in the reticulate stage, sometimes takes place after the thick
prophasic threads have been developed. Weniger (1918) reports that
in Lilium the egg nucleus is reticulate and the male nucleus in prophase
as they unite. Whatever the state of the nuclei at the time of their
fusion, all of the chromosomes, paternal and maternal, split longitudinally
in the first mitosis in the zygote, the daughter chromosomes so formed

Fig. 144. — Syngamy in angiosperms. A, end of pollen tube from basal portion of
style of Lilium auratum, showing two male cells and tube nucleus. {After Welsford,
1914.) B, double fertilization in Lilium canadense; sexual nuclei about to fuse in egg;
second male and two polar nuclei fusing at center of embryo sac; s, synergids, one degen-
erated; a, antipodal cells. C, fusion of sexual nuclei in egg of Lilium philadclphicum.
(After Weniger, 1918.) D, the second male and two polar nuclei in Lilium Martagon.
{After Nothnagel, 1918). E, vermiform male nucleus in contact with egg nucleus in Triti-
cum durum. {After Sax, 1918.) F, spireme stage of triple fusion nucleus in Triticum
durum., showing distinctness of chromatic elements of the three nuclei. {After Sax.)
G, inclusion of cytoplasm in fusing sexual nuclei of Peperomia sintenesii; this seems to be an
occasional phenomenon with no special significance. {After W. H. Brown, 19186.)

being distributed to the two resulting nuclei, just as in all the subsequent
divisions in the developing embryo.

The time elapsing between pollination and the union of the gametes
varies greatly in different plants, but the variation shows no necessary
correlation with the length of their styles. The following examples"
may be cited: Zea Mays, 18 to 24 hours; Triticum vulgare, 18 to 20 hours;
Lilium philadelphicum, 60 to 72 hours; Phaseolus vulgaris, 8 to 9 hours;
Acer negundo, 40 to 72 hours; Monotropa unifiora, 5 days; Secale cereale,

2^ See Schnarf (1929) for an extensive list with citations to literature.

238 INTRODUCTION TO CYTOLOGY

7 hours; Phajus grandifolius, 2 months; Hicoria pecan, 5 to 7 weeks;
Datura stramonium, 25 hours at 20°C.; CEnothera ruhrinervis, 36 hours;
Quercus rubra, 13 to 14 months. In Beta vulgaris, growing under summer
field conditions, the period is 20 hours, and a period of equal length
elapses before the fertilized egg divides (Artsch wager, unpubl.). It has
been shown in certain cases that the rate of pollen-tube growth varies
with the temperature and other conditions, which accounts in part for
the discrepant reports of different observers.

The Endosperm Fusion. — The second male nucleus (it may be either
the first or the second to emerge from the pollen tube) passes to one or
both polar nuclei or to the product of their fusion. The fusion of the
three nuclei to form the primary endosperm nucleus is carried out in a
variety of.ways. The most commonly reported mode is that in which the
two polars unite to form a polar-fusion nucleus ("embryo-sac nucleus")
before the entrance of the pollen tube, the male nucleus being added later.
Less frequently the male nucleus meets and fuses with the polar nucleus of
the micropylar end of the sac, the other polar then fusing with the
product. This is the method described by S. Nawaschin (1898, 1899a) in
his accounts of the discovery of double fertilization in Liliuni Martagon
and Fritillaria tenella. In Zea the male nucleus and one polar complete
their fusion while the two polars are in contact but still unfused (V.
Rhoades, unpubl.). The simultaneous fusion of all three nuclei appears
to be a common occurrence ; it has been described in some detail by Noth-
nagel (1918) for Trillium and Lilium. Different modes may occur in
the same plant under varying conditions, notably of temperature (Shibata,
1902, on Monotropa). Although the three nuclei often appear exactly
alike, it is frequently possible to distinguish the male from the polars,
not only by its shape and smaller size, but by the condition of its karyotin.
In Lilium longiflorum (Weniger, 1918), for example, the male nucleus is in
the prophase while the polar nuclei are still reticulate. The membranes
of the three nuclei may persist for some time after they come into intimate
contact, and even after they have disappeared the chromatic elements of
the three constituent nuclei may in many cases be distinguished if the
section has been made in a favorable plane. When fusion occurs in the
metabolic stage this is not so apparent, but when it occurs in the prophase
the three chromatic groups are made out with little difficulty.

As the division of the endosperm nucleus approaches, the chromatic
elements of the three contributing nuclei become increasingly distinct,
even if one or more of the nuclei have fused in the reticulate condition
(Fig. 144, F). As the prophase proceeds, all of the chromosomes (the
triploid number) are seen to be split longitudinally. Since this is repeated
in every subsequent mitosis, the resulting endosperm nuclei are normally
all triploid, each of them having one paternal and two maternal chromo-
some sets. In most angiosperms the developing endosperm passes

SYNGAMY 239

through an early free-nuclear stage, no walls appearing until some time
later (p. 173). In other cases walled cells may be formed from the start. ^^

Although the nuclei throughout the endosperm are all derived by
repeated division from the triple-fusion nucleus in the great majority of
plants studied, cases are known in which at least some of them may be
produced by the polar-fusion nucleus alone without the male, or by the
fusion product of the male and one polar, or by one polar alone. Com-
binations of these methods may be found in tjie same embryo sac. In
Petunia the polar-fusion nucleus divides before the pollen tube opens,
and four endosperm cells are formed. One male nucleus then fuses with
that in the micropylar endosperm cell. That portion of the endosperm
which is derived from this cell is triploid (21 chromosomes), while that
derived from the three other cells is diploid (14 chromosomes) (Ferguson,
1927). Cases of "mosaic endosperm" frequently reported may have their
explanation in such unusual modes of development. Probably more
often they are due to aberrant mitotic behavior on the part of endosperm
nuclei initially triploid.

The propriety of extending the term "fertilization" to the endosperm
fusion may be questioned. Obviously this fusion is not a true syngamic
one. It is followed by a resumption of activity on the part of the nuclei
in the embryo sac; but since this may occur with no nuclear fusion, it
seems evident that it is due to some peculiar condition pervading the sac
after the pollen tube enters. Only rarely does the egg develop without a
nuclear fusion. An activating, or "fertilizing," effect can be recognized
in both fusions, but it now seems proper to regard the endosperm in
angiosperms as gametophytic tissue which, unlike that of gymnosperms,
is arrested in development until after the pollen tube enters the sac; it
then proceeds with development, usually with, but sometimes without,
the addition of extra nuclei.

ANIMALS

The story of syngamy in animals^^ is complicated by the fact that in
many cases the periods of "maturation" and fertilization may overlap.
In sea urchins the two meiotic divisions in the oocyte are completed before
the spermatozoon enters. In certain other cases maturation proceeds as
far as the metaphase of the first mitosis (certain annelids, nemertines,
mollusks, and insects) or the metaphase of the second mitosis (frog,
mouse) but goes no further unless penetration occurs. Finally, in Nereis

*^See Coulter and Chamberlain (1903), Samuelsson (1913), Jacobsson-Stiasny
(1914), Dahlgren (1922, 1923), Stenar (1925), Svensson (1925), Schtirhoff (1926), and
Schnarf (1929).

2^ In the preparation of this portion of the chapter the author has drawn freely
upon Prof. F. R. Lillie's Problems of Fertilization, (1919). See also Lillie and Just
(1924), Doncaster (1920), Agar (1920a), and Wilson (1925).

240

INTRODUCTION TO CYTOLOGY

(annelid) and Ascaris (nematode) penetration takes place before the first
mitosis^" (Fig. 154).

Probably in most animals the whole spermatozoon enters the egg (Fig.
145). In some sea urchins only the head and middle piece enter, while in
Nereis the head alone passes in, leaving the middle piece and tail on the
egg surface. The details of penetration in two of the best known cases
are as follows.

In Nereis the egg has a vitelline membrane, an alveolar cortical layer,
many yolk and oil droplets, and a large central germinal vesicle (nucleus).
If many spermatozoa are present in the vicinity, a large number attach
themselves to the egg, but usually all but one are carried away by an

outflow of jelly from the alveoles of the
cortical layer. This layer now takes
the form of a zone traversed by radial
protoplasmic plates representing the
walls of the alveoles. A transparent
"fertilization cone" extends from the
inner region of the egg across this zone
and touches the membrane at the point
where the spermatozoon is beginning to
penetrate. The perforatorium goes
through the egg membrane and
becomes attached to the transparent
cone. The latter is now withdrawn,
carrying the head of the spermatozoon
into the egg with it. Thus it appears
that the initiative for the final act of
penetration lies with the egg rather than with the spermatozoon. Since
only the head enters the egg, it seems that the only necessary portion of
the spermatozoon in the actual union is the nucleus; the middle piece and
tail are accessory and function only as locomotor organs (F. R. Lillie,
1912, 1919).

In the starfish (Fig. 146) the blunt-headed spermatozoa swim about
with spasmodic movements and apparently by chance come in contact
with the thick zone of sticky jelly surrounding the egg. The egg then
responds to the presence of the spermatozoa by forming one or more
hyaline conical projections on its surface. From the summit of each cone
a delicate filament grows outward through the jelly until it touches and
adheres to any sperm head (now motionless) which happens to lie in its
path. The filament then retracts, drawing the spermatozoon inward
through the jelly to the summit of the cone. Other filaments are at the
same time withdrawn whether they have secured spermatozoa or not.

30 See Wilson (1925, p. 397) and literature cited; also McKay (1927) and Crabb

(19276). -■ ' '.'

Fig. 145. — Syngamy in Physa (snail).
Sperm head and amphiaster at right;
long flagellum extending toward left;
second meiotic division in progress.
{After Kostanecki and Wierzyski, 1896.)

SYNGAMY

241

When the spermatozoon arrives at the surface of the cone it is immediately
engulfed and passes deeper into the egg. The cytoplasmic granules at the
base of the cone disappear, leaving a hyaline pathway along which the
sperm head glides. Other spermatozoa being drawn through the jelly are
usually dropped by the retracting filaments when the first sperm enters
the egg; in case they do reach the egg surface they are stopped by the
fertilization membrane (Chambers, 1922c, 19236, 1930c).

The most striking feature in both of these cases is the relatively
passive role played by the spermatozoon. Instead of actively forcing its
way into the egg by its own power, it is "swallowed" by the egg after its
own movements have ceased. In this connection Bowen (1923, 1924a6)

^i'..Vov^ ^^oi^'^'i'^!^'^'^ Ci5^ii5r^^fc^l-^s^^

f f. C*'n j^"^ ^..*<. .

2'30"

2'33"

2'34"

2 '40"

Fig. 146. — The entrance of the spermatozoon into the egg of the starfish,
occupied by the process is indicated. {After Chambers, 19236.)

The time

has advanced the view that the acrosome with its perforatorium is not
primarily a cutting tool but "essentially a secretory product the principal
function of which is to initiate the physico-chemical reactions of fertiliza-
tion." The spermatozoon may show no such movements as would be
necessary for the use of a cutting or boring tool, and in some animals the
acrosome is neither of the right shape nor properly located to act in such a
capacity. In other animals, however, boring movements do occur.
Probably a pointed perforatorium is advantageous in either active or
passive movement through the jelly and egg membrane.

K fertilization membrane is commonly formed as a result of fertilization.
In the echinoderm it first appears at the point where the spermatozoon is
attached and spreads over the egg with great rapidity. This really
consists in the elevation of a delicate vitelline membrane already present.

242

INTRODUCTION TO CYTOLOGY

a process which Heilbrunn has associated with a lowering of surface
tension. ^1 These changes do not depend upon the actual entrance of the
spermatozoon into the egg ; in Nereis they occur before the slow penetra-
tion can be completed, or even if the spermatozoon is shaken loose shortly
after penetration has begun. In some animals (frog) the amount of
fluid in the "perivitelline space" under the membrane is great enough to
permit the rotation of the egg within it.

In describing the remarkable transformation undergone by the sper-
matozoon within the egg it will be convenient to deal with its various
parts separately.

The Nucleus. — Immediately after gaining entrance to the egg (Fig.
147), the sperm head begins to enlarge and assume the usual form and

Fig. 147. — Diagram of syngamy and cleavage in an animal. It is assumed in this case
that meiosis has been completed before the entrance of the spermatozoon.

structure of a nucleus. Meanwhile it advances toward the egg nucleus.

As Lillie points out, both nuclei pass toward a position of equilibrium in a

cell preparing to divide and consequently meet; the assumption of an

attractive force between them is unnecessary. By the time they meet,

the sperm nucleus has usually, but not always, become equal in size and

appearance to the egg nucleus. The union of these two "pronuclei"

usually occurs at once. In a great many cases there may be no actual

fusion of the nuclei as such. As they come close to one another each

passes through the prophase stages and gives rise independently to its

group of chromosomes, the two groups arranging themselves in a common

spindle which organizes as the nuclear membranes disappear. The

nuclei may behave variously in this respect within the same species. In

Strongylocentrotus lividus, Danchakoff (1916) observed three general

" Heilbrunn (1913, 1915, 1924c, 19256). See also Peterfl (1927), Hobson (1927),
and Chambers (1930a) on the fertilization membrane; also the papers of Just (1920
et seq.).

SYNGAMY 243

modes of behavior : (a) the chromatic sperm nucleus may be added to the
comparatively achromatic egg nucleus, the two forming a common
reticulum from which the chromosomes later condense; (6) the sperm
nucleus may become achromatic before uniting with the egg nucleus, the
achromatic fusion nucleus forming a reticulum from which the chromo-
somes develop; (c) the sperm nucleus may condense its chromosomes
before uniting with the egg nucleus, no common reticulum being formed
and the maternal and paternal chromosomes remaining separate through-
out their development.

In the first cleavage mitosis, whether the gamete nuclei have formed
a common reticulum or not, each chromosome undergoes a longitudinal
division, the halves passing to the two daughter nuclei. This process is
repeated in every subsequent somatic mitosis, so that every somatic
nucleus has descendants of every parental chromosome originally present
in the fertilized egg. In most animals the first cleavage mitosis is fol-
lowed by the division of the fertilized egg into two cells (blastomeres),
but in some cases there are several free nuclear divisions before any
cleavage into cells occurs. In some instances it has been shown that the
plane of the first cleavage is determined by the chance point of entrance of
the spermatozoon, and that the bilaterality of the embryo bears a direct
relation to this cleavage. ^^ In other animals, on the contrary, the plane
of the first cleavage does not coincide with the plane of bilateral symme-
try; moreover, some eggs may show such symmetry before fertilization
(e.g., many insects).

The more or less independent formation of the maternal and paternal
chromosomes without an intimate nuclear fusion before the first cleavage
mitosis is known as gonomery and has been observed in both animals and
plants (Fig. 143). It occurs in Drosophila (Huettner, 1924). Further-
more, in several organisms it has been found that the two parental groups
of chromosomes can be distinguished not only in the first embryonal
mitosis but also in several divisions thereafter. ^^ This is especially
evident in hybrids. There is reason to believe that the chromosomes
brought together by the two gametes, although they are intermingled in
the nuclei of the new individual, never actually fuse in such a way as to
lose their essential organization. They are joined with one another in the
reticulum and undergo occasional transfers and exchanges of parts, as will
be shown in subsequent chapters; but this does not involve the complete
mixing of their substance which was once thought to occur. The evident
fact that certain nuclear elements maintain their identity through suc-

32 Wilson and Mathews (1895) on the sea urchin; Just (1912) on Nereis. See
Morgan (19246) and Wilson (1925; p. 1012). The plane of cleavage is associated
with gravity by Giglio-Tos (1926).

" Riickert (1895) and Haecker (1895c) on Cyclops; Conklin (1901a) on Crepidula;
B. G. Smith (1919) on Crypiobranchus.

244 INTRODUCTION TO CYTOLOGY

cessive life cycles in spite of such rearrangements is of the greatest impor-
tance in connection with problems of heredity.

The Centrosome. — Shortly after the penetration of the spermatozoon
into the egg an aster develops in the cytoplasm near the base of the sperm
head, and at the focus of the aster a centriole appears (Figs. 145, 147).
The inclusion of a spermatid centriole near the nucleus during spermio-
genesis and the appearance of the aster and centriole in this general region
after fertilization led to the widely accepted view that the newly appearing
centriole is, in reality, that of the spermatid. Whatever its origin, it
soon divides into two which function in the first cleavage mitosis. These
facts had much to do with the formulation of a theory of fertilization
according to which the egg is not able to undergo division because of the
lack of any centrosome to initiate the process, while the spermatozoon
has a centrosome but not sufficient cytoplasm in which to act. Through
the union of the gametes all the organs necessary for division are brought
together and cleavage proceeds (Boveri, 1887, 1891).

Various other theories regarding the origin of the cleavage centrioles
have been propounded, some workers identifying them with those of the
egg and others deriving them from both egg and sperm (see Wilson,
1925, p. 438). In practically all cases there are gaps in the known history
of these centrioles. It remains to be clearly proved that the cleavage
centrioles are continuous with those of either gamete, although in some
cases such proof is very closely approximated. On the other hand, it has
been shown that the formation of asters with centrioles can be induced in
the cytoplasm by treating the eggs with certain chemicals (see p. 154),
and that such structures, provided they originate near the nucleus, may
divide and function in the cleavage which follows,^* This suggests that
the spermatozoon may carry a substance which brings about centriole
formation by the cytoplasm in normal fertilization. However this may
be, the importance of the centrosome undoubtedly lies in its relation to
cleavage rather than to syngamy.

Cytoplasm and Chondriosomes. — In animals, as in plants, the
evidence in general indicates that the cytoplasm of the male gamete is of
relatively little importance in syngamy. A considerable amount of pater-
nal cytoplasm is introduced in some cases {Ascaris), but in others none at
all can be seen to enter. This is particularly true of such a case as Nereis,
in which the middle piece and the tail remain outside the egg. These
facts are of interest in connection with the suggestion of Meves (1911)
that chondriosomes introduced by the sperm are responsible for the trans-
mission of certain paternal hereditary characteristics. The observed
behavior of these bodies during cleavage^^ does not support the theory.

34 Tharaldsen (1926), Beams (1927).

35 Van der Stricht (1902), Lams (1913), Meves (1914a). See Wilson (1925; p. 412).

SYNGAMY 245

One should not, however, lose sight of the fact that cytoplasm and
chondriosomes are passed from generation to generation through the
egg. As will be pointed out later, much that happens in the embryo
depends upon the constitution of the egg cytoplasm. That which under-
goes development is a complete protoplast; no differentiation occurs
without the combination of nucleus and cytoplasm, both of which are
derived directly from the preceding generation through one or both of the
gametes. The presence of chondriosomes in the egg and sometimes in
the sperm probably indicates the occurrence of certain physiological
processes as it does in other cells. Such processes may influence the
course of differentiation, but there is as yet no adequate evidence that
the chondriosomes act as differential factors of inheritance in any way
comparable to the action of nuclear factors.

Conjugation and Endomixis. — From among the many kinds of
syngamic phenomena in Protozoa^*' a single peculiar example is selected
for description here. Conjugation in Paramoecium, as originally shown
by Maupas (1889), involves a complicated series of nuclear changes.
Wilson (1900) describes these as follows:

... in Paramoecium caudatum, which possesses a single macronucleus and
micronucleus, . . . conjugation is temporary and fertilization mutual. The
two animals become united by their ventral sides and the macronucleus of each
begins to degenerate, while the micronucleus divides twice to form four spindle-
shaped bodies. Three of these degenerate, forming the "corpuscles de rebut,"
which play no further part. The fourth divides into two, one of which, the
"female pronucleus," remains in the body, while the other, or "male pronucleus,"
passes into the other animal and fuses with the female pronucleus. Each animal
now contains a cleavage-nucleus equally derived from both the conjugating
animals, and the latter soon separate. The cleavage-nucleus in each divides
three times successively, and of the eight resulting bodies four become mac-
ronuclei and four micronuclei. By two succeeding fissions the four macronuclei
are then distributed, one to each of the four resulting individuals. In some
other species the micronuclei are equally distributed in like manner, but in P.
caudalum the process is more complicated, since three of them degenerate and
the fourth divides twice to produce four new micronuclei. In either case at the
close of the process each of the conjugating individuals has given rise to four
descendants, each containing a macronucleus and a micronucleus derived from
the cleavage-nucleus. From this time forward fission follows fission in the usual
manner, both nuclei dividing at each fission, until, after many generations,
conjugation recurs.

It was supposed for a long time that conjugation involving an inter-
mixture of nuclear material from two individuals was necessary for the

^See M. Hartmann (1909, 1914), Erdmann (1920), G. Hertwig (1921), and
especially Jennings (1923), Belaf (1922), Kofoid (1923), E. B. Wilson (1925), and
Calkins (1926). For a diagram of conjugation in Paramcecium, see Morgan (1913,
p. 6). Conjugation in Dileptus is described by Visscher (1927).

246 INTRODUCTION TO CYTOLOGY

continued vigor of the race in such animals, and that without a periodic
recurrence of the process the race would become increasingly senescent
and finally die out. The long-continued experiments of Woodruff,
Jennings, and others showed that this is not what happens. Given a
properly regulated environment, these organisms will give rise to thou-
sands of successive generations with no conjugation and no decline in
vigor. The natural conclusion seemed to be that protoplasm does not
necessarily become senescent through continued vegetative activity.

The problem assumed a new aspect with the discovery of endomixis by
Woodruff and Erdmann (1914). In conjugation, as shown above, the
micronucleus in each individual initiates a series of three mitoses, one
of the resulting nuclei passing as a gamete nucleus to the other individual,
where a fusion takes place. Since some of the products of the division of
the fusion nucleus become macronuclei, conjugation involves a replace-
ment of the old macronucleus by material from the micronucleus, as
well as the exchange and fusion of micronuclei. In endomixis, on the
other hand, there is such a replacement but no exchange or fusion. For
example, in Paramcecium aurelia, which has two micronuclei, it is found
that after every 40 or 50 generations (by fission) the macronucleus dis-
integrates in the cytoplasm, while each micronucleus undergoes two
successive mitoses (rather than three). All but one or two of the
resulting nuclei degenerate, those which remain later dividing to produce
the new macronuclei and micronuclei.

The question of whether the race can continue to live without either
conjugation or endomixis has awaited answer for several years. In
Paramcecium aurelia and P. caudatum the periodic recurrence of this
nuclear reorganization is coincident with a rhythmic acceleration in
metabolic activity, which at least in part explains the ability of these
animals to maintain their vigor without conjugation. Furthermore, if
endomixis ceases, the cultures die. But in other species endomixis takes
place in the encysted stage or is lacking altogether, yet the metabolic
rhythms occur and the race continues. This indicates some factor other
than endomixis as the cause of the periodic acceleration of vital activity.
The results of several researches" point to the general conclusion that
neither conjugation nor endomixis is necessary for the continued existence
of the race, although under environmental conditions inducing senile
change both processes have rejuvenating effects.

Endomixis thus resembles syngamy in its stimulative effect on metab-
olism and development, but its possible relation to variation and heredity
is not so clear. There is no evidence that in endomixis there is any
meiotic disjunction of chromosomes in the formation of the degenerating
nuclei; in fact, there are certain indications that in the process of conjuga-

3' Woodruff and Spencer (1924), Spencer (1924), E. L. Moore (1924). See
especially Woodruff (1925), Calkins (1926), and Jennings (1920).

SYNGAMY 247

tion disjunction occurs in the third or gamete-producing mitosis, this
mitosis being the one which is lacking in endomixis. Molecular rear-
rangements doubtless occur, but to what extent these may affect the
constitution or action of the physical basis of heredity remains for
future work to determine.

The Physiology of Fertilization. — The problem of identifying the
physico-chemical changes involved in the activation of the egg has been
attacked through studies of artificial parthenogenesis, as well as through
direct analyses of the chemical constitution of the gametes at these
stages. ^^

In 1899 Jacques Loeb made the important discovery that the parthe-
nogenetic development of certain animal eggs can be artificially induced.
In most cases two successive treatments were found necessary; first, a
brief treatment with sea water containing some permeability-increasing
substance (certain fatty acids, bases, soaps, alkaloids, glucosides, and
foreign blood sera) ; and, second, a longer treatment with hypertonic sea
water, or oxygen-free sea water, or sea water with a trace of KCN, or low
temperature. The first treatment caused the formation of a fertilization
membrane, which seemed to be a condition necessary for continued
development. The critical change was apparently a momentary increase
in surface permeability which set in motion the developmental reactions,
but in most cases the eggs became sickly and died unless given the second
treatment. Loeb concluded that the spermatozoon in normal fertiliza-
tion may carry two substances, one of which produces the necessary
initial surface changes, even when the spermatozoon fails to enter the
egg, while the other in some way acts as does the second treatment in
artificial parthenogenesis. This suggestion seems less plausible in the
light of Just's (1922) discovery, that normal sea-urchin larvse can be
produced by treating the eggs with hypertonic solutions alone.

Loeb thought the sickliness of eggs given only his first treatment to
be due to a continuance of the cytolytic action begun by this first treat-
ment, but F. R. Lillie pointed out the greater probability of the view that
it is due to some internal cause, citing as supporting evidence certain
cytological phenomena observed by Herlant in eggs activated by Loeb's
method. During the healthy period (12 to 24 hours) immediately
following the first treatment, Herlant (1917) observed the following
changes. After the formation of the membrane and a hyaline zone,
the nucleus becomes the seat of a series of conspicuous alterations. The
nuclear membrane disappears, and around the chromosomes there is
formed a one-poled achromatic figure but no amphiaster. The chromo-

38 For general accounts, see Loeb (1913), F. R. Lillie (1919), Lillie and Just (1924),
R. S. Lillie (1923), and Gray (1931). For work on plants, see J. B. Overton (1913)
on Fuciis, Tahara (1927) on Sargassum, and Popoff (1920, 1922, 1931) on somatic
tissues.

248 INTRODUCTION TO CYTOLOGY

somes divide but do not separate. Although the cytoplasm becomes
active, no cytokinesis ensues. The chromosomes then return to the
reticulate condition. This process is repeated several times, the nucleus
increasing in bulk each time, but it soon becomes very irregular and the
egg ultimately breaks down by general cytolysis. The second treatment
in some way gives the egg the capacity to divide regularly. Morgan
(1899) and Wilson had long before shown that such treatment with hyper-
tonic sea water causes aster formation in the unfertilized sea-urchin egg.
Herlant showed that one of these asters and a second aster formed near
the egg nucleus together form an amphiaster, normal division then
ensuing. Thus the breakdown of the egg after the first treatment alone
appears to be related to the absence of a proper coordination of nuclear
and cytoplasmic division. The second treatment produces a regula-
tory effect, partly through aster formation, this resulting in normal
development.

Among other agencies inducing activation in certain cases may be
mentioned high temperature (R. S. Lillie, 1908, 1915; Heilbrunn, 1925a),
carbon dioxide (Herlant, 1920), puncture by needles, allowing gases or
other substances to pass the membrane (Bataillon, 1910, and others), and
release from the vitelline membrane (Heilbrunn, 19206). With respect
to the effect of heat, Heilbrunn (1925a) finds a measurable increase in
viscosity at temperatures inducing artificial parthenogenesis and reiterates
his theory (1915) that all such activating methods produce a gelation or
coagulation in the egg cytoplasm.

F. R. Lillie (1913 et seq.) advanced the theory that the egg is an
"independently activable system," the spermatozoon contributing
neither organs nor substances necessary to activation. "The egg
possesses all substances needed for activation; the spermatozoon is an
inciting cause of those reactions within the egg system upon which devel-
opment depends." As a result of his direct analysis of the gametes during
the fertilization period, Lillie identified a substance in the egg which he
called fertilizin. This substance is present in the egg for a short time
only. Its formation usually begins at about the time of the breakdown
of the germinal vesicle, from which it probably emanates; immediately
after fertilization its production ceases. As a rule, it is only during the
brief period when fertilizin is present that spermatozoa will enter the
egg. Moreover, membraneless egg fragments without fertilizin are not
entered. Hence it seems clear that the entrance of more than one sperma-
tozoon is normally prevented, not simply by the mechanical barrier of the
fertilization membrane which develops when the first sperm enters, but
also by the physiological state of the egg protoplasm itself.

Fertilizin has two effects: it first acts by causing an agglutination of
the spermatozoa at the surface of the egg, and later causes the activation
of the egg. It may thus be said to stand between the spermatozoon and
the activation reactions in the egg. Being present in the egg secretion

SYNGAMY 249

at a certain period, it binds the spermatozoon to the surface of the egg;
and the spermatozoon, without necessarily penetrating the egg at all,
releases the activity of the fertilizin within the egg, this resulting in
development. In brief, the activating substance is already present in
the egg and is not brought to it by the spermatozoon. It may be incited
to activity by the spermatozoon but by other agencies as well. According
to Woodward (1918) and Glaser (1921), the agglutinating material and
the parthenogenetic agent are two distinct substances.

Among other immediate physiological consequences usually following
fertilization may be mentioned: an increase in permeability to oxygen,
CO2, pigments, water, alkalies, vital dyes, and certain other substances;
an increase in the rate of oxidation; an increase in viscosity, centering in
the sperm aster; a rise in electrical conductivity; the loss of fertilizin
(Lillie, 1919). Just (1920) points out that most of these changes are not
incident to the fertilization reaction per se but are primarily changes
bound up with the egg's division.

In this connection one may be cautioned against the assumption that
normal activation is complete when the spermatozoon has gained entrance
to the egg. Morgan (1924/) cites the fact that, if an inseminated egg be
cut into two pieces in such a way that one fragment contains the egg
nucleus and the other the sperm nucleus, only the latter develops; he
therefore emphasizes the inadequacy of theories of fertilization which
terminate with the entrance of the spermatozoon.

Conclusion. — Syngamy is a mutual process: that which undergoes
development following syngamy is a zygote — the fusion product of two
gametes, no matter how dissimilar these may have been in their morpho-
logical and physiological differentiations. Syngamy has two important
results: there is a physiological alteration with profound effects upon the
behavior of the protoplasts concerned, and there is a nuclear reorganiza-
tion which is no less significant. In view of the cardinal importance of
the latter change with respect to current theories of heredity, it should
be remembered that in the syngamic nuclear union two monoploid sets of
chromosomes are brought together and form a diploid complement in the
zygote nucleus; and since every chromosome of this complement divides
equationally in every somatic mitosis throughout the development of the
resulting individual, every nucleus in this individual contains a descendant
of every chromosome originally present in the zygote.^^

As the finer details of syngamy and the significance of its results
become better understood, the aptness of Huxley's (1878) often quoted
simile, in which he compared the organism to "a web of which the warp
is derived from the female and the woof from the male," becomes increas-
ingly striking.

^' Only typical "diploid" organisms are considered here. The phenomena in
"polyploid" organisms are essentially the same except for the number of chromosome
sets present (see p. 339).

CHAPTER XVI

MEIOSIS

No subject in the field of cytology is of greater importance than
meiosis. This is mainly because the meiotic process affords a key to the
explanation of many phenomena of development and inheritance which
would otherwise be quite unintelligible ; in fact, the modern study of the
role of chromosomes in heredity has largely centered about changes in
nuclear constitution which occur at the meiotic period. Meiosis may
therefore be taken as the starting point in our discussion of cytogenetics,
which will be begun in the next chapter.

As pointed out at the conclusion of the preceding chapter, each somatic
nucleus in ordinary diploid plants and animals contains a complement of
chromosomes made up of two intermingled sets descended by division
from those brought together in the previous union of gametes. In meiosis
there is accomplished what has long been referred to as "the reduction of
the chromosomes." This expression has had two meanings. In the
first place, it has meant the change from the zygotic to the gametic
number which occurs at this time; this is haplosis, or "numerical reduc-
tion." In the second place, it has been applied more specifically to the
disjunction of the two members of each pair of corresponding ("homolo-
gous") chromosomes present in the diploid complement, an event which
constitutes the central feature of meiosis.

The Stage in the Life Cycle at Which Meiosis Occurs. — Haplosis
and chromosome disjunction are accomplished during the course of two
nuclear divisions known as the meiotic divisions. Because of its peculiar
appearance the first of these mitoses was termed "heterotypic" by
Flemming (1887), while the second, which was seen to resemble a somatic
division in certain features, was called "homoeotypic." Advances in our
knowledge of meiosis have led most cytologists to drop these terms and
to refer simply to the "first and second meiotic divisions." They are
also called "maturation divisions," especially in the zoological literature.
Since meiosis involves two divisions, the resulting nuclei or cells are
formed in groups of four, or quartets, although it frequently happens that
some members of the quartet do not function. For convenience the two
meiotic mitoses will be referred to frequently in subsequent pages as
I and //.

In the normal life cycle of higher animals meiosis occurs at the time
of gametogenesis (Fig. 148). In the male the two divisions result in a

250

MEIOSIS

251

quartet of spermatids, which then transform into spermatozoa (p. 214).
In the female they result in an egg and three (sometimes only two)
polocytes (p. 213). Each gamete, male or female, thus contains the
reduced, or gametic, number of chromosomes. In bryophytes and
vascular plants meiosis occurs normally during sporogenesis, hence the
spores are formed in quartets. Each spore carries the reduced number of
chromosomes, this number being retained through the development of the
gametophyte and its gametes (p. 204). The conditions found in lower
plants will be summarized toward the end of the chapter.

ANIMAL

Fig. 148. — Diagram of chromosome cycles of animals and plants.

The term meiocyte may be used to designate any cell in which meiosis is
initiated, whatever its origin or position in the life cycle. ^ In higher
animals the meiocytes are therefore the primary spermatocytes in the
male and the primary oocytes in the female. In bryophytes and vascular
plants they are the sporocytes — the microsporocytes and megasporocytes
in heterosporous forms. The immediate products of meiosis, i.e., the
nuclei or cells formed in quartets, may be referred to as gones.

Preliminary Sketch of Meiosis. — Before proceeding with the detailed
description of meiosis it will be advantageous to have clearly in mind
certain general features of the process without the complications which
must be introduced later, and to visualize the more conspicuous differ-

^ Other terms which have been used in this sense are auxocyte (Lee, 1897) and
gonotokont (Lotsy, 1904).

252 INTRODUCTION TO CYTOLOGY

ences between meiosis and mitosis of the somatic type. These points are
illustrated in Fig. 149.

In the division of a somatic nucleus each and every chromosome of the
complement divides longitudinally into two halves which come to lie in the
two daughter nuclei. Both of these nuclei are therefore like the original
nucleus in containing equivalent derivatives of all the chromosomes;
hence somatic mitosis is said to be equational.

In the prophase of the first meiotic mitosis the two members of each
pair of homologous chromosomes approach each other and come into
intimate association; this is known as synapsis. As a result of synapsis
the nucleus contains bivalent chromosomes in the reduced number. ^ At
some period during the prophase it becomes evident that each of the
members of a synaptic pair is double as the result of a longitudinal split-
ting. Hence each bivalent appears not simply double, but quadruple:
it is a tetrad chromosome. The four members of each tetrad, two of them
derived from one synaptic mate and two of them from the other, are
known as chromatids.^ At the close of the first meiotic prophase, there-
fore, the meiocyte nucleus contains the reduced number of tetrads.

In the two meiotic mitoses the four chromatids of each and every
tetrad are distributed (with or without certain alterations) to the four
resulting nuclei. When the tetrads are oriented in the spindle as shown in
the diagram, the two paternal chromatids are separated from the two
maternal ones'* with which they have been in synapsis; this is known as
disjunction, or reduction in the stricter sense. Each two associated
chromatids passing to each pole constitute a dyad. When disjunction
occurs in the first mitosis the second mitosis is obviously equational in
character, since dyads which are then separated into single members are
sister chromatids formed by longitudinal division.

In some cases it is known that tetrads may be so constituted and
oriented in the spindle that they divide (at least in part; see p. 265)
along the plane of splitting in the first mitosis and consequently along
the synaptic plane (disjunctionally) in the second. Both types of division
may occur in the same cell, so that each of the two meiotic mitoses may be
both disjunctional (for some elements in the chromosomes) and equational

2 This is often called "pseudoreduction." Bivalent chromosomes are sometimes
called gemini (= twins). "Homologous" chromosomes in the complement are those
which correspond in function (see p. 272).

^ It is customary, though somewhat awkward, to apply the term "chromosome"
rather indiscriminately to single chromosomes, split chromosomes, univalents, biva-
lents, multivalents, and tetrads. When the two halves (chromatids) of a split
chromosome or the four chromatids of a tetrad separate from one another, each is
then referred to as a "chromosome."

* It is convenient to designate the chromatids in this way because the synaptic
mates are ordinarily derived from the male and female gametes. It will be shown,
further on, that this is not always the case, and that parental derivation is not the
essential feature of "homology."

MEIOSIS

253

ABC CI be

ABC Abe

DIAGRAM COMPARING

SOMATIC MITOSIS WITH

THE MEIOTIC MITOSES

First column: E^u^fionoil
division of a diploid somatic
chromosome complement.

Second column: The melotic
divisions, changing the diploid
to the monoploid stc^te.

abC

ABc

Fig. 149.

254 INTRODUCTION TO CYTOLOGY

(for other elements). Disjunction in I is called "prereduction"; that in
//, "postreduction."

It should be noted that the several tetrads in the first meiotic meta-
phase are arranged entirely at random with respect to the poles toward
which the paternal and maternal members are directed (see Fig. 149).
All of the paternal elements may face one way and all of the maternal ones
the other, or any other possible arrangement may obtain ; apparently this
is wholly a matter of chance.^ Hence the distribution of chromosomes
in meiosis is a random matter so far as their parental derivation is
concerned.

At the close of meiosis each of the four resulting nuclei has a mono-
ploid chromosome group (a set) made up of one chromatid of each of the
tetrads. In other words, the set comprises a longitudinal half of one
member of each of the pairs of homologous chromosomes in the original
diploid complement. Thus meiosis involves two nuclear divisions but
only one chromosomal division. Representing the three pairs of chromo-
somes in Fig. 149 by the letters Aa Bh Cc, it is found that two of the four
nuclei have A and the other two a; two have B and two b; two have C and
two c. It should be readily understood that the random assortment
of the three pairs of parental elements makes it possible for a nucleus
of the quartet to have any one of eight possible combinations: ABC, A Be,
AbC, Abe, aBC, aBc, abC, abc.^

A further point should be noted. Two nuclei having A and a,
respectively, may be considered to differ qualitatively according to the
degree of difference between these chromosomes. If, in the meiocyte
nucleus, the members of this pair are unlike (Aa), two of the quartet
nuclei will differ qualitatively from the other two; whereas, if the members
are alike (A A or aa) in the meiocyte, all of the quartet nuclei will be alike
so far as this pair is concerned. The same holds for all of the pairs.
Were the two members exactly alike in every pair, meiosis could occur
without producing any qualitative differences whatsoever among the
nuclei of the quartet. The essential point to be borne in mind here is that

^ The same would be true of dyads in the second mitosis in cases of postreduction.
Random distribution was first demonstrated with pairs composed of dissimilar mem-
bers in the orthopteran genera Brachystola and Trimerotropis (Carothers, 1913 1917).

^ These statements are made on the assumption that the chromosomes remain
individually intact throughout meiosis. When homologous chromosomes exchange'
portions with one another, as will be shown later, the statements will still hold for a
given small region of a chromosome.

When all of the chromosomes disjoin in / and divide equationally in //, as shown
in the diagram, there are chromosome sets of two types in the nuclei of the quartet,
each type being represented twice. When / is equational for portions of tetrads and
the dyads are not oriented similarly in the two spindles at //, it is possible to have
sets of four types in the quartet. Since the organism usually produces many quartets,
there is abundant opportunity for the production of all possible types.

MEIOSIS 255

each nucleus of the quartet resulting from the meiotic divisions contains
but one member of each homologous chromosome pair, rather than two as
in the meiocyte nucleus. Although qualitative differences among the
four nuclei usually obtain as a result of certain dissimilarities in the
homologous chromosomes, such differences are not always a necessary
consequence of meiosis.

The main points brought out in this section may be summarized provi-
sionally as follows :

In a somatic mitosis each chro7nosome of the com'plement is divided
longitudinally, the halves passing to the daughter nuclei; hence these nuclei are
similar to each other and to the original nucleus: somatic mitosis is equational.

In meiosis each chromosome enters into synapsis with its homologue and
also splits longitudinally; this gives a tetrad chromosome composed of
four chromatids. The four chromatids of every tetrad are distributed to
the four nuclei by the two meiotic mitoses. Each chromosome {or portion of
a chromosome) is thus disjoined from its homologue in one mitosis and
divided equationally in the other.

Each of the quartet nuclei contains a monoploid chromosome set made up
of a longitudinal half of one member of each of the original homologous pairs.
The four nuclei differ qualitatively among themselves to the degree in which
the various chromosomes differ from their respective homologues, and they
furthermore differ from the original meiocyte nucleus in having only half as
many chromosomes.

In the next chapter evidence will be presented to show that meiosis
involves essentially a change from the condition in which both members of
a pair of corresponding genetic units are present in the nucleus to the
condition characterized by the presence of but one. This change may be
accomplished for all of the units at one of the meiotic mitoses, or for some
units at the first mitosis and for others at the second.

Detailed Description of Meiosis. — The literature pertaining to
meiosis is characterized by a sharp conflict of opinion regarding the struc-
tural alterations which take place, especially during the first prophase.
This divergence in interpretation has been both annoying and stimulating,
especially because important theoretical considerations have been
involved. During the past few years some of the long-debated questions
have received generally accepted answers, but other problems have arisen
in their places. On the whole, very substantial progress has been made in
this important field.

In this section we shall describe the successive appearances presented
by the nuclear elements during the process of meiosis. The course of
events is naturally not precisely the same in all organisms, but the follow-
ing account is found to apply very widely, at least so far as essentials are
concerned. In order to avoid confusion it will still be necessary to post-

256 introduction' TO CYTOLOGY

pone consideration of certain problematic matters until later in the
chapter.^

As the prophase of the first meiotic mitosis begins, the reticulum of
the meiocyte nucleus transforms into the diploid number of long and very-
slender threads (leptonema stage) (Fig. 150, 1). These thin threads
represent essentially the chromonemata of the chromosomes. Owing to
their attenuation and the scarcity of enveloping substances they may show
clearly their small chromomeres and other structural details. Their
doubleness is a matter of debate. Although considerable evidence has
been brought forward to show that in some cases at least they are already
split at this time, or even in the telophase of the last premeiotic mitosis,^
the microscope in other cases reveals no trustworthy evidence of double-
ness. The threads may lie without any regular orientation in the nucleus,
or, especially in animals, their ends may be directed toward one side,
forming what has been called a "bouquet."

The leptonema threads now begin to conjugate in pairs (synapsis).
This involves a series of movements which are not well understood but
which in some way bring each chromosome where it can enter into close
union with its homologue in one or more regions {zygonema stage).
Synapsis seems to begin at certain points in the threads, notably at their
ends, and then gradually to extend throughout their length. While this
is in progress the nucleus may show both paired and unpaired threads;
this amphitene condition is well shown in bouquets. During these stages
the threads show a notable tendency to shrink and collapse into a more
or less tight knot under the influence of fixatives. This shrinking is
known as synizesis. In most cases it is obviously an artifact due largely
to inadequate fixation of the karyolymph, but in some a certain amount

^ No attempt can be made in a work of this scope to give a complete summary
and classification of all the interpretations that have been put upon the meiotic
phenomena. Only enough will be presented to afford a starting point for a study of
this complex subject. For a review and criticism of all views expressed up to 1910,
see Grcgoire (1905, 1910). The subject may be followed further in the more recent
general accounts of Agar (1920a), Doncaster (1920a), Tischler (1921-1922), McClung
(1924), Wilson (1925), Belaf (1928), Reuter (1930), and Darlington (1931f/, 1932a).
Useful lists of works on somatic and meiotic mitosis in angiosperms are given by
Picard (1913) and Ruys (1925); see also Schiirhoff (1926).

Meiosis as outlined in the following paragraphs was first described by von
Winiwarter (1900), A. and K. E. Schreiner (1904 et seq.), and Marechal (1904 ei seq.)
for animals; and for plants by Dixon (1895), Gregoire (1904, 1907), Berghs (1904,
1905), Rosenberg (1905, 19076, 1909a), C. E. Allen (19056c), and J. B. Overton
(1905, 1909). Many of the stages have been observed in living cells: see Chambers
(1924, 1925) on Dissosteira, Chodat (1924) on Gymnadenia, Lenoir (1927) on Lilium,
and Belaf (1928) on Chorthippus. Recent detailed accounts of meiosis are cited in
subsequent footnotes.

»W. R. B. Robertson (1919, 1920, 1921, 1931a) and McClung (1924, 1927a,
1928a) on Orthoptera, Kaufmann (1926a, 1931a) and Nebel (1932) on Tradescantia
and Rhoeo. The significance of these cases will be discussed later in the chapter.

MEIOSIS

257

of shrinkage is claimed to be natural. Eventually the synapsis of homol-
ogous threads becomes complete, and the tendency to collapse, which
renders many cytological preparations worthless, is no longer so evident.

6^

(W(3

9 10 11 12

Fig. 150. — Semidiagrammatic representation of the principal stages of meiosis. 1,
leptonema; threads present in the diploid number (6). 2, zygonema; synapsis of homo-
logous chromosomes in progress. 3, pachynema. 4, diplonema; note chiasmata. 5,
diakinesis; chiasmata fewer; matrix developed. 6, metaphase /. 7, anaphase /; tetrads
separated into dyads. 8, telophase /. 9, prophase II; chromatids remain associated
at spindle-attachment regions. 10, metaphase //. 11, anaphase //. 12, telophase //;
each nucleus has the monoploid number (3) of chromatids. The split which is to become
effective in the first postmeiotic mitosis is indicated in portions of the chromonemata in
8-12. Cf. Fig. 54.

The nucleus now contains the reduced number of bivalent threads,
each of which represents two homologous chromosomes in synaptic union

258

INTRODUCTION TO CYTOLOGY

(Fig. 152). These threads soon undergo a marked shortening and com-
monly become noticeably thicker; hence this is called the pachynema
stage. The pachynema threads may lie irregularly in the nucleus, or they
may retain the bouquet type of orientation for a time. In suitable
preparations their bivalent nature is obvious in their distinct doubleness.
Moreover, the chromomeres and other structural features show a close
correspondence in the two synapsed threads: the pairing tends to be
carried out very precisely, part for part. Closer examination, at least

r

a

«^—

m

R

Q JfJ

/

£"

h

Fig. 151. — Stages in first meiotic mitosis in Tidipa. a, zygonema (leptonema threads
synapsing laterally). 6, single pair of zygonema threads, c, pachynema, d, diplonema.
e, early diakinesis. /, late diakinesis. g, diakinesis, showing all of the 12 tetrads, h,
early anaphase, showing tetrads beginning to disjoin into dyads, i, later anaphase.
{After Newton, 1927.) i,Sv

late in the pachynema stage, reveals the fact that each of the synapsed
threads is double as the result of splitting. Hence each late pachynema
thread consists of four chromatids; it is a tetrad. The origin of this split
is very difficult to determine. It is said to appear first during late pachy-
nema or in the immediately following stage by several observers,^ but
others, as already pointed out, find evidence for it at earlier stages. This
latter evidence falls in well with that for the presence of two chromone-
mata in each chromosome in somatic telophases, but it should not be
assumed without adequate evidence that the somatic and the last pre-
meiotic mitoses are in all respects alike.

^ E.g., Newton (1927) and Newton and Darlington (1929) on Tulipa; Darlington
(1929c et seq.) on Hyacinihus, etc.; Belling (1931a6) on Allium and Lilmm; Gelei (1921)
on Dendrocoelum, Janssens (1924) on Stethophyma (Mecostethus); and Huskins (1932)
on Trillium.

MEIOSIS

259

The pachynema now passes into the diplonema stage, so called because
doubleness in the thick threads, if hitherto obscure, now becomes plainly
visible (Figs. 150, 4.; 151, d; 155, a). In each tetrad two of the chromatids
widen out from the other two through the greater portion of their length,
but all four tend to remain together in a characteristic manner in one
or more regions. In passing along a tetrad it is often observed that at
such a region the paired chromatids appear to exchange partners, thus

Fig. 152. — Chromosomes of Zca Mays in prophase of first meiotic division in micro-
sporocyte. a, whole nucleus, showing all of the chromosomes (in closely synapsed pairs).
Chromosome III at upper right; chromosome VI attached to right side of nucleolus;
(c/. Fig. 65); looped over VI is chromosome I. b, chromosome VII; note knobs, c,
chromosome VIII. d, chromosome III. e, chromosome IX. /, chromosome X. Spindle-
attachment regions indicated by arrows. Taken from different preparations and therefore
not strictly comparable as to size. Cf. Figs. 66 and 170. {Photographs by McClintock.)

constituting a chiasma. The origin and fate of these chiasmata are
matters of cardinal importance with respect to the significance of meiosis,
hence they will be discussed in detail in a later special section. During
this stage the threads often appear markedly twisted {strepsinema
condition). It should be noted that a diplonema tetrad which has
several chiasmata, and therefore several successive closed or open loops
in alternating vertical and horizontal planes, may present a false appear-
ance of twisting when viewed under the microscope. During the

260 INTRODUCTION TO CYTOLOGY

diplonema stage the threads become progressively shorter^" and pass
gradually into the stage known as diakinesis, toward the end of which
they become compact bodies lying well scattered throughout the nucleus.

At diakinesis the tetrads differ in several respects from those seen
earlier in the prophase. Their length has become greatly reduced. In
certain cases it has been found that a tetrad may be only one-fifteenth or
one-tenth as long as the leptonema and early pachynema threads from
which it is derived. This shortening, from the time it begins in the early
prophase, involves a number of characteristic alterations which are,
however, not precisely comparable in all organisms. As the pachynema
threads shorten, their small ("ultimate") chromomeres may group into
larger ("secondary") ones (c/. p. 143). Later on, notably as the diplo-
nema stage passes into diakinesis, the matrix becomes conspicuous, giving
the tetrad a smoother contour. At the same time the chromonemata
become more uniform in thickness and may form rather regular spirals
within the matrix. "^^ In rye the chromosome shortens about one-third
between diplonema and metaphase, but the chromonemata retain their
original length by coiling; during metaphase the chromonemata shorten
about one-third while the chromosome length remains unchanged. In
other organisms, notably maize and grasshoppers, the chromonemata at
diakinesis do not form very conspicuous spirals, the chromosome exhibit-
ing a structure resembling that in the pachynema stage more than would
be thought possible after so much shortening. This raises interesting
questions regarding the transfer of materials to and from the chromosomes
during these stages.

The various peculiar shapes assumed by the tetrads at diakinesis are
due mainly to the position of their spindle-attachment regions, which
look as if they were repelling each other, and to the number and position
of their chiasmata. A single interstitial (non-terminal) chiasma gives
the tetrad the form of an X ; a terminal chiasma or association gives a V ;
two terminal ones give an 0 ; other arrangements of chiasmata give other
shapes, as can be readily seen in Figs. 150 to 156. Since long chrome-
somes tend to have more chiasmata than short ones, the small tetrads of
a group are in general simpler in form than the large ones. Moreover,
the number of chiasmata per chromosome tends in many organisms to be
reduced in passing from diplonema to diakinesis, a fact whose theoretical
importance will be touched upon in a later section. Although the type
of tetrad which develops is thus largely due to the chiasmata formed by
the chromonemata, the matrix contributes much to its general appearance.
In some tetrads, notably short ones in animal meiocytes, the matrix is

1" It is here that a "second contraction" stage is often described in accounts of
meiosis.

" E.g., Babcock and J. Clausen (1929) on Crepis, Sax (1930c) on Secale, Taylor
(1931) on Gasteria, and Nebel (1932) on Tradescantia.

MEIOSIS 261

distinct about each of the four chromonemata, so that the whole tetrad is
obviously quadruple (Fig. 154). In other cases (Figs. 151, e; 156) it
appears to form a common mass about any two chromonemata lying
close together and not to divide until the chromonemata are separated
later in meiosis. This means that such chromosomes at diakinesis are
tetrads with respect only to their chromonemata.^- It has now been
shown that each of the four chromonemata in the large tetrads of Zea
(McClintock), Tradescantia (Nebel), and Trillium (Huskins) is longi-
tudinally double in the late prophase or metaphase. This suggests
either that the threads are double before synapsis, or that two splittings
must occur in the meiotic prophase (Huskins, 1932a).

Before proceeding further with the history of the tetrads, mention
should be made of a remarkable phase through which they pass during
the late pachynema and diplonema stages in many meiocytes. During
the prophase of the first meiotic mitosis the cell and its nucleus usually
become considerably enlarged. In case this growth continues well into
the latter part of the prophase, the chromosomes may show a marked
tendency to recede from their compact form toward the more finely
divided condition of the metabolic stage. In the sporocytes of plants
this alteration is ordinarily not noticeable; the diplonema threads may
be irregular in outline, but usually they seem to pass into the diakinesis
stage with little change other than shortening and thickening. In
growing animal spermatocytes this modification of the threads is in
some cases carried much further, so that a characteristic "diffuse stage"
ensues. It is in the much more extensive "growth period" of the animal
oocyte that it is most pronounced. At this time the cell increases
enormously in size and develops most of the differentiation which is to
characterize the egg, and as it does so the pachynema or diplonema
threads become profoundly altered in appearance. They send out
thready processes in all directions, assume an irregular brush-like form,
and lose their basichromatic character partially or completely. These
changes seem to be associated with the metabolic processes concerned
in cell growth. When the growth is completed, the original staining
capacity returns while the chromosomes again assume a compact form
and pass into the diakinesis stage.

The prophase of the first meiotic mitosis comes to a close with the
development of the achromatic figure. If centrosomes are present in the
cell (animal spermatocytes and the meiocytes of certain lower plants),
asters develop about them in the cytoplasm. With or without an inward
shrinking of the nuclear membrane the karyolymph becomes organized
as a spindle figure, as already described (p. 151). The tetrads take up

12 The claim is made, however, that in some cases each of the four spiral chro-
monemata is accompanied by its own individual matrix, the several matrices being in
contact but not continuous (Nebel, 1932; on Tradescantia and Zebrina).

262 INTRODUCTION TO CYTOLOGY

their metaphasic positions with their attachment regions in the equator. ^^
Owing to their compactness and their arrangement in a regular plane,
the tetrads are easily counted at this stage if viewed from a polar direction.
The anaphasic movement begins very soon. Two chromatids of each
tetrad gradually move away from the other two, the movement starting
at the attachment regions. As they diverge, it is observed that the
chiasmata often appear to offer considerable resistance to the forces of
disjunction so that the tetrads may become drawn out into strange
shapes which depend upon the relative positions of the attachment
regions and the chiasmata as well as upon the number of the latter.
Eventually the pairs of chromatids (the dyads) become free and continue
their poleward movement.

Fig. 153. — Plant chromosomes in anaphase /, showing tetrad nature and shapes due
to different locations of spindle attachments. {From the works of Allen, Mottier and
Strasburger.)

During the anaphase the two chromatids of each dyad tend to spread
away from each other except at the spindle-attachment region, even
before the dyads have lost their metaphasic contact (Fig. 153). To what
extent this involves an actual division of the matrix or only a separation
■ of two matrices in contact is not altogether clear in many cases. In much
of the older literature, particularly that pertaining to plants, it was
assumed that this was actually the division of the chromosomes for the
second meiotic mitosis; but it is now evident that even in such cases the
tetrad chromosomes in the first meiotic metaphase are quadruple with
respect to their chromonemata, and that the spreading in the anaphasic
dyads represents merely the divergence of two chromatids developed at a
much earlier stage. As a result of this spreading of the free ends a dyad
with terminal attachment appears as a single V and one with median
attachment as a double V. The division of the attachment region is
presumably completed in anaphase, telophase, or later.

After the two diverging groups of dyads reach opposite poles, each
group usually begins the organization of a telophase nucleus at once. The

13 The suggestion has been made that if the attachment region in each synapsing
chromosome is the last portion to become effectively double, the two chromatids facing
the same pole at this region would be regularly sister chromatids. Whether or not
this is actually the case is not known.

MEIOSIS

263

extent to which the telophasic transformation is carried varies greatly
in different cases. Sometimes what are essentially metabolic nuclei
are formed, but probably more often the changes do not proceed far
enough to render the individual dyads indistinguishable. In extreme
cases, notably certain animal oocytes (Fig. 154), the second mitosis
follows so closely upon the first that the dyads at the close of I, imme-
diately and without any structural change, take their places in a spindle
newly formed for //. The interval between the two meiotic mitoses is
known as interkinesis. Ordinarily the two nuclei at this stage come to be

Fig. 154. — Meiosis and syngamy in Ascaris. A, spermatozoon about to enter egg.
B, spermatozoon inside; first meiotic division in progress. C, first mitosis completed;
first polar body budded off. D, second meiotic division, forming second polar body;
nucleus of spermatozoon below. E, meeting of male and female pronuclei, each with 2
chromosomes. F, first cleavage mitosis, showing 2 paternal and 2 maternal chromosomes.
(After O. Hertwig.)

fairly large, and within them the chromatids appear as somewhat slender,
crooked threads associated in dyads at their spindle-attachment regions
(Figs. 150, 155). Anastomoses may be more or less evident, depending
on the degree of telophasic transformation.

Cytokinesis follows the completion of division I in many meiocytes.
In animals the primary oocyte is thus divided into a secondary oocyte and
a polocyte, and the primary spermatocyte becomes two secondary sperma-
tocytes. In the sporocytes of higher plants cytokinesis may follow divi-
sion /, but in many cases it is delayed until after //, when the sporocyte
is divided simultaneously into four spores (p. 167). In the meiocytes of
lower plants various conditions are known.

264

INTRODUCTION TO CYTOLOGY

In the prophase of the second meiotic mitosis the condensing chromo-
somes appear characteristically in the form of threads or rods, still
associated in dyads at their attachment regions but diverging widely
elsewhere (Fig. 155). They thus present a marked contrast to the
closely parallel halves of split chromosomes seen in a somatic prophase.
By the end of prophase II their matrices have become conspicuous about
their chromonemata, and as the spindle develops they take their places
with their attachment regions in its equator. Often they appear con-

FiG. 155. — Stages in meiosis in Gasteria. a, diplonema. b, dyad in telophase /. c,
interkinesis. d, chromonema in early prophase //, showing doubleness (one chromatid),
e, /, prophase 77; note association of chromatids by spindle-attachment regions, g,
metaphase 77; chromonema doubled in each chromatid, h, late anaphase 77. i, telophase
77. (After W. R. Taylor, 1931.)

siderably longer and more slender than in the first mitosis and hence tend
to resemble somatic chromosomes in this respect. In the anaphase
the two chromatids constituting each dyad move toward opposite
poles, their shapes at this time depending chiefly upon the position of
their attachment regions. After reaching the poles at the end of the
anaphase each of the four groups of chromatids begins the telophasic
organization of a nucleus which passes into the metabolic condition.

Since each chromatid is now a complete and independent chromosome,
it should be evident that each of the four nuclei contains a single mono-
ploid set of chromosomes, the set being composed of one chromatid from

MEIOSIS 265

each of the tetrads seen in the late prophase of the first mitosis. Cyto-
kinesis soon ensues, giving in typical cases four cells (spermatids; egg
and polocytes; spores), each with the reduced, or gametic, number of
chromosomes in its nucleus.

In certain cases evidence has been brought forward to show that the
chromonema in each chromatid at the close of the second meiotic mitosis
is already split "in preparation for" the first postmeiotic division. The
time of origin of this split is difficult to determine. In Gasteria it is
clearly seen in the early prophase of the second meiotic mitosis (Fig.
155, d), and its presence in the anaphase of the first mitosis is suggested.
In Tradescantia it can be seen at this stage, while in Zea it has been
observed in diakinesis.^^ This accords with the evidence that in large
somatic chromosomes the chromonema is longitudinally doubled at least
one mitotic cycle in advance of the anaphase in which separation is to
occur along the plane so marked out (c/. p. 137). Whether or not this is
true of the last premeiotic mitosis in forms with wholly typical meiosis is
still a debated question. We shall revert to this point later in the chapter.

Disjunctional and Equational Division. — It has now been shown that
each tetrad chromosome appearing in the late prophase of the first meiotic
mitosis is formed by the synaptic union of two homologous chromosomes
which in turn are longitudinally split ; and, further, that the four chroma-
tids composing the tetrad at late prophase are distributed to four nuclei
(and cells) by the two meiotic mitoses. From this it would appear that
one of the mitoses must be disjunctional, in that it separates synaptic
mates, while the other is equational, since it separates sister chromatids.
Which mitosis is to be regarded as disjunctional (reductional in the strict
sense) and which as equational?

The four chromatids composing a tetrad are ordinarily similar to one
another in appearance when fully condensed, so that it is difficult or
impossible to determine by direct observation whether the separation in
the first anaphase is along the synaptic or along the equational plane.
It has, however, been found in some cases, notably in certain insects,
that the synaptic mates are sometimes unlike in size and hence form
" heteromorphic " tetrads with two large and two small chromatids.
Observations on the behavior of distinguishable chromosomes of this kind
have made it possible to show that a given tetrad may divide disjunction-
ally in I in some cells but equationally in others, at least in the hetero-
moipiiic region. In certain species there is nevertheless a strong tendency
to behave in one way rather than the other. ^^ Furthermore, since the

" W. R. Taylor (1931) on Gasteria, Nebel (1932) on Tradescantia, McClintock
(unpubl.) on Zea.

1^ Wenrich (1916) on Phrynotettix, McClung (1928a) on Mecostethus, Carothers
(1931) on T rimer otr opts, Mecostethus, and Amphitornis. The behavior of hetero-
morphic sex-chromosome tetrads, summarized by Wilson (1925, p. 753), tends to be
uniform in a given species.

266 INTRODUCTION TO CYTOLOGY

several tetrads in one mitotic figure may behave differently in this respect,
each of the two mitoses in such cases may be disjunctional for some
elements and equational for others. Taking the chromosome comple-
ment as a whole, the disjunction of its homologous elements and the
equational separation of their halves are complete only at the conclusion
of the second mitosis.

As will be shown in subsequent chapters, genetic data yield valuable
evidence bearing on the distribution of chromosomes in meiosis. By such
methods it can be shown, especially when the four products of meiosis can
be followed individually,^^ that some pairs of genetic units segregate in /
while others do so in //. There is evidence which indicates that, although
some portions of a tetrad divide equationally in /, the division tends
strongly to be disjunctional in the neighborhood of the spindle-attach-
ment region." How such a result could be brought about by an exchange
of portions between two non-sister chromatids in the tetrad will be shown
in the following section on the chiasma. Certain observations suggest
either that sister chromatids in the tetrad are more closely associated
at the attachment region than are non-sisters, possibly because this region
divides very late, or that for some other reason the non-sisters {i.e., the
synaptic mates) tend to separate rather consistently in 7. To what
extent this suggestion can be generalized and applied to the markedly
heteromorphic tetrads mentioned above cannot be stated at present.

The Chiasma. — It was once thought by some observers^* that the
two homologous chromosomes entering into synaptic union fused com-
pletely and then split twice along new planes to form the four chromatids
of the tetrad. Subsequent investigation has shown this to be erroneous,
as was claimed from the first by another group of workers. ^^ Modern
cytologists and geneticists are now generally agreed that chromosomes
preserve their essential identity through the period of synaptic associa-
tion, at least so far as concerns those chromonematic elements which are
responsible for their finer morphology and genetic functions.

This statement requires one very important qualification. It is
now known that frequently two of the chromatids in the tetrad exchange
corresponding portions with each other, as originally maintained by
Janssens (1909). Beginning with Morgan (1911a) this "crossing-over"
has been regarded as the mechanism responsible for the frequent recom-

^^ E.g., the four spores of a single quartet in Sphoerocarpos (C. E. Allen, 1924 et
seq.; see 1930a).

" Morgan (1925), Bridges and Anderson (1925), Anderson (1925, 1929), Redfield
(1930).

^^E.g., Vejdowsky (1907), Bonnevie (1906, 1908, 1911), von Winiwarter and
Sainmont (1909), and H. Schneider (1914).

" Berghs (1904, 1905), A. and K. E. Schreiner (1905, 1906), Marcchal (1907),
Gregoire (1907, 1910), Schleip (1906, 1907), Montgomery (1911), J. B. Overton
(1905, 1909), Robertson (1915, 1916), Kornhauser (1914, 1915), Wenrich (1915, 1917).

MEIOSIS 267

bination of characters associated with linked genes (p. 294). That this
interpretation is correct has been rendered practicaDy certain by studies
on pairing chromosomes in which characteristic structural features
were exchanged at the time recombinations were produced (p. 303).
That such exchanges somehow involve the chiasmata observed in the
tetrads from the diplonema stage onward has been strongly suspected
from the first, although much of the evidence has been open to question.
It is the prominent role played by crossing-over in present-day researches
in the field of cytogenetics that now makes it necessary to consider the
chiasma in some detail.

OC ^ ^

Fig. 156. — Bivalent chromosomes (tetrads) in metaphase and early anaphase of first
meiotic mitosis in Vicia faba, showing various numbers of chiasmata. First row: chromo-
somes with subterminal spindle attachment. Second row: longer chromosomes with
median attachment. (After Maeda, 19306.)

As already explained, a chiasma is a region where the four chromatids
appear to trade partners when the tetrad opens out in the diplonema
stage. The number of chiasmata developing frequently varies with
the length of the tetrad.^" In Hyacinthus orientalis, for example, there
are commonly three in the longest tetrads (which may have as many as
six), two in the medium-sized tetrads, and one in the shortest ones. In
Vicia faba (Fig. 156) the commonest numbers are three in the short
tetrads and eight in the long one. They appear to be located more or
less at random in some species, but to be more localized near the spindle-
attachment region in others. ^^ Of considerable significance is the further
fact that in many organisms the number of chiasmata tends to be reduced
as the tetrads develop from the diplonema to the diakinesis stage. ^^ In
Callisia repe7is, for example, the six tetrads show a total of about 25

'"' Darlington (1929c) on Hyacinthus, Maeda (19306) on Vicia. Darlington
(1932a) presents an extended discussion of chiasmata and their supposed significance.

21 At random in Hyacinthus, Fritillaria imperialis, and probably Tradescantia;
localized in Fritillaria meleagris (Newton and Darlington 1929, 1930; Darlington,
1929c, 1930d) and Allium fist ulosum (Levan, 1933).

22 Newton (1927) and Newton and Darlington (1929) on Tulipa, Darlington
(1931a) on Primula, Sax (1930cf/) on Secale and Callisia, Belling (1928a, 19316) on
Lilium, Philp and Huskins (1931) on Matthiola, Erlanson (1931a) on Rosa.

268

INTRODUCTION TO CYTOLOGY

chiasmata at diplonema and about 10 at diakinesis. In Rosa the mean
number of chiasmata per tetrad is 2.66 at late diplonema and 1.53 at
metaphase /. As a general rule each tetrad retains at least one chiasma
or a terminal association through to the metaphase, indeed, it is believed
by some observers that the continued association of the dyads at meta-
phase is due primarily to the presence of retained chiasmata rather than to
any mutual attraction existing between them at this time (Darlington). ^^

Fig. 157. — Diagram of a tetrad with one chiasma and chromatid exchange as inter-
preted on the two-plane theory {A) and the one-plane theory {B). The chromatids of
the two conjugated chromosomes are shown in solid lines and broken lines, respectively,
and one end of each is marked with a knob. Spindle-attachment regions indicated by
stippling.

With regard to the origin of the chiasma, there are two principal
interpretations which for convenience may be called the "two-plane
theory" and the "one-plane theory" (Fig. 157).

According to the two-plane theory, ^^ when the four chromatids seen in
the pachynema stage open out two by two to give the diplonema condi-

23 The statistical statements in this paragraph involve the assumption that the
nodes and terminal associations observed in the tetrads actually represent chiasmata.
In many instances this interpretation is probably open to question. In view of
genetic evidence and the behavior of small chromosomes, particular!}' in individuals
with no crossing-over, it seems especially improbable that strictly terminal associa-
tions at metaphase represent chiasmata (Sax, 1930rf; Reuter, 1930; Belling, 19316).

^_* Granata (1910), McClung (1914, 1924, 1927a6), Wenrich (1916), Robertson
(1916), Wilson (1925), Seller (1926), B61af (1928), Sax (1930c, 1932), Newton (1927),
Newton and Darlington (1929), Darlington (1929c; see, however, our footnote 26),
Babcock and J. Clausen (1929).

MEIOSIS

269

tion, the opening is along the synaptic plane in some portions of the tetrad
and along the equational plane in other portions. Where two openings
in different planes meet, the chromatids must "trade partners." When
viewed from a given direction under the microscope two of the chromatids
may appear to cross each other at the resulting chiasma while the other
two continue more or less straight, and they are usually represented thus
in conventional diagrams; but a three-dimensional model makes it clear

"■>;x_-

B

y^

T

""--'*v«^-/'

D

Fig. 158. — A, tetrad with three chiasmata (abc) as interpreted on the two-plane theory.
Two of the chiasmata are shown yielding chromatid exchanges (a'b'), while the third (c)
separates in anaphase (third figure) without exchange. B, similar tetrad as interpreted
on the one-plane theory, with terminalization: chiasma a has been terminalized to a', b has
been moved to b', and c has been terminalized to c'. C, D, tetrads disjoining without
chromatid exchange (two-plane theory). Spindle-attachment regions indicated by
stippling.

that all of the chromatids may be equally bent, the angle of view determin-
ing which two appear to be crossed. If, however, there is a twist of
the tetrad at the chiasma, two chromatids may be crossed and in contact
while the other two are not. When opening out begins at a number of
points, a diplonema tetrad may appear as a series of rings in alternating
vertical and horizontal planes (Fig. 158, A).

The fate of the chiasma as meiosis proceeds beyond the diplonema
stage may be variously conceived on the basis of the two-plane theory.
The four chromatids might contract to the diakinesis condition and move
apart in the first anaphase without undergoing any exchange of portions
(Fig. 158, C, D). On the contrary, the continued opening out of the
tetrad in the diplonema stage and early diakinesis might impose such

270 INTRODUCTION TO CYTOLOGY

strains upon two of the chromatids, especially those crossed and in con-
tact, that they would find it easier to break at the point of greatest strain
than to separate unbroken (A in Figs. 157 and 158). In this way they
would exchange equivalent portions. ^^ Such a process would also result
in genetic recombination as well as in a reduction in the number of
chiasmata. It has been suggested further that such an exchange between
chromatids might be caused by the resistance of chiasmata to the forces
which draw the tetrads apart into dyads at anaphase.

The one-plane theory-^ is essentially the "incomplete chiasmatypy" of
Janssens. According to this view, the openings between the chromatids
in the diplonema stage are all in the synaptic plane: the portions of two
chromatids running closely parallel in any region when the tetrad first
opens are always sisters {i.e., two formed by splitting of one) (Figs.
157, B; 158, B). Hence, in order to account for the characteristic
arrangement of the four chromatids at the chiasma, it is necessary to
assume that an exchange of portions between two of them must have
occurred at this point. In other words, chiasmata regularly indicate
crossing-over. How such an exchange could occur in the pachynema
tetrad before its opening out is an unsolved problem."

To account for the reduction in the number of chiasmata observed
between diplonema and late diakinesis, Darlington postulated a process
called ''terminalization."-^ This is a movement of the chiasmata away
from the spindle-attachment region toward the ends of the tetrad, the
four threads closing ahead of the moving chiasma and opening in the
other plane behind it (Fig. 158, B). The single terminal association
remaining in many tetrads at late diakinesis is accordingly regarded as a
"terminal chiasma, " that is, one which has reached the end of the tetrad.

2^ According to the hypothesis of Sax (1930c) a partial twisting of the tetrad bi'ings
two of its chromatids into close contact, the strains set up b}^ further twisting or
unequal contraction causing a break at the point of contact. The same result could
be accomplished by the forces opening the tetrad without twisting and contact, pro-
vided the paired threads were meanwhile held strongly in synapsis close to the chiasma
on either side, for there is evidence that broken ends of chromosomes have a tendency
to reunite (McClintock, 1932c).

25 Janssens (1909, 1924), Belling (19276 et seq.), Darlington (1930c et seq.; cf.
our footnote 24, p. 268), Maeda (1930a6).

27 According to the hypothesis of BeUing (19316, 1933), new longitudinal connecting
strands develop between successive daughter chromomeres formed by division in the
pachynema stage, such strands forming at half-twists in the threads being so arranged
that they join portions of different chromatids. If the two strands forming the cross
lie in the same plane {i.e., on the same side of the tetrad considered as a regular
bundle of four chromatids), the chiasma is said to be "direct"; whereas, if they lie
in different planes (on different sides of the tetrad), it is said to be "oblique." The
chromatids "crossed" at the chiasma are unchanged, while those running straight are
the exchanged ones.

28 See especially Darlington (19296) on Tradescantia and (1931a) on Primula; also
(1931d, 1932a), where observations of other investigators are interpreted on this basis.

MEWS IS 111

Comparisons indicate that different species often show different character-
istic amounts of terminaUzation, some having almost none while others
show only terminal associations at the end of the prophase.

Cytological and genetical evidence is as yet not sufficiently critical
to permit a confident decision between the two rival interpretations of the
chiasma. Various phenomena have been held to conform better to the
one-plane theory ^^ or to the two-plane theory, ^° but none of them can be
regarded as really decisive. What is needed is a series of observations of
such a nature that less dependence upon personal judgment will be
necessary. Direct evidence has been sought in the behavior of hetero-
morphic tetrads, in which the two chromatids of one synaptic mate
differ visibly from those of the other. In Aloe the opening is regularly
in the synaptic plane in the heteromorphic region (Belling, 19316).
Also, in strains of Zea having large terminal knobs on two of the four
chromatids the opening appears always to be in the synaptic plane at the
ends carrying the knobs. Since such knobs are masses of substance
extending beyond the ends of the other chromatids, and since they show a
decided tendency to stick together at various stages, it is quite possible
that they prevent an opening in the equational plane which might other-
wise occur. Tetrads with more minute grades of heteromorphism,
particularly in non-terminal regions, may be expected to yield more
trustworthy evidence on this point. But even here caution will be
necessary in determining along which plane a tetrad first opens in any
given region, because terminalization, if this occurs in the cases studied,
would separate regions of chromatids originally together and vice versa.
Favorable cytogenetic material should yield an answer to the question
of whether it is chromatid exchange, or terminalization, or both of these
processes, which reduces the number of chiasmata during the later por-
tion of the prophase, and to a considerable extent clarify our notions of
the mechanism of genetic recombination.

Before proceeding further it will be well to point out the fact that
according to either the two-plane or the one-plane theory a tetrad with
one original chiasma and exchange of parts consists of two chromatids
altered by the exchange and two unaltered ones. Since these four
chromatids are distributed to four nuclei by the two meiotic mitoses, two
of these nuclei contain each a chromosome with its original coristitution,
while the other two contain each a chromosome made up of portions of the two
synaptic mates (Fig. 157). This is a point of cardinal importance with
respect to the discussions of genetical problems in subsequent chapters.

2* Configurations in trivalent, quadrivalent, and catenated chromosomes (Belling,
1929; Darlington, 1930crf, 1931e), interlocked tetrads (Belling, 19316; Catcheside,
19316), aspects in pachynema stage (Gelei, 1921; Belling, 1931a).

'" Genetic data in Drosophila (Sax, 1932; Beadle, 1932). See also S. Emerson and
Beadle (1932) and Beadle and Emerson (1932).

272 INTRODUCTION TO CYTOLOGY

It may be added that when there are several chiasmata in a tetrad the
same two chromatids are not necessarily involved at all of them. This
creates a more complicated situation, but it should not be allowed to
obscure the principle just illustrated with a simpler tetrad. The state-
ment emphasized above still holds for the region about any one chiasma
in a more complex tetrad.

It should now be clear why, as a general rule, neither of the two meiotic
divisions is wholly disjunctional or wholly equational in character. Even
if it be held that the first mitosis is regularly disjunctional for the spindle-
attachment regions of the chromosomes, it is evident that this mitosis
must be equational for certain other regions when chiasmata and chroma-
tid exchange are involved. The conclusions stated at page 255 should
now be reread in the light of the foregoing discussion.

The Synaptic Reaction. — The forces bringing about synapsis ordi-
narily begin to manifest themselves in the early prophase of the first
meiotic mitosis and operate for a comparatively brief period. In certain
exceptional cases pairing is evident during the closing phases of the last
premeiotic mitosis and may become so intimate that it looks much like
synapsis. ^^ Pairing has sometimes been reported in the spermatogonia
several cell generations before meiosis.'^ Again, cases are known in
which a tendency to associate loosely in pairs is shown in some measure
in the somatic cells. In extreme examples the pairing occurs directly
after the gametic chromosome sets are brought together in syngamy and
persists throughout development. This is notably true of the Diptera,
as shown especially by Metz (1916a et seq.) (Figs. 71, 196). A tendency
toward such a paired arrangement, but no actual synapsis, has frequently
been reported in somatic cells of plants. Reports of a "late synapsis"
taking place at diakinesis are frequent in the literature. It has been
shown in some such cases^^ that this is probably "a secondary coupling
that has been preceded by a typical synapsis at the usual time and a
subsequent deconjugation" (Wilson).

The two chromosomes which undergo synapsis to form each tetrad are
the corresponding members of the two monoploid sets composing the
diploid complement. They are "homologous" not only because of their
ultimate common origin but also in the sense that they perform similar
roles in the life of the organism. More specifically stated, they somehow
influence similar groups of functional reactions during the development

^^ Asilus (Metz and Nonidez, 1921), Drosophila (Metz, 19266). See also Mont-
gomery (1901) on certain Hemiptera, Sutton (1902) on Brachystola, M. Blackman
(1903, 1905) on Scolopendra, and Dublin (1905) on Pedicellina.

32 Certain Hemiptera and Ascaris (Montgomery, 1904, 1905, 1908, 1910), Alytes
(Janssens and Willems, 1909), Helix and Sagiita (Stevens, 1903; Ancel, 1903), certain
Diptera (Stevens, 1908, 1911), and Pediculus (Doncaster, 19206).

^^ Lepidosiren (Agar, 1911), Rhodites (Hogben, 1920a), Cyanotis (Rau, 1930).
See Wilson (1925, p. 563).

MEIOSIS 273

of the organism and presumably after maturity. Their effects on the
course of development may or may not be precisely the same, but they
differ regularly in certain important respects from those exerted by the
other chromosomes of the complement. As a consequence of this influ-
ence on developmental reactions, the two homologous chromosomes are
responsible in some measure for the appearance of morphological and
physiological characters which are the results of those reactions. Very
little is known concerning the nature of the physical and chemical reac-
tions through which the chromosomes thus influence development, and
still less can be said about additional roles they presumably play in the
metabolic activity of the mature organism. It will be seen in the follow-
ing chapter how researches in the field of cytogenetics have established
firmly the theory that a given chromosome influences the development of a
certain group of characters because it is composed in part of a certain
number of semiindependent elements known as genes. In the terms of
genetics, therefore, homologous chromosomes carry similar groups of
genes.

Ordinarily the two members of a homologous pair are about alike in
size and form, so that in many diploid chromosome complements they
can be readily recognized on this basis (Figs. 67, 69). Sometimes they
exhibit certain differences, some of which can be shown to bear a relation
to differences in function. An extreme case of this is seen in the sex-
chromosome pair in many animals and plants. Moreover, non-homol-
ogous chromosomes are often alike so far as the eye can tell. Hence
it becomes unsafe to depend upon size and form alone as criteria of
homology.

The most reliable cytological criterion of homology is normal synapsis
itself. Caution is nevertheless necessary in using it, for it has been
found that a number of agencies may induce a partial or complete failure
of synapsis (asynapsis) on the part of chromosomes known to be homol-
ogous.^'* The chromosomes may sometimes synapse in the megasporo-
cytes but not in the microsporocytes. Cases are even known in which
asynapsis behaves as a recessive Mendelian character. It should be
pointed out that absence of pairing in late prophase and metaphase alone
should not be accepted unconditionally as evidence of asynapsis, for the
chromosomes may sometimes synapse as usual and then separate before
the end of the prophase. Such absence of pairing may therefore indicate
desynapsis ("deconjugation") rather than true asynapsis (" non-con juga-

^^ E.g., Abnormal temperatures (Belling, 1925a, on Uvularia; Sakamura and Stow,
1926, on Gagea; Stow, 1926, 1927, on Solarium; and others); a recessive Mendelian
gene (Beadle and McClintock, 1928, and Beadle, 1930a, on Zea; Schwemmle, 1928,
on (Enoihera); X-rays (Goodspeed, 19296, on Nicoiiana); nutritional differences in
anthers and ovules (J. Clausen, 19306, on Viola); genetical conditions affecting pairing
in hybrids (Kihara, 1929c; Karpechenko, 1930). See further footnotes in Chap. XIII.
Synapsis is often deficient in plants with more than two homologues (p. 355).

274

INTRODUCTION TO CYTOLOGY

tion")- This point has been especially neglected in many investigations

of meiosis in hybrids.

Recent studies have shown clearly that normal synapsis is due

primarily to an interaction of small homologous portions of the two

chromosomes rather than of the chromosomes as wholes (Gelei, 1921).

Evidence for this is not easy to obtain in normal diploid organisms, but

it is inescapable in certain other types to be dealt with in later chapters.

A striking case is afforded by a strain of maize in which a small portion

of one of the homologues has been "deleted."
At the time of synapsis the normal chromosome
pairs closely with the deleted one along the
regions present in both of them, while the region
having no counterpart in the deleted chromo-
some extends laterally as an unpaired loop (Fig.
182, c). Moreover, it sometimes happens that
an exchange of segments between non-homolo-
gous chromosomes gives rise to a condition in
which two regions of one chromosome are
homologous respectively with two different
chromosomes. Synapsis occurs here between
homologous parts and results in a group of
three or more chromosomes. Again, a small
free fragment of a chromosome tends to synapse
at the proper time with the portion of the
chromosome with which it would have paired.

It is now a workable
hypothesis that the synaptic reaction occurs

synapsed with one of the primarily between "homologous" genes, or

others. All three are closely i, ■■, -ii-- tj. •••j.

associated at the spindle- between substauces m their immediate vicmity,
attachment region. {From a the Synaptic pairing of whole chromosomes thus

preparation by McClintock.) -u • j.i. ix ^ r xi j. x-

being the resultant oi the separate synaptic
reactions of their many constituent genes.

There is reason to believe further that the synaptic reaction is one
which occurs characteristically and fully between two elements only at
one time at a given locus in the chromosomes concerned. This is indi-
cated in an interesting way by synaptic behavior in polyploid plants,
which have more than two chromosomes of a kind.^^ In triploid tulips or
maize, for example, all three of the homologues come near to one another,
but the intimate synaptic union appears characteristically between two
only in a given region (except often at the spindle-attachment point)
(Fig. 159). The third one may be synapsed with either of them at

^^ M. Lesley (1926) on Lycopersicum, Newton and Darlington (19276, 1929)
on Tulipa, Darlington (1929c, 1930c, 1931a) on Hyacinthus and Primula, McClintock
(unpubl.) on Zea.

Fig. 159. — Trivalent chro-
mosome in early meiotic pro-
phase in Zea. Note that any

one of the three members had it never bccomc free.

shows clearly its two chro
matids only where it is not

MEIOSIS 275

another region; or, if the two are synapsed throughout their length, the
third may remain free altogether. The genetic evidence in triploid
Drosophila also indicates such behavior. These phenomena suggest
that the "synaptic force" operating at any region in the homologues is
somehow "exhausted" when two members are intimately synapsed, so
that the third member cannot establish synaptic union with them at
this region. Chemical and electrical analogies naturally come to mind,
but nothing is known about the precise nature of the forces concerned.

That synaptic "attraction" exists primarily between pairs of elements
is suggested further by the opening out of ordinary bivalent tetrads at the
diplonema stage. After the longitudinal doubleness of each synaptic
mate becomes complete and obvious, whatever the time of its inception,
the four chromatids "fall apart" into pairs except at chiasmata, as if the
forces tending to hold the threads together could now operate between
any two of them but not between all four. It is largely upon phenomena
of this character that certain current theories of the origin and causes of
meiosis have been based.

The suggestive hypothesis advanced by Darlington (see especially
193 Ic^ and 1932a) may be stated briefly as follows. During their pro-
phasic contraction, chromosomal threads normally show a strong tend-
ency to be associated in pairs. When the contraction begins in somatic
mitosis the threads are already double as a result of splitting,^" so that
this tendency is already satisfied. In the meiotic prophase, on the con-
trary, the contraction begins before the splitting; hence the tendency to
be double is satisfied by the synapsis of the threads in pairs. After the
paired threads become split in the late pachynema stage, this pairing
becomes superfluous and the tetrad opens out to give the diplonema con-
dition, the split threads remaining associated only at chiasmata until
anaphase. Meiosis is thus conceived to be due to a precocious prophasic
contraction of the chromosomes, this precocity being in some way asso-
ciated with unusual features of the preceding interphase.

An alternative hypothesis is that advanced by Huskins (1932a). This
author accepts the evidence that the chromosomal threads may split one
mitotic cycle in advance of their separation in somatic divisions and
therefore contends that the event which initiates the meiotic process is
the suppression or retardation of splitting during the last premeiotic
division, rather than the precocious contraction in the meiotic prophase.
As a result of such suppression, which is probably due to the peculiar
physiological state of the cells at this period, the leptonema threads of
the meiotic prophase are single until after the contraction and synapsis
begin and must therefore undergo their splitting in the pachynema stage. ^^

^^ Darlington assumes the splitting to take place in the metabolic stage and rejects
the evidence for its earlier occurrence.

^^ As already pointed out, Huskins finds the metaphase tetrads of Trillium to have
four double chromonemata. Hence the synapsing threads are thought to split twice

276 INTRODUCTION TO CYTOLOGY

Huskins points out that those organisms in which the chromosomes are
reported to be split in the premeiotic telophase (p. 256) are either forms
with incomplete synaptic pairing or with no crossing-over, suggesting
that such doubleness is actually a hindrance to normal meiosis. This is
in accord with his observations on the inverse relation between splitting
and pairing in certain speltoid wheats and fatuoid oats.

It is interesting to speculate upon the possible relation between the
synaptic "attraction" and the later "repulsion" which is suggested by the
behavior of the chromatids in diplonema and anaphase, but such specu-
lations have as yet little of a definite nature to support them. Attempts
to identify the immediate causes of meiosis and especially its origin in the
evolution of organisms can yield little of value until many other questions
have been answered by reliable observation.

/

Fig. 160. — At left: Zea chromosome II folded back upon itself in meiotic prophase;
spindle-attachment region near one of the folding points. At right: Zea chromosome VIII
eynapsing with a homologue having a portion of one of its arms inverted; see Fig. 170.
{After McClintock, 1933.)

That synapsis is not solely a matter of gene homology, but is influ-
enced by some condition pervading the nucleus or cell generally, is
indicated by derangements of synapsis caused by abnormal cultural
conditions or by a single Mendelian gene (p. 273). It is also strikingly
shown by the fact that non-homologous parts of chromosomes are some-
times observed in a close association to all appearances like that of homol-
ogous parts (McClintock, 1932a, 1933; on Zea). For example, when an
"interchanged" chromosome synapses with other chromosomes with
which it is in part homologous (pp. 329 to 333), the association which
begins between homologous parts may sometimes extend along the
threads in such a way as to bring non-homologous parts together. Fur-
thermore, a single chromosome normal in other respects may fold back
upon itself at various levels, one portion thus entering into close associa-
tion with the other (Fig. 160). Such association usually disappears
before diakinesis. It is rightly emphasized (McClintock, 1932c) that

in the meiotic prophase, the first of these being the split which was delayed from the
premeiotic mitosis and taking effect in division //, while the second is that taking
effect in the first postmeiotic division.

MEIOSIS 277

synapsis is influenced by a considerable group of factors, including gene
homology, a tendency to form pairs, and peculiar conditions at chromo-
some ends. It is successful and wholly "normal" only when the actions
of the various factors are so correlated as to permit homologies to be
completely satisfied. When the normal relationship of the several
influences is disturbed, as in structurally unbalanced types especially, a
variety of unusual results may be expected.

Not only do these phenomena bear upon our hypotheses of synaptic
attraction, but they raise fundamental questions regarding the role they
probably play in the production of translocations, deficiencies, and other
modifications of the chromosome complement of significance in the
alteration of species. They further serve to emphasize the importance of
a knowledge of the finer morphology of the individual chromosomes in the
interpretation of the phenomena of meiosis. Much that has been written
about meiotic chromosome configurations must be reevaluated in the
light of critical evidence of this kind.

Meiosis in Lower Organisms. — In the foregoing account of meiosis
only higher plants and animals have been considered. This section will
summarize briefly the conditions in lower groups, with special reference
to the stage in the life cycle at which meiosis occurs. The statements
should be compared with those made in the preceding two chapters
regarding the other reproductive phenomena in these groups.

Among the Protozoa, ^^ the matter of chromosome organization and
behavior in many groups is very obscure. In others, however, definite
chromosome numbers and meiotic phenomena essentially like those in
higher organisms have been demonstrated. In most species with a
permanent union of gametes the vegetative stages have the zygotic
chromosome number, and haplosis occurs in connection with gameto-
genesis,^^ as in Metazoa (Fig. 161). In the infusoria, which have a tem-
porary union of cells known as conjugation (see p. 245), meiosis occurs in
the first two divisions of the micronucleus just prior to the formation of
gamete nuclei.''" In a few sporozoa the vegetative stages have nuclei
with the gametic number of chromosomes, meiosis taking place in the
zygote after the fusion of the sexual nuclei.^' In one of these, Aggregata
eberthi, the monoploid set is made up of one long, one short and four
medium-sized chromosomes. There is also genetic evidence that in the
phytoflagellate Chlamydomonas meiosis occurs in the zygote (Pascher,

^ See Minchin (1912), Jennings (1920, 1929), Calkins (1926), and Belaf (1926).

'' E.g., ActinosphcBrium eichhomii (R. Hertwig, 1898b) and Aciinophrys sol (Schau-
dinn, 1896; Belaf, 1922). The paper by Belaf is especially noteworthy.

'^'^ Opercularia (Enriques, 1907, 1908), Chilodon (Enriques; MacDougall, 1925),
Carchesium (Popoff, 1908), Uroleptus (Calkins, 1919), Oxytrichia (Gregory, 1923),
Euplotes (Turner, 1930). For further cases, see Calkins (1926, p. 518).

*^ Aggregata eberthi (Dobell and Jameson, 1915), Diplocystis schneideri (Jameson,
1920).

278

INTRODUCTION TO CYTOLOGY

1916c). Meiosis with spore formation is reported in Paradinium (Chat-
ton, 1927).

Turning to the myxomycetes, it seems that meiosis accompanies the
formation of the spore nuclei, a fusion of nuclei in the Plasmodium having
preceded the process. ^^ In Plasmodiophora brassicce, according to
Prowazek (1905), the Plasmodium breaks up into uninucleate masses

Fig. 161. — Meiosis and syngamy in Actinophrys sol. In each of the copulating indi-
viduals meiosis occurs, after which one of the resulting nuclei unites with a similar one from
the other individual. (From Minchin, after Schaudinn.)

which fuse in pairs and become spores with two nuclei each. These
nuclei in two mitoses give off "reduction nuclei," leaving two sexual
nuclei which then fuse. In this species, therefore, the sexual nuclei are
the only reduced ones in the cycle.

The green algse, formerly supposed to show "zygotic" meiosis exclu-
sively, are now known to have other types also. Three general categories
may be distinguished: haplonts, diplonts, and diplohaplonts.*^ As

^"^Ceratiomyxa fOlive, 1907; Jahn, 1908), Trichia and Arcyria (Kranzlin, 1907),
Didymium (Skupiehski, 1928; genetic evidence).

"Terms introduced by Svedelius (1915, 1931). Haplonts are sexual plants in
which only the zygote has the zygotic chromosome number. Diplonts are sexual
plants in which only the gametes have the gametic number. Diplohaplonts are those
with an alternation of two generations having the gametic and zygotic numbers respec-
tively. For general reviews of reproduction and alternation of generations in the
algse, see Bonnet (1914), Janet (1914), Oltmanns (1922-1923), West (1927), and
G. M. Smith (1933). Davis (1916) gives a convenient summary of the life histories of
the red alga}. Svedehus (1931 ) and Knight (1931 ) discuss and diagram the various life
cycles in Rhodophyceae and Pha;ophyceae, respectively. Dodge (1914) compares the
cycles of red algse and ascomycetes. For further discussions, see Tansley (1912), Buder
(1916a), Kylin (19166), Renner (1916), Fritsch (1916), and Svedelius (1921, 19276,
1931).

MEIOSIS

279

representatives of the first category may be cited species of Spirogyra
(Karsten, 1908; Trondle, 1911), Zygnema (Kurssanow, 1911), Coleo-
chcete (C. E. Allen, 1905c), Cylindrocystis (H. Kauffmann, 1914), Volvox
(W. Zimmermann, 1921), and Ulothrix (I. Gross, 1931; Lind, 1932).
These plants have the gametic chromosome number and undergo meiosis
in the first two mitoses in the zygote (Fig. 162). In a number of other
genera, such as (Edogo7iium, Sphceroplea, and Closterium, in which the
chromosomes are not so well known, it is probable that the same condition
exists, since the zygote upon germination gives rise with considerable
regularity to four cells or nuclei; in some cases {(Edogonium) the four
cells are zoospores.

It has recently been discovered that some of the green algae are
diplonts. Here the somatic cells have the zygotic chromosome number,
which is reduced at the time of gametogenesis, i.e., meiosis is "gametic."

Fig. 162. — Behavior of nuclei and plastids in zygospore of Spirogyra. A, second
meiotic mitosis in S. calospora. B, four nuclei resulting from meiotic divisions in S.
longata. C, degeneration of three of the four nuclei after meiosis in S. longata. D, degenera-
tion of plastids contributed by "male" gamete in S. neglecta. (After Trondle, 1911.)

In this category are the coenocyte genera Codium and Acetabularia
(M. Williams, 19256; Schussnig, 19286, 19306). There is also some
evidence that Vaucheria may have gametic meiosis (Mundie, 1929).

Of even greater interest are the forms with two well-marked genera-
tions in the life cycle. Here the gametes are borne on plants with the
gametic chromosome number and the spores on other morphologically
similar plants with the zygotic number; meiosis occurs at zoosporogenesis.
Known examples are Enteromorpha and Chcetomorpha (M. Hartmann,
1921, 19296, 19306), Cladophora (Schussnig, 19286; Foyn, 1929; Higgins,
1930) and Ulva (Foyn). Furthermore, it appears that in these cases the
sexual plants are dicEcious.

Among the Charales, meiosis in the germinating zygote has been
described for Char a by Oehlkers (1916). In another form at first thought
to be a species of Nitella, Tuttle (1924, 1926) reported haplosis in the
apical cells of the oogonia and antheridia, which would make the vegeta-
tive body a diplont rather than a haplont. In the oogonium the four
cells resulting from meiosis were shown to be strikingly like the egg and
polocytes of animals. On the contrary, Karling (1926) and Lindenbein

280 INTRODUCTION TO CYTOLOGY

(1927) find no haplosis in the antheridia of Nitella gracilis, Chara aspera,
and other representatives of the group.

In the diatoms^^ the bilaterally symmetrical Pennatse and the radially
symmetrical Centricae have been said to be characterized respectively by
gametic and zygotic meiosis, but observations in the latter group are
scanty and at least one exception to the rule is known. In Surirella
saxonica, a pennate form, meiosis occurs at the time of conjugation. In
each individual the nucleus divides to four, reducing the chromosome
number, after which one of the four unites with one from the other indi-
vidual as the cells fuse. The fusion product is an auxospore (Karsten).
In Corethron valdivice, a centric type, the behavior of the nuclei suggests
the occurrence of chromosome reduction in the germination of the zygote,
which in this case is formed by the union of motile gametes (Karsten).
Biddulphia sinensis, however, resembles pennate forms in having gametic
meiosis (Schmidt).

Among the brown algae, many of which exhibit a well-marked alterna-
tion of generations, meiosis occurs in most cases in sporangia on plants
with the zygotic chromosome number. In some groups the spores are
motile,'*^ whereas in others they are non-motile tetraspores.^^ In Fucus
the vegetative body has the zygotic chromosome number, but it produces
gametes instead of spores. Meiosis occurs in the early divisions in the
oogonia and antheridia. "^^ Hence Fucus is a diplont with a life cycle closely
similar to that of animals. It is the opinion of some algologists {e.g.,
Svedelius) that spores have been replaced by gametes in Fucus through a
progressive abbreviation of the gametophytic phase.

Among the red algae^^ two principal conditions are known. In
Scinaia and Nemalion, meiosis occurs in the zygote. There are then
developed gonimoblast filaments and carpospores with the reduced
chromosome number, these spores in turn developing into new plants
which retain this number. In Polysiphonia and several other forms
meiosis does not take place in the zygote, but the carpospores develop into
plants with the zygotic number. Meiosis eventually occurs in tetra-
sporangia on these plants, the resulting tetraspores producing plants
with the reduced number.

^^ See especially Klebahn (1896), Karsten (1900, 1904, 1912), P. Schmidt (1923,
1927a6), Geitler (1927a6c, 1928a6c, 19296, 1931), and von Cholnoky (1928, 1929).

*^ Cutleria-Aglaozonia (Yamanouchi, 1912), Zanardinia (Yamanouchi, 19136),
Ectocarpus (Kylin, 1918), Pylaiella (Knight, 1923), Egregia (Myers, 1928), Stypocaulon
(Higgins, 1931).

« Dictyota (Mottier, 1900; J. Williams, 1904a), Padina (Williams; P. Carter, 1927).
Zonaria (Haupt, 1932) has more than four spores.

*' Yamanouchi (1909) on Fucus; Kunieda (1926) and Okabe (1929) on Sargassum.

^ Yamanouchi (1906) on Polysiphonia; I. F. Lewis (1909) on Griffithsia; Svedelius
(1914a6c, 1915) on Nitophyllum, Delesseria, and Scinaia; Cleland (1919) on Nemalion;
Yamanouchi (1913c, 1921) on Corallina; Mathias (1928) on Callithamnion. For a
summary, see Svedelius (1931).

MEIOSIS

281

Very little is known concerning nuclear behavior in the phycomycetes,
largely because of the minuteness of their nuclei. According to Woycicki
(1927), meiosis in Basidioholus ranarum occurs when the zygote nucleus
divides, three of the four nuclei then degenerating. Kniep (1930)
reports an alternation of gamete-producing and spore-producing plants in
Allomyces javanicus. Here reduction probably occurs in the "resting

*^' - 'laa!

f

Fig. 163. — "Double reduction" in Pyronema confluens. a, prophase in germinating
spore, showing 6 chromosomes, b, vegetative hypha. c, nuclei in tip of ascogenous
hypha, showing 12 chromosomes, d, first meiotic mitosis in ascus, showing 24 chromo-
somes disjoining into groups of 12. e, metaphase of second mitosis. /, metaphase (below)
and anaphase (above) of third mitosis, showing 6 chromosomes passing to each pole.
{After Gwynne-V aughan and Williamson, 1931.)

cells" producing zoospores from which the gamete-producing individuals
arise.

In the ascomycetes meiosis occurs in the mitoses by which the fusion
nucleus in the ascus gives rise to the nuclei of the ascospores. The chief
question at issue concerns the nature of the third mitosis, for ordinarily
eight spores are formed. Most observers'*^ have contended that meiosis
is completed in the first two divisions; but it has also been claimed by
some investigators^" that a further " brachymeiosis " is accomplished in

*8 Maire (1905a) on Galactinia, Faull (1905, 1912) on Hydnoboliles and Laboul-
benia, P. Claussen (1912) on Pyronema, W. H. Brown (1909, 19116) on Pyronema
confluens and Lachnea, Bagchee (1925) on Pusiularia, E. Schultz (1927) on Peziza.
Researches on ascomycetes are reviewed by Atkinson (1915).

^ Fraser (1907, 1908) on Humaria; Fraser and Welsford (1908) on Otidea and
Peziza; Fraser and Brooks (1909) on Lachnea; Carruthers (1911) on Helvetia; Gwynne-
Vaughan and Williamson (1930, 1931, 1932) on Humaria, Pyronema confluens, and
Ascobolus; Tandy (1927) for some asci in Pyronema domesticum.

282

INTRODUCTION TO CYTOLOGY

the third mitosis, such a double reduction being required by the two
nuclear fusions supposed to occur in the life cycle (see p. 230) (Fig. 163).
A compromise is suggested by Tandy, who reports that only some of the
sexual nuclei fuse in the ascogonium, so that the ascogenous hyphse
have both monoploid and diploid nuclei and give rise to asci in which the
definitive nucleus is therefore sometimes diploid and sometimes tetra-
ploid. In diploid asci, meiosis is accomplished in the first two mitoses,
whereas in tetraploid ones three mitoses are required to produce mono-

6 7 8 9 10

Fig. 164. — Meiosis in basidium of Cortinarius cinnamomeus. 1, two nuclei in young
basidium. 2, fusion nucleus. 3-5, prophases of division 7; four bivalents. 6, early
anaphase I. 7, telophase I. 8, telophase //; four chromosomes in each group. 9, four
spore nuclei still in basidium; sterigmata forming. 10, mitosis in one of the four spores.
{After Wakayama, 1930a.)

ploid spore nuclei. An interesting light is thrown upon this problem by
the fact that segregation of Mendelian factors (hence presumably of
homologous chromosomes) in the asci of Neurospora occurs in either of the
first two mitoses but not in the third (B. O. Dodge, 1927 et seq.; Lindegren,
1932, 1933).

In the basidiomycetes, meiosis follows immediately upon the fusion
of nuclei, which ordinarily occurs in the basidium or its homologue.
In hymenomycetes, the fusion nucleus subdivides twice to form the
nuclei of the four basidiospores (Fig. 164), which thus carry the reduced
chromosome number.^^ Cases are known in which no fusion occurs in the
basidium, two spore nuclei being formed without meiosis (Bauch). In

" Sappin-Trouffy (1896), Juel (1898a), Holden and Harper (1903), Maire (19056),
Guilliermond (1910), Kniep (1911, 1913), Levine (1913), Lindfors (1924), Bauch
(1926, 1927), Wakayama (1930o) and others.

MEIOSIS 283

the rusts, meiosis ordinarily occurs as the fusion nucleus in the teliospore
divides to form the four nuclei of the sporidia.^^

Meiosis in bryophytes^^ and vascular plants takes place in the divi-
sions produci-ng the nuclei of the spore quartets.

Conclusion. — From the foregoing account it may be concluded that
meiosis is a process which probably occurs in some form in all nucleated
organisms reproducing normally by sexual means. Haplosis in some
form is obviously a necessary consequence of syngamic nuclear fusion.
The view long current that synapsis is itself a sexual process, the "cul-
mination of fertilization," is, however, rendered less easy of acceptance
by what has been ascertained regarding synapsis (1) in polyploids and
hybrids, where the synaptic mates are often from the same gamete, (2) in
certain parthenogenetic organisms, and (3) between different parts of the
same chromosome, exceptional as this may be. Theorizing on this
subject will be more profitable when more has been learned about the
forces actually concerned in the "attractions" of cells, nuclei, chromo-
somes, and their constituent elements in the life cycles of different
organisms.

The cell in which meiosis is initiated (the meiocyte) may be a sporo-
cyte, a gametocyte, a zygote, an ascus, a basidium, or some other cell;
but whatever the relative position of syngamy and meiosis in the life
cycle, these two cytological crises are events of the highest significance
with respect to the reproduction of the organism. The following chap-
ters will deal with phenomena of heredity exhibited chiefly in successive
generations of plants and animals reproducing sexually; hence, if the
essential features of chromosome behavior in the two cytological crises
are not borne clearly in mind, these chapters will not be intelligible.

62 W. H. Blackmail (19046), Dietel (1911), Fitzpatrick (19186), Colley (1918), and
others. See Arthur (1929), Gaumann-C. Dodge (1928), B. O. Dodge (1929a), and
Jackson (1931) for accounts of the various types of life cycle in rusts.

63 Farmer (1894, 1895) and A. C. Moore (1903, 1905) on Pallavicinia; B. M.
Davis (1899, 1901) on Anthoceros and Pellia; Walker (1913) and Vandendries (1913) on
Polytrichum; Melin (1915) on Sphagnum; C. E. Allen (19176, 1919) and Schacke (1919)
on Sphorrocarpos; Florin (1918a) on Chiloscyphus; Blair (1926) on Reboulia; Heitz
(1928o6) on Pellia; Lorbeer (1924, 1927) on Anthoceros, Sphcerocarpos, and Pellia.
The cytology of bryophytes is reviewed by Motte (1929).

CHAPTER XVII
CHROMOSOMES AND MENDELIAN HEREDITY

Since the beginning of the present century the study of the role of
the chromosomes in heredity has been a major activity in biology. The
primary stimulus for such investigation came in the discovery that the
behavior of the chromosomes through the life cycle, particularly at
syngamy and meiosis, afforded an unmistakable clew to an explanation of
Mendel's laws of inheritance, which were rediscovered in 1900. Before
turning to the special evidence for the chromosome theory of heredity,
however, attention should be given to certain more general matters.

Development and Heredity. — The problem of individual development
and that of racial heredity can never be wholly divorced. It should be
obvious that the course of ontogenetic development depends upon the
organization of the protoplast with which it begins, i.e., upon the type
of protoplasmic system concerned, and also upon the environmental
agencies which influence its action. The problem of development is,
therefore, to ascertain in what manner intrinsic and extrinsic factors,
together composing a single interacting system, operate to produce the
succession of changes which constitute ontogenesis: it is a problem per-
taining primarily to the individual. But any inquiry of this nature soon
leads beyond the individual life cycle to a consideration of the race and
hence to the problem of heredity. The protoplasmic organization upon
which the course of development so largely depends is itself an inheritance
from the past; indeed, the most fundamental fact which cytology has
contributed to the study of heredity is that the protoplasm of successive
generations is genetically continuous. These generations pass through
the same general series of ontogenetic stages and thus tend to develop
similar characters for the reason that the protoplasm with which each
ontogenetic cycle begins is of essentially the same constitution by virtue
of this continuity. Most characters are not literally "transmitted"
but are redeveloped in each generation. Generations may be regarded as
periodic developments of a persistent, though not unchangeable, proto-
plasmic system: the physical basis of heredity is protoplasm.

It is not solely with resemblances that heredity is concerned. The
non-appearance of Mendelian characters in certain generations according
to definite rules, and hence the frequent unlikeness of parent and offspring,
are known to be just as dependent on the operation of intracellular
mechanisms as is the regular appearance of such characters in every

284

CHROMOSOMES AND MENDELIAN HEREDITY 285

generation. Even wholly new variations permanently affecting the
germinal constitution and thus modifying the characters of subsequent
generations are supplementary, rather than opposed, to heredity. In
the general process of heredity we witness the results of processes occur-
ring in a protoplasmic system which, though it maintains a specific type of
organization through successive generations, undergoes minor alterations
which modify the characteristics of the race. Hence it may be said that
heredity is the occurrence of related hut not necessarily identical conditions,
events, or characters in successive generations of organisms as a consequence
of their protoplasmic organization.

From these considerations it follows that the problem of heredity
which confronts the cytologist is that of ascertaining in what respect
resemblances and differences in the characters manifested by successive
generations are correlated with similarities and dissimilarities in the
organization of the protoplasts with which the successive developmental
cycles begin, and how such constitutional conditions arise. Search is
to be made for a mechanism which remains comparatively stable as it
operates through regularly recurring ontogenetic cycles, and yet under-
goes orderly alterations of a kind which will help to account for the
observed phenomena of heredity and variation, as well as to approach
an understanding of evolutionary advance.

The method followed in such studies is mainly that of altering the
cytological constitution of the organism and observing the effect of this
upon the inherited characters. Such alterations may be induced by
various means, but the one which concerns us in this chapter is that of
crossing individuals unlike with respect to cytological or external charac-
ters and noting the results in following generations. In this way valuable
evidence is gained regarding the cytological basis of the inheritance of
those characters in which the individuals may differ.

The Role of the Nucleus. — The hypothesis that "the nucleus of
the cell is the principal organ of inheritance" was suggested by Haeckel
in 1866. Cytological evidence in support of this view was brought
forward by a number of workers who described the behavior of the nucleus
in the various stages of the life cycle, particularly in somatic cell-division,
syngamy, and meiosis (p. 441). Of special interest was the discovery by
0. Hertwig and Strasburger that in animals and plants the two nuclei
which fuse in the process of syngamy are derived from the two gametes
and hence from the two parents. Since it was only in their nuclei that
the gametes appeared structurally alike in higher organisms, and since
inheritance from the two parents in general seemed to be equivalent,
Haeckel's hypothesis was advanced to the rank of a theory, and it was
not long before the nucleus was assigned a monopoly in hereditary
transmission.

286 INTRODUCTION TO CYTOLOGY

Subsequent researches have shown that the characters in which cross-
able organisms may differ and which appear in successive generations
according to Mendehan rules may be "transmitted" equally by the two
parents, and that their development depends in a special way upon the
nuclear organization of the gametes and hence of the zygote (or other
cell with which development begins). This analysis of the role of the
nucleus has been possible because the nucleus contains a relatively small
number of visible bodies, the chromosomes, whose distribution in succes-
sive cycles can be readily traced, so that the effects of their behavior can
be stated in simple mathematical terms. The success of the method
has led some workers to extend the nuclear theory to all heredity, and
to consider the cytoplasm as little more than an adaptive, nutritive
medium for the chromosomes.

It is clear that the nucleus does not deserve this monopoly of the
responsibility for all hereditary phenomena. Cases are known in which
certain characters are obviously due to the constitution of the cytoplasm
and may be influenced unequally by the two parents (Chapter XXV).
Breeding data indicate clearly a causal connection between chromosomes
and Mendelian differences; but since the crosses made must necessarily
be narrow, relatively speaking, they yield little evidence as to the basis
for the inheritance of those characters which are always the same in the
crossed individuals.^ It is to be remembered that in all cases the cyto-
plasm is an essential component of the system which undergoes develop-
ment and produces the characters; in fact, it is mainly in the extra-nuclear
portion of cells that characters are differentiated. The cytoplasm, even
though it may be derived from but one parent, obviously is concerned
in, and conditions, the reactions which eventuate in inherited characters,
and this cytoplasm must not vary in constitution beyond certain limits.
Hence the "physical basis of heredity" in a fundamental sense is the
whole protoplasmic system concerned in development, although the
course of certain developmental reactions and therefore the appearance
of certain characters may be correlated with peculiarities in the organiza-
tion of the nucleus. The nucleus is not an arbitrary determiner of
development: it rather contains a set of conditioning or differential
factors which somehow influence in particular ways the developmental
processes in the protoplast of which they are an integral part. Evidence
for this special influence of the nucleus will now be presented.^

1 Cf. Gates (1915a6), Johanssen (1923), and Winkler (1924).

2 For accounts of Mendelism and the chromosome theory, see Morgan (1919a,
1925), Morgan et al. (1922, 1925), Walter (1922), Sirks (1922), Castle (1924), Wilson
(1925), D. F. Jones (1925), Sinnott and Dunn (1925), Babcock and Clausen (1927),
Goldschmidt (1928a), Stern (1928), Belaf (1928a), Baur (1930), Ekman (1930), Pun-
nett (1927), M. Hartmann (1929a), and Sansome and Philp (1932). Matsuura
(1929) summarizes researches in plant genetics for 1900-1925. English translations
of Mendel's classic paper may be seen in Jour. Roy. Hort. Soc. 26 (1901), Bateson's

CHROMOSOMES AND MENDELIAN HEREDITY 287

Examples of Mendelian Heredity. — Mendel crossed plants of a
pure-bred race of tall peas (6 to 7 feet in height) with plants of a pure-
bred dwarf race (% to 1^ feet in height) (Fig. 165). All the plants of the
first filial generation {F^) were tall like one of their parents. When
these tall hybrids were self-pollinated (or bred to one another), it was
found that the second generation {F^) comprised individuals of the two
grandparental types, tall and dwarf, in the proportion of 3:1. It was
further found that the tall individuals of this generation, though alike
in visible characters, were unlike in genetic constitution: one-third of
them, if bred for another generation, produced nothing but tall offspring,
showing that they were "pure" for the character of tallness; whereas
the other two-thirds, if similarly bred, produced again in the next genera-
tion both tall and dwarf plants in the ratio of 3:1, showing that they
were hybrids with respect to tallness and dwarfness. The dwarf plants
of the second generation {F^ produced nothing but dwarfs when inter-
bred: they were "pure" for dwarfness. From these facts it was evident
that the plants of the F2 generation, although they formed only two
visibly distinct classes, were in reality of three kinds: pure tall individuals,
tall hybrids, and pure dwarfs, these kinds occurring in the ratio of 1:2:1.

It should be understood that the above ratios merely indicate the
probability of obtaining the various types through chance combinations
of gametes. If the population is sufficiently large, the ratio is approached
rather closely; sometimes it is equalled exactly, even in a small population.
The ratios, then, represent a statistical result.

The explanation offered by Mendel for these phenomena may be
stated briefly as follows. The germ cells produced by the pure tall plant
carry something (now termed 2i factor, or gene, represented in Fig. 165 by
T) which tends to make the resulting plant tall. The germ cells of the
dwarf plant carry something {t) causing the dwarf condition. In the first
hybrid generation (Fi) both factors are present, T coming from one
parent and t from the other, but T "dominates" and prevents the
expression of the "recessive" t so that the plants of this generation are all
tall. When the hybrid (Fi) produces germ cells, the two factors for tall-
ness and dwarfness segregate, half of the gametes receiving T and the
other half t. Each gamete therefore carries either one or the other of the
two factors in question but never both; it is "pure" either for T or for t.
This segregation in the germ cells of factors associated throughout the
soma is the central feature of the entire series of Mendelian phenomena
and is often referred to as Mendel's first law. Since the gametes, both
male and female, produced by the hybrid plants of the Fi generation are of
two kinds (half of them bearing T and half bearing t), four combinations

Mendel's Principles of Hetxdity and the first two editions of Castle's Genetics and
Eugenics.

288

INTRODUCTION TO CYTOLOGY

r^

T T

PAREMT5

r^

XX

/\

/\

00 00

CAMtTLS

F,

Tt

T t

GAMtTES

/ \ /\

0000

Fig. 165. — A typical example of simple Mendelian heredity. In a cross between pure
tall and pure dwarf peas, tallness is dominant over dwarfness in the first filial generation
(Fi). In the second filial generation (Fi) tall plants and dwarfs occur in the ratio 3:1.
At the right is shown the distribution of factors for tallness (T) and dwarfness (t) through
these generations. The letters T and t may also be considered as representing a homolo-
gous pair of chromosomes.

CHROMOSOMES AND MEN DELI AN HEREDITY

289

are now possible: a T-sperm with a T-egg, a T-sperm with a ^-egg, a
/-sperm with a T-egg, and a /-sperm with a /-egg. These four combina-
tions result respectively in a tall plant (pure dominant, TT), two tall
hybrids {Tt), and a dwarf plant (pure recessive, //). It is obvious that
in the long run these three types will tend to occur in the ratio of 1:2: 1.
The pure tall individuals and the tall hybrids in F^ are ordinarily
distinguished from each other by the "back-cross test. " It will be readily
seen that when a pure tall plant {TT) is crossed with the pure recessive
type (//), all of the offspring will be tall {Tt); whereas, when a tall hybrid
{Tt)\s crossed with //, half of the offspring will be tall {Tt) and half will be
dwarf (//).

MlRAfilLU JALAPA

Fig. 166.— Inheritance of flower color in Mirabilis. See text. {Adapted from. Correns.)

The Mendelian proportion of hybrids and pure types is perhaps better
illustrated by characters in which dominance is imperfect or lacking.
In Mirabilis jalapa, for example, the hybrids are more or less intermediate
with respect to flower color and are easily distinguishable from the pure
parental types (Fig. 166). When plants bearing pure crimson flowers are
crossed with those bearing pure white flowers, the hybrid plants of the
Fi generation have magenta flowers. When these hybrids are bred
among themselves, the resulting F2 generation comprises plants of three
visibly different types: pure dominants with crimson flowers, hybrids
with magenta flowers, and pure recessives with white flowers; and these
types tend to occur in the ratio of 1 :2:1.^

Mendel's researches on peas included also a study of six other pairs
of heritable characters (now known as allelomorphic pairs), the two

^See further Kiernan and White (1926) on this case.

290 INTRODUCTION TO CYTOLOGY

members of each pair behaving toward each other in a manner similar to
that described above for tallness and dwarfness. He further observed
that the seven pairs were entirely independent of each other in inheritance.
For instance, smoothness and wrinkledness of seeds were allelomorphic
characters, and either of them was transmitted as often with tallness as
with dwarfness in crosses involving both pairs of characters. This
independence of the various pairs of factors was set forth in Mendel's
second law. The law held for the seven principal pairs studied by
Mendel, but it has since been learned that many pairs are not thus
independent, as will be pointed out below.

Terminology. — We may here introduce certain terms prominent in the
literature of genetics. The genotype is the entire assemblage of genetic
factors, or genes, which the organism actually possesses in its constitution,
irrespective of how many of these may be expressed in externally visible
characters; or, it is a class of individuals with the same genetic constitu-
tion. The phenotype is the aggregate of externally visible characters,
irrespective of any other factors, unexpressed in characters, which may be
present in the organism; or, it is a class of outwardly similar individuals.
For illustration: in the case of the tall and dwarf peas there are in the
second generation {F2) three genotypes (with respect to the single char-
acter pair discussed) : TT, Tt, and tt, represented, respectively, by pure
tall plants, tall hybrids, and dwarfs; but there are only two phenotypes:
tall and dwarf, because the complete dominance of tallness over dwarfness
renders the hybrids externally indistinguishable from the pure tall
individuals. Thus one phenotype (tall plants) here includes individuals
with two genotypic constitutions, and the two can be distinguished only
by a study of their progeny. In Mirabilis, however, there are represented
in the F^ generation not only three genotypes but also three phenotypes,
since incomplete dominance renders the hybrids externally unlike either
of the pure forms. Practically, a phenotype is a class of individuals which
look alike, and a genotype is a class of individuals which breed alike
(Castle).

An individual is said to be homozygous for a given allelomorphic
factor pair if it has received the same type of factor from the two parents —
a pea, for example, with the constitution TT or tt. If it has unlike
members in the pair, such as Tt, it is said to be heterozygous. It may be
homozygous for some allelomorphic pairs and heterozygous for others, or
it may conceivably be either homozygous or heterozygous for all of its
factors. Thus an organism with the genotypic constitution AABbcc is
homozygous for the factors AA and cc and heterozygous for Bh. It is
a pure dominant with respect to A and a, a pure recessive with respect
to C and c, and a hybrid with respect to B and b. The phenotypic
appearance of the organism is here determined by the dominant factors A
and B and the recessive c. It is a common practice to represent dominant

CHROMOSOMES AND MEN DELI AN HEREDITY

291

factors by capital letters and their recessive allelomorphs by the corre-
sponding small letters.

The C5rtological Basis of Mendelian Heredity. — The history of the
chromosomes through the critical stages of the life cycle, as more fully
described in the chapters on syngamy and meiosis, must be recalled at this
point (see Figs. 148 and 167). Each parent furnishes the offspring with a
set of individually different chromosomes, the two sets (represented in
Fig. 167 by A BCD and ahcd) together constituting the diploid comple-
ment present in all of the nuclei of the new individual. When gametes
(or spores followed later by gametes in the case of higher plants) are to be
formed by this individual, descendants of the homologous chromosomes of

FEETILIZATIOH
Union of simplex groups

CLEAVAGE
Duplex groups
ABCO abed

SOMATIC DIVISIONS
Duplex groups

Aa Bb Co Dd
SYHAPSI S

GERM CELLS
Simplex groups

Fig. 167. — Diagram of chromosome cycle. (After E. B. Wilson, 1913.)

the two gametic sets conjugate in pairs (synapsis). In one of the meiotic
divisions the two members of each pair disjoin and come to lie in different
nuclei. In the other meiotic division the chromosomes divide equation-
ally. The result of the two meiotic divisions, therefore, is a group of four
gametes (or spores), two of which differ from the other two with respect to
any given chromosome pair : two of them have derivatives of A while the
others have derivatives of a, and so on for all the other pairs. The
chromosomes of the diploid complement are in this way assorted into
monoploid sets, each gamete (or spore) having a set made up of one
member of each of the pairs. This set represents the contribution made
to the following' generation. - ,

It is of importance to recall also that the various pairs of chromosomes
are independent of each other as regards their orientation in' the mitotic
figures and hence in their distribution to the daughter nuclei (p. 254).

292

INTRODUCTION TO CYTOLOGY

As a result a given gamete (or spore) in an organism with four pairs of
chromosomes may have any one of 16 possible monoploid combinations
(Fig. 168)."

It will be observed at once that the distribution of the chromosomes
through the life cycle and successive generations is precisely like that of
the Mendelian factors. Two groups of factors are brought together in
syngamy and are associated in the body of the offspring. In the germ
cells the factors of each allelomorphic pair segregate and pass to different

WW©

Aa Bb

Cc Dd

Fig. 168. — Diagram showing the 16 gametic combinations formed by four independent
heterozygous pairs of factors. {After E. B. Wilson, 1913.)

gametes (or spores). The factors and the chromosomes alike form a
duplex group in each somatic nucleus and a simplex group in each gamete
(or spore) : both chromosomes and factors are aggregated in syngamy and
segregated in meiosis. The precise nature of the parallelism is seen not
only in the factor and chromosome groups as wholes but also in the indi-
vidual pairs. When a single pair of chromosomes, for example Aa in
Fig. 167, is followed through successive cycles, it is seen that there is an
exact parallelism between the distribution of a given homologous pair of
chromosomes and that of a single allelomorphic pair of Mendelian factors.
This is just the condition that should result if the two factors are present

* The possible number of different monoploid gametic combinations and of diploid
zygotic combinations after self-fertilization (or crossing with an exactly similar
individual), when each chromosome pair shows some degree of heterozygosity, may
be readily calculated. Where n = the number of pairs, the number of gametic
combinations is 2" and the number of zygotic combinations is 3". If two individuals
differing in all their chromosomes are crossed, there will be 4" possible kinds of com-
binations in Fi and 10" in F., (see Winge, 19196).

CHROMOSOMES AND MENDELIAN HEREDITY 293

as units of some kind in the two members of the pair of chromosomes. In
the disjunction of these members in meiosis is recognized a cytological
mechanism adequate to accomphsh the factorial segregation underlying
Mendel's first law. In Fig. 165 the symbols T and t may be taken to
represent either a pair of factors or a pair of chromosomes. The same
is true of the letters in Fig. 167.

The cytological basis for Mendel's second law is seen in the inde-
pendent distribution of the various chromosome pairs. Different factor
pairs are independently distributed, as Mendel held, if they are associated
with different chromosome pairs ; but this will not be the case if they lie in
the same pair. The discovery of "linkage," to be described below, has
accordingly made necessary an important qualification of Mendel's
second law, but this has served to show even more strikingly the significant
relation between chromosome behavior and Mendelian heredity.

Mendelian studies are often rendered more difficult by a number of
phenomena which tend to alter the characteristic ratios obtained. It
frequently happens that among sister individuals with unlike genie
combinations some do not proceed far with development, so that an
expected class may be partially or wholly absent from the progeny. The
germination of pollen grains with certain combinations is also sometimes
deficient; even when all the grains germinate it may be found that the
pollen tubes carrying certain combinations outgrow the others and so
reach all or most of the ovules before the slower tubes arrive. Further-
more, there are known a number of "lethal factors" which in certain
combinations retard or prevent development at certain stages, notably in
the gametes and zygotes. As would be expected, occasional abnormal
chromosome behavior results in abnormal ratios also. Because of these
phenomena there is often a marked "developmental selection" which
favors the multiplication of certain genetic types at the expense of others.
In such cases the analysis of the genetic data becomes a more complicated
problem, but in this analysis the fundamental assumptions regarding the
association of chromosomes and factors are found to be adequate.*

Linkage and Crossing-over. — When two pairs of Mendelian char-
acters are due to differential factors located in different chromosome
pairs they are inherited independently, that is, either character of one pair
has an equal chance of appearing with either character of the other pair
because of the independent distribution of the two chromosome pairs.
On the contrary, when their differential genes are located in the same
chromosome pair, certain character combinations tend to appear much

5 Buchholz and Blakeslee (1922, 1927a, 1929, 1930ac, 1932) on Datura pollen
tubes; Buchholz (1922) on developmental selection in general; Brink and MacGillivray
(1924), Brink (19256, 1927a), Brink and Burnham (1927), Mangelsdorf (1929),
Brieger (1926), Nishiyama (1928) and D. F. Jones (1928) on selection among pollen
and male gametes. For lethal factors, see Muller (1917, 1918), Li (1927), B. M.
Davis (1923), and Morgan et al. (1922).

294

INTRODUCTION TO CYTOLOGY

more frequently than others. Such linkage of genes and of characters is
well illustrated in the following case in Drosophila (Fig. 169).

Two well-known characters in Drosophila cultures are black body and
vestigial wings. Each of these is a recessive character, appearing in a
fly only when the gene has been received from both parents in the reces-
sive condition h or v. In the dominant conditions B and V these genes
produce, respectively, normal gray body and normal long wings. When a
fly, homozygous for both dominant factors, is mated to one with all of
the corresponding factors recessive, the offspring all have normal body and

.^/ ^

B^' V

>*r
M

b

V N^

B b

83
%

V

B b

Back- cross

b b

\!^.

Fig. 169. — Linkage in Drosophila. One pair of somatic chromosomes in each fly is
represented by parallel lines; chromosomes in gametes represented by diagonal lines. For
explanation, see text. {Adapted from Morgan et at., 1922.)

wings, because of the dominance of B and V over h and v, respectively.
If the females of this Fi generation are back-crossed to the homozygous
recessive, flies of four types appear in the next generation: gray-long,
black-vestigial, gray- vestigial, and black-long. Those flies with the
original combinations (gray-long and black-vestigial) together comprise
83 per cent of the total number; only 17 per cent are of the new types
(gray- vestigial and black-long). It thus appears that if the two charac-
ters, gray body and long wings, are "contributed" to the offspring by the
same parent, they tend to appear together in the majority of the individ-
uals resulting from the back-cross; in other words, they are "linked."
This is explained by the fact that the differential genes concerned are
located in the same chromosome. The same is obviously true of the
allelomofphic characters, black body and vestigial wings: their genes are

CHROMOSOMES AND MEN DELI AN HEREDITY 295

also carried in the same chromosome. Hence in the Fi fly one chromo-
some of a certain homologous pair carries B V, while the other carries 6 v,
and they tend strongly to continue into the next generation in these
conditions. Were the two pairs of genes in question, B b and V v, carried
by different pairs of chromosomes instead of in the same pair, there would
be no linkage: the two characters, gray and long, and likewise the two
characters, black and vestigial, would then be exhibited together in the
next generation by about 50 per cent of the flies, the chance frequency,
rather than 83 per cent.

We have next to inquire into the origin of the new combinations
appearing in 17 per cent of the flies after the back-cross. In the original
female both chromosomes carry B V; hence every egg has this combina-
tion. The male has & t; in both chromosomes of the pair; hence every
sperm has 6 v. All flies in Fi will therefore have B V in one chromosome
of the pair and 6 ?; in the other; they are heterozygous for both pairs of
genes. When the females of the Fi generation mature their eggs, the two
chromosomes disjoin in meiosis so that half of the eggs carry one and half
the other. If the chromosomes are passed along unaltered, no new
combinations appear in the next generation.

Now let it be supposed that in some of the oocytes'' two non-sister
chromatids exchange portions at some point between the two pairs of
genes in question. This will mean that some eggs will carry unaltered
chromosomes {B V) (b v) while others will carry altered ones (B v) (h V).
Fertilization of these four classes of eggs by sperms carrying b v will
obviously result in flies of four classes, two of which are of new kinds.
This mutual exchange of corresponding portions of homologous chromo-
somes, which may result in such recombinations of linked characters,
is known as crossing-over. The percentage of recombinations appearing
depends upon the proportion of the oocytes in which chromatid exchange
occurs between the two pairs of genes. If it occurs in every oocyte,
50 per cent of the resulting flies should show the recombination (other
things being equal), since two normal and two altered chromatids result
in any one cell. From this it can readily be seen that the frequency
(17 per cent) of recombination in the above example is due to the fact
that the proper chromatid exchange occurred in but 34 per cent of the
oocytes. Such crossing-over between pairs of genes linked in various
degrees is a phenomenon occurring generally in plants and animals,
although in some cases, notably in the males in Drosophila, it is absent.^

* That crossing-over occurs in the primary oocytes rather than in earUer or later
cells is shown by the work of Plough (1917) and Gowen (1929a, 1933).

^ Huettner (1930) reports that in Drosophila males synapsis is incomplete and of
brief duration, but that the meiotic mitoses are otherwise normal. Other works on
meiosis in Drosophila are those of Huettner (1924), Metz (19266), League (1929),
Guyenot and Naville (1929), and Woskressensky and Scheremetzewa (1930).

296 INTRODUCTION TO CYTOLOGY

It should be pointed out that if the original cross in the foregoing
example had been made between a fly homozygous for black-long and
one homozygous for gray-vestigial, these combinations would have
appeared in about 83 per cent of the F2 individuals after back-crossing
to a pure recessive, while gray-long and black-vestigial would have
formed about 17 per cent of recombinations because of crossing-over.
In other words, one combination is as likely to appear as another in a long
series of generations, barring detrimental effects which may attend one
of them. The condition rather arbitrarily called "normal" is usually
the one which is most prevalent in healthy flies; sometimes it is the one
which happens to be observed first.

Because the Mendelian factor pairs so far outnumber the chromosome
pairs, it is evident that each of the chromosomes must carry a consider-
able number of genes. Extensive researches on linkage relations in
various plants and animals have brought out the fact that the genes and
hence the Mendelian characters fall into linkage groups, the members of
each group being linked to one another in various degrees but showing
independent assortment with the members of other groups. Moreover,
when the linkage relations of enough genes are known, it is found that the
number of such linkage groups in an organism is the same as the number of
its chromosome pairs. This is well illustrated by Drosophila melano-
gaster and Zea Mays, the two organisms concerning whose genetic
behavior our knowledge is most advanced. In Drosophila melanog aster
there are four pairs of chromosomes; pair I is rod-shaped, pairs II and III
are longer and bent, and pair IV is very small (Fig. 196). The genes in
this species fall into four linkage groups, and it is noteworthy that three
of the groups are large while the fourth comprises only a very few known
genes (Morgan, Muller, Sturtevant et al.). In Drosophila Willistoni there
are three chromosome pairs and three linkage groups (Metz) and in D.
obscura five pairs and five groups (Lancefield) . In Zea Mays, where there
are normally 10 pairs of chromosomes, 10 linked groups have been
identified (Emerson et al.). In Pharbitis Nil, which has 15 pairs of
chromosomes, there have been identified 10 groups and several independ-
ent factors probably representing the five other groups (Imai, Hagiwara).
It is an interesting fact that Mendel, in his classic researches on Pisum,
which has only seven chromosome pairs, happened to select for special
study seven pairs of characters evidently belonging to as many different
linkage groups and so did not detect the phenomenon of linkage. In
view of such facts, it is possible to look upon a chromosome as a body
containing a definite group of genes which influence the development of a
definite group of characters; but it is not to be concluded from this that
the chromosome in question is solely responsible for these characters.

Assignment of Linkage Groups to Chromosomes. — The first character
found to be definitely associated with a distinguishable chromosome was

CHROMOSOMES AND MENDELIAN HEREDITY 297

that of sex (McClung). In certain insects it was observed that one pair
of chromosomes was markedly different from the others in appearance and
behavior; moreover, the two members were unUke in size, so that they
could be followed through successive generations. Furthermore, males
and females were observed to differ with respect to this chromosome pair,
females commonly having two large ones {XX) while the males had one
large and one small {XY). In some species the Y was absent altogether,
so that the two sexes were characterized by different chromosome num-
bers. The logical conclusion that this chromosome pair exerts a special
influence upon the sex of the organism has since been borne out in a large
number of unisexual animals and plants. In typical cases this "sex-
chromosome" mechanism tends to produce equal numbers of males and
females in each generation. A number of characters other than sex were
seen to be linked with sex in inheritance, so that their genes were assigned
to the sex-chromosomes. Such genes are said to be "sex-linked. " These
topics will be discussed further in Chapter XXIII.

The studies of Morgan and his associates on Drosophila melanogaster
have shown that pair I, which is heteromorphic in the male, has a special
influence on sex determination and carries a considerable group of genes
for sex-linked characters. Pair IV, the smallest of the group, carries
the very small linkage group, as was shown particularly well by occasional
flies which had one too many or too few of these small chromosomes. The
two large linkage groups were accordingly assigned to the two large
chromosome pairs, and it has since been demonstrated that the slightly
longer pair carries the genes of the "third" linkage group (Dobzhansky,
1929a6).

In Zea Mays the 10 chromosomes of the monoploid set (and hence the
10 pairs) can all be distinguished on the basis of their size and structure
(McChntock, 19296, 1932c). It has now been possible to identify each
linkage group worked out by Emerson and his associates with one of
these 10 chromosomes (Fig. 170). This has been accomplished largely
through a study of occasional "trisomic" plants. In such plants one of
the members of the set is present in triplicate in the somatic cells while the
nine others are in duplicate as usual ; hence at the time of meiosis some
spores, and therefore gametes, receive one member of the "trisome"
while others receive two. From this it follows that any characters due to
genes in the triplicate chromosome should appear in abnormal proportions
in successive generations, while other characters should at the same time
appear in normal Mendelian ratios. The method is, therefore, to deter-
mine genetically which characters give "trisomic ratios" when the plants
are bred, and to observe cytologically which chromosome of the .set is
present in triplicate in the somatic cells and in duplicate in some of the
microspores. In this way it was found that in a strain of maize with an
extra chromosome, number X (the smallest of the set), an aleurone color

298

INTRODUCTION TO CYTOLOGY

due to the gene R showed trisomic ratios while characters in other linkage
groups showed ordinary ("disomic") ratios. Hence this gene and other
genes of the same linkage group are carried by the smallest chromosome of
the normal set (McClintock and Hill, 1929, 1931) (Fig. 66, d).

In Datura stramonium, which ordinarily has 12 pairs of chromosomes,
similar studies on trisomic strains have led to the assignment of certain
genes to certain distinguishable chromosomes. In this species each of the
12 chromosomes produces, when present in triplicate, a characteristic

m

TS

"21

•sn

vnr

TL

\

O

P

as

br

f

oin

B

sk
■tsi

cr

de*

V2

oX

^j

J

dl

Goi

bm

msj

ra

msg

tS4

TS51

bv

Y

V5

bal

sa

Pr

PI

gli

Ai

Ta

ys

sm

Bn

ygz
c

sh

VI

12

3'
P9'

Fig. 170. — Diagram of chromosome set of Zea Mays, showing the relative lengths and
the location of the spindle-attachment regions (cross lines) in the 10 members. Inversions
and translocations sometimes cause variations in these features. Chromatic knobs
appearing in one or more of the chromosomes of certain strains are also indicated. Below
the chromosomes are some of the genes which they carry. Cf. Figs. 171, 66, and 152.
(Based on diagrams and data of McClintock, Emerson, and others.)

appearance in the plant which may be readily recognized in the breeding
plot (Belling, Blakeslee).

Such results as these serve to emphasize the fact that the chromosome
set is a definitely differentiated system, each member containing a group
of elements with specific effects upon the course of development and
therefore upon the characters which appear in the organism.

Location of Genes in the Chromosome. — That the genes of a given
linkage group are arranged in a definite linear order in the chromosome
was first clearly shown by the extensive researches on linkage relations
in Drosophila. It was observed that some factor pairs were closely
linked, i.e., crossing-over occurred between them very rarely; whereas,
other pairs were more loosely linked, as shown by the consistently high
frequency of crossing-over between them. The hypothesis was advanced

CHROMOSOMES AND MEN DELI AN HEREDITY

299

that the frequency with which crossing-over occurs is a function of the
actual distance apart of the factor pairs in question (Sturtevant, 1913).
In other words, the farther apart two pairs of genes he, the greater the
chance for a crossover to occur between them. It was assumed that
when flies showed 1 per cent of recombinations after a back-cross, the two
pairs of genes concerned were one "unit" apart in the chromosome, and
so on for other percentages. Certain refinements have since been made in
this hypothesis, but linkage studies in many organisms, together with

inn

O + P 0+ baz O-l-oij

W

m

"vn

VTTT

TX.

26 - -CIS

55
61

98

125

V4*

21 -|-sk

29-- B

br

59

-7Q -L C^

/o- -oin 79

3t
32

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gk

61 --d

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17 • - TSc:

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49 -134

Gen O+ys 0-foil O + Bn 0
4--I1

9 --pr

22 ■ - bt%. . .

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36

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54

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37

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gs

fi

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pgz

mS}
na

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sc

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tn

fi

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re4

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s,

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W7

52 - -wx
60- -V,

CIU2

w„

5

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df

M
l2

u

u
V18

biTifl

sr

Fig. 171. — Linkage map for Zea Mays, showing the arrangement of the genes as deter-
mined genetically. The length of the lines does not indicate actual chromosome length;
cf. Fig. 170. The position of genes marked with asterisks is only approximate. The
genes below the lines are known to belong to the linkage groups indicated, but they have
not yet been assigned to definite loci. {After R. A. Emerson, 1933.)

evidence from translocations of portions of chromosomes (see next
chapter), have given it striking confirmation.

The method of determining the relative position of genes by studying
their linkage relations may now be illustrated with a case in Zea (Fig. 172).
In chromosome pair II there are, among others, the following pairs of
genes = Lg Ig, for liguled vs. liguleless leaves; B b, for more intense vs.
less intense plant color; Sk sk, for normal vs. silkless ears. Between
Lg lg and B h (region a) the percentage of recombination was found to be
28.6, so that these pairs of genes were assigned to loci 28.6 units apart in
the "map" of the chromosomes. Between B b and Sk sk (region |8) the

300 INTRODUCTION TO CYTOLOGY

percentage was 6.9, so that Sk sk had to be placed this number of units
from B h. Either of two positions was possible for Sk sk: to the right
or to the left of B h. Obviously a choice between these positions might
be made if the percentage of recombination between Lg Ig and Sk sk were
known. This turned out to be 34 ; hence Sk sk was assigned a position
farther away from Lg lg than was B b. The relative position of the three
pairs of genes was thus established.

It will be noted that the percentage of recombination between Lg lg
and Sk sk is somewhat less than the sum of the percentages shown in
regions a and /3. This is due to the fact that two crossovers sometimes
occur between widely separated genes in the same chromosome pair.
Thus two exchanges between Lg lg and Sk sk would leave the same genes
linked, one crossover neutralizing the effect of the other. Since all three
gene pairs were studied simultaneously in the above experiment, it was

Lg

6

Sk

,

cc

y3

1-9 b Sk

Fig. 172. — Diagram of linkage relations of certain genes in chromosome II of Zea
Mays. The four lines represent portions of the chromatids of a synapsed pair. See text.
(After data from M. M . Rhoades.)

possible to show that crossing-over had actually occurred simultaneously
in regions a and j3 in 11 out of the 1,392 cases. Because of such "double
crossing-over," the map distances often exceed the percentages of recom-
bination for widely separated genes.

The observed percentages of recombination due to random crossing-
over between the four chromatids of a tetrad approach 50 as a limit since
only two of the four chromatids are altered by any one exchange (Emer-
son and Rhoades, 1933). In well-developed chromosome maps like those
of Zea and Drosophila (Figs. 171, 173) it will, however, be noted that map
distances may exceed 100 units. This is because the map is built up by
adding the distances between closely linked genes and not by observing
directly the recombination percentages for widely separated genes.
It does not take account of such modifying influences as double crossing-
over. Hence the map distances represent actual recombination per-
centages only for rather closely linked genes (not more than about 10
units apart in Drosophila) . It will accordingly be observed that the map
distance between "black" and "vestigial" in the second chromosome is
18.5 units, whereas the percentage of recombination is 17, as shown in
Fig. 169.

CHROMOSOMES AND MEN DELI AN HEREDITY

301

I(X)

0.

o±

O.t

■, 0.3

^06

\

I 1.5
\|3.
13.i
4.5
\ 5.5
\6.9

;^5

137
- - \I6.±
-- \l.t

20.

21.

27.5
T 27.7

n

m

lY

yellow CB)
Hairy wing (W)
scute (H)
Iethal-7'
broad CW)
prune CE)
whiteCE)
face+fE)
Notch CE)
Abnormal CB)
echinus (E)
bifid (W)
ruby (E)
crossveinless (W)
club (W)
delte>^CW)
cut Cw)
singed CH)

torn CB)
lozenge (E)

0.
2.
3.+

telegraph QN)

Star CE)
arista I ess CB)

6.± expanded (vv)

[

0. roughoid CE)

12.t
13.
14.+
16.

Gull Cw)
Truncate Cw)
doichsous Cb)
Streak CB)

-•31.

33. vermillionCE)

36.1 miniature Cw)

36.2 dusky (W)

38.1 furrowed CE)

43. sable Cb)
444 garnet Ce)

54.2 small wing

54.5 rudimentCTryCW)

56.6 forked CH)
Bar CE)
srnall eye
fused (W)
Beadex CW)
Minute-n CH)

cleft Cw;

•35.

• •41.

46.±
48.5
48.7

54.5
57.5
60.+

57.

585

59.

596

62.

65.

dachs Cb)
Ski-E Cw)

Jammed Cw)

Minute-e CH)
black Cb)
Jaunty Cw)

20. olivengent Cw)

26. sepia CE)
26.5 hairy CB)

purple CE)
cinnabar CE)
safranin CE)

-• 44.

- • 64.± pink-wingCEW)

vestigial Cw)
telescope CW)

67.
68.±

35.
36.2

40.1
40.2
40.4
42.2

rose Ce)
cream-IH CE)

Minute-h CH)
tilt Cw)
Dichaete CH)
thread CB)

scarlet CE)

- - 72. Lobe (.£)

74.±
-♦-I- 10. bobbedCH) -1-75.5

gapCw)
curvecf Cw)

• 48. pink CE)
- - 49.7 maroon CE)
50.t dwarf CB)
,50. curled CW)
54.8 Hairy wing supr
58.2 S-tubble (H)
58.5 spinelessCH)
4^. 587 bithoraxCB)
4- '-69.5 bithorax-b
•f . 62. stripe CB)

BIctss Ce)
elta Cw)

•835 fringed Gv)

-90. humpy Cb)

'-69.5
62.

-63.1
66.2

hairless Ch)
ebony Cb)

69.5
70.7
72. band CB)

75.7 cardinal Ce)
76.2 white ocelli Ce)

bent Cw)
shaven CB)
eyeless Ce)
rotated Cb)
Minute-IYCH)

male fertility

Long bristled

4- 100.5 DlexusCw)

911 rough Ce)

93. crumpled Cw)
93.8 Beaded Cw)
94.1 PaintedCw)

male fertility

99.5 arc Cw)

pi. . .

.. 102.+ lethal-Eo.

(105. brown CE)
-'-it05.± blistered Cw) 1007 claret Ce)

. . 106. purpleoid CE) - - 101. Minute CH)

1107.± moruJaCE)
■-(107. speck CB)
-^ 107.5 balloon CW) -»- 106.2 Minute-g Ch)

Fig. 173. — Linkage map for Drosophila melanogaster, showing relative positions of many
of the known genes in the chromosomes as determined genetically. The letters in paren-
theses indicate the portion of the fly in which the characters appear: B, body; E, eye;
H, hairs; W, wings. The arrows indicate positions of spindle-attachment regions. In
the F-chromosome, "Long bristled," which is the normal allelomorph of "bobbed," and
the two factors for male sterility have not been precisely located. In chromosome IV the
genes are all very closely linked. {Adapted from Morgan, Sturtevant, and Bridges (1925)
and Stern (1929)).

302 INTRODUCTION TO CYTOLOGY

It is important to note further that crossovers may not occur with
equal frequency in all portions of the chromosome. For instance, it has
been shown that crossing-over in Drosophila occurs less frequently near
the spindle-attachment region than elsewhere. Of interest in this con-
nection is the observation in Zea that the chromatids, as they open out in
the diplonema stage, tend to remain together and therefore to form fewer
chiasmata near the attachment region (McClintock). From such facts
it follows that the map, although it shows correctly the serial order and
linkage relations of the genes, may not give a true picture of their actual
spacing in the chromosome. We shall revert to this topic in the next
chapter.

In interpreting recombination data it is often necessary to consider a
phenomenon known as interference. If the genes are arranged in a close
linear series in the chromatid, and especially if chiasmata account for
crossing-over, it might be expected that when crossing-over occurs between
any two pairs of genes, the near-by pairs would show no crossing-over,
since the physical conditions might prevent the formation of two chias-
mata or of two breaks very near each other. It has been found that the
data often conform with these expectations. The recombination per-
centage characteristic for genes in a given region of the chromosome is
noticeably lowered when crossing-over occurs at a near-by point. This
interference with crossing-over varies from a high value for closely linked
genes to zero for very loosely linked ones (Muller, Sturtevant, Weinstein).
A further interesting fact is that interference in Drosophila and Zea is
weak across the spindle-attachment region; each arm of the chromosome
behaves more or less independently in this respect. The frequency of
crossing-over has been show^n to be affected in certain cases by age,
temperature, sex, and irradiation.*

Chromatid Exchange as the Mechanism of Recombination. —
Many years ago it was suggested that an exchange of some sort occurs
between homologous chromosomes during the synaptic period.^ Cyto-
logical evidence for an exchange of portions between chromosomes in
certain insects was brought forward by Janssens in 1909. Although this
evidence was not considered conclusive by many cytologists, chromosome
exchange was provisionally assumed to represent the physical basis of
recombination by Morgan and his associates in their successful develop-
ment of the chromosome theory of Mendelian heredity. Many bits of
evidence have pointed toward the correctness of the exchange hypothesis,
but a complete demonstration of the fact that two chromosomes actually
exchange corresponding portions as the genes in these regions are recom-

^E.g., Bridges (1915, 1927, 1929) on age; Plough (1917, 1921) and Stern (1926c)
on temperature; Mavor (19236), Mavor and Svenson (1923), E. G. Anderson (19256),
and Muller (1926) on X-radiation.

9 Correns (1902), DeVries (1903), Strasburger (1905a), C. E. Allen (1905o).

CHROMOSOMES AND MENDELIAN HEREDITY

303

bined has proved difficult to obtain. In 1931 evidence of great cogency
was yielded by both Zea and Droso-phila. In each of these cases the
chromosome pair involved was heteromorphic in two regions and had two
pairs of genes between these regions which could be followed genetically
as the history of the chromosomes was being traced.

The situation in Zea Mays is as follows (Creighton and McClintock,
1931) (Fig. 174). The plant selected for the test had a heteromorphic

ZEA

DROSOPHILA

•

^ ,

cr

- -

■Cr Zr-

c

C c

c

B

■ ■

b b-

V/x-

- ■

wx wx -

wx

?

</

Co
st<

or
7ir

•ed

:hy

1

1

Col

1

or

/01X

ess

y

Non-

roirt
Bar

nation

Non- carnation
Non-bar

1 + j
1 1

1 a
1 1
1 )

^

Female

! ga

metes

\/ Male gametes

Female gametes ' ' Moile gametes

---^

1

y^

X^

c-

c C-

• ■

c c

- ■

c C

■ ■

■c

CI--

Cr-

Cr-

cr-

■

B-

■

b-

B

b-

-

Wx-

■ •

■wx wx

•wx wx-

-wx Wx

- ■

-wx

s

1 !

Colorless Colored Colorless Colored
stcHTchy waxy waxy stoirchy

Carnation Non-carn. Non-cam. Carnation
Bar Non- bar Bar Non-bar

Non- CrossoverTypes Crossover Types

Non- CrossoverTypes CrossoverTypes

Fig. 174. — Diagram of evidence for the view that genetic recombination is due to an
exchange of portions of homologous chromosomes. In Drosophila, only the males among
the progeny are represented; the females also showed some crossover types. The L-shaped
chromosome is the F-chromosome. Further explanation in text. (Based on diagrams of
Creighton and McClintock for Zea, and of Stern for Drosophila.)

chromosome pair. One member of the pair had a large knob at one end
and a portion of a non-homologous chromosome attached to the other
end ; it also carried the gene C for colored endosperm and the gene wx for
waxy endosperm. The other member of the pair had no knob and no
translocated piece, and it carried the gene c for colorless endosperm and
the gene Wx for starchy endosperm. The approximate positions of
these genes in the chromosomes were known. This plant was crossed
with one having two knobless, normal chromosomes carrying c wx.^'^
^^ c wx, c Wx in the original experiment; c ivx, c wx in later crosses.

304 INTRODUCTION TO CYTOLOGY

Among the offspring were four types. In the first type the maternal
member of the chromosome pair in question had neither knob nor trans-
located piece, and the characters of the plants showed that it carried c
and Wx. In the second type the chromosome had both knob and trans-
located piece, and it carried C and wx. The two remaining types had
morphologically altered maternal chromosomes, one of them showing the
piece but no knob while the other had a knob but no piece. Hence the
female parent had furnished gametes of four kinds with respect to the
chromosome in question, crossing-over having resulted in the two altered
chromosomes. The characters of the plants showed that the genes
concerned as well as portions of the chromosomes had been exchanged in
the crossover.

Almost at the same time there appeared Stern's (1931a) report of an
essentially similar situation in Drosophila (Fig. 174). In this case two
special strains were used, one having a portion of the F-chromosome
attached to an X-chromosome, and the other having one of its X-chromo-
somes broken in two. By suitable crossing there was produced a female
with one X-chromosome fragmented and the other carrying the attached
piece of a F; hence this chromosome pair was heteromorphic at two points:
the attachment and the break. The fragmented X carried the genes cr
(for recessive carnation eye-color) and B (for dominant bar eye), while
the other X carried their respective normal allelomorphs. When this
fly was crossed to a normal male, it was observed that among the offspring
some of the male individuals (which receive their X-chromosome from
their mother; see p. 378) carried unaltered X-chromosomes and the
maternal factor combinations, whereas others indicated in their chromo-
some morphology and genetic behavior that an exchange somewhere
between Cr cr and B b had taken place in the maternal X-chromosome
pair. The females also gave similar evidence that an exchange of cor-
responding regions by homologous chromosomes is associated with a
recombination of linked characters.

Among other observations suggesting an exchange of portions of
homologous chromosomes may be mentioned the following. In the
diplonema tetrads of Stethophyma grossum, Janssens (1924) described
breaks or thin regions in two of the four chromatids at the chiasma,
and in some cases two of the four chromatids in anaphase / appeared to be
composite in structure. Darlington (1930c) reported configurations in
the multivalent chromosomes of polyploid Hyaciyiihus which, on the
assumption that more than two homologous chromosomes never associate
closely enough for chromatid exchange in one small region, he could only
interpret on the basis of chromatid exchange. Further evidence was
seen in the peculiar "figure-of-8" configurations and the interlocking
bivalent rings in (Enothera (Darlington, 193 le; Catcheside, 19316). In

CHROMOSOMES AND MEN DELI AN HEREDITY

305

none of these cases was the distribution of genes followed as in Drosophila
and Zea.

The behavior of knobbed chromosomes in Zea has served further to
show directly that in a diploid meiocyte an exchange may occur between
only two of the four chromatids in a given level (Creighton and McChn-
tock, 1932). In the plant in question there was a chromosome having

Goimetes

2ygo+e

■ ■ ■ •
• !!•

Or

■ I ii
• III
II II
1 1 II

Non- cross-over

V

*'^.»-:5

Cross -over

Synoip+Ic Configura+ion La+e Prophoise

Fig. 175. — Diagram of cytological proof in Zea that crossing-over involves two of the four
chromatids. For explanation, see text. {From Creighton and McClintock.)

a large knob at one end and a translocated piece at the other, and a
homologous partner with a small knob and no extra piece (Fig. 175).
While these chromosomes remained attached at the ends after opening
out from their laterally synapsed position, ^^ it could be seen that in some
of the sporocytes one small-knobbed chromatid had exchanged portions
with one large-knobbed chromatid. That it was not whole chromosomes
that had exchanged places was shown by the presence of the translocated
piece and the synaptic relations in the whole complex. For some time
" Thus forming a ring with two other chromosomes because of a reciprocal trans-
location between non-homologous pairs, as explained in Chapter XIX.

306

INTRODUCTION TO CYTOLOGY

there has been at hand genetic evidence that crossing-over usually, if not
always, involves only two of the four chromatids at a given locus, and
it has also been shown that the same two chromatids are not always
involved in all the crossovers in one tetrad. ^^ Recent data from Droso-
phila indicate further that crossing-over occurs only rarely, if at all,
between sister chromatids. ^^

Mendelism in Monoploid Plants. — The principles enunciated by
Mendel were based on phenomena observed in organisms with diploid

A BC

ZY&OTE.

SYNAPSIS

ABC aire

Aa Bt Cc

abc

ntioTic niTOSLs

Fig. 176. — Diagram illustrating chromosome cycle of plant with monoploid (haploid)
body. Owing to independent orientation of the several chromosome pairs in the meiotic
mitoses, a given monoploid individual may have any one of eight possible chromosome
assortments when there are three pairs of chromosomes.

somatic nuclei and monoploid gametes. Since that time most genetic
investigations have been carried on with such organisms. It will now
be of interest to see how the same principles hold in the case of organisms
having the monoploid number of chromosomes in their somatic nuclei.
Genetic work of this nature has been done with haplonts (in which only
the zygote is diploid; p. 278) and with the gametophytes of diplohaplonts,
especially among bryophytes.

The chromosome cycle of a haplont (e.g., certain green algae) is shown
in Fig. 176. The monoploid plants produce monoploid gametes which

12 Bridges (1916), Bridges and Anderson (1925), Anderson (1925c, 1929), L. V.
Morgan (1925), Rhoades (1932), Redfield (1930), Anderson and Rhoades (1931).
" Weinstein (1932), L. V. Morgan (1933).

CHROMOSOMES AND MENDELIAN HEREDITY 307

fuse to form a diploid zygote (oospore or zygospore). When the zygote
germinates, the chromosome number is at once reduced, the monoploid
products of meiosis (here represented as spores) giving rise to the indi-
viduals of the next generation. The cycle is the same in the bryophytes,
except for the important fact that the zygote germinates to form a diploid
sporophyte in which meiosis is delayed until sporogenesis (Fig. 217).
In the body of a haplont or of a moss gametophyte, therefore, only one
member of each chromosome pair is present in each nucleus rather than
both members as in the diploid bodies of animals and plant sporophytes.

The expectations based on the chromosome theory of Mendelism are
as follows. Two contrasting " allelomorphic " characters of the monoploid
individuals introduced into a zygote by crossing should segregate at once
in the next generation in the ratio of 1 :1. In these individuals, therefore,
there should be no "dominance," since only one factor of a given pair is
present. Every factor should have an opportunity to produce its full
effect upon the characters. With respect to a given pair of characters,
diploid individuals show one genotype in Fi (after pure types are crossed)
and three in F2, whereas monoploid ones show two in every generation.

In the moss genera Funaria and Physcomitrium, von Wettstein^"*
studied the progeny of crosses between types differing in various pairs of
contrasting gametophytic characters and found that such characters
segregate 1:1 in the next generation. For example, when two types
differing in leaf form were crossed, the spores from the hybrid capsule
produced gametophytes of the two parental types in equal numbers.
The sporophytic characters (form and color of capsule) were inherited
as would be expected in diploid individuals. Von Wettstein was able
to show that the segregation of the factors for the gametophytic characters
takes place in each sporocyte: two spores of a quartet produce one type
of gametophyte and two produce the other. This clearly indicates a
segregation in one of the meiotic divisions.

In the liverwort, Sphcerocarpos Donnellii, C. E. Allen^^ has shown that
the gametophytic character "polycladous" segregates from its allelo-
morph "typical" nearly 1:1 in the first gametophyte generation after a
cross, and that two spores of a quartet produce one type and two the
other. The same holds for the character "tufted." Both characters are
independent of sex, which had formerly been shown to be inherited in the
same manner (p. 382). Hence the spores produced by a single hybrid
sporophyte give rise, for example, to tufted males, tufted females, typical
males, and typical females. Ordinarily the spores of a single quartet
are of only two of these types, but Allen found a few exceptional cases in

1* Von Wettstein (19216, 1923, 1924a6). Literature on heredity in bryophytes is
reviewed in 1924c. Later papers (1926, 1927, 1928, 1930) deal largely with heredity
in polyploid mosses and the hereditary role of the cytoplasm.

1^ C. E. Allen (1924a6, 1925a, 1926a6c, 1930a6). For a general account, see 1930a.

308 INTRODUCTION TO CYTOLOGY

which all four were present. Whether this should be attributed to an
occasional disjunction of two chromosome pairs in different meiotic
mitoses or to some other cause is not yet clear.

In Spirogyra, a typical haplont, three of the four nuclei formed at
meiosis in the zygospore degenerate. Hybrids between species are of
the two parental types in equal numbers, so far as any one pair of char-
acters is concerned. When two pairs of characters are considered, the
hybrids are of four types; when three are considered, they are of eight
types. These results are in accord with expectations based on the
independent assortment of factors and the equal chance of survival of the
four meiotic nuclei (Transeau, 1919).

The pollen grains of angiosperms, since they normally belong to the
reduced phase of the life cycle, may be expected to show a 1 :1 segrega-
tion of parental pollen characters in each generation if such characters
are due primarily to the constitution of the monoploid nuclei in the grains.
Such a segregation occurs in a number of known instances. ^^ Contrasted
with these are certain other cases ^^ in which pollen characters (chiefly
color and shape) show dominance and behave as sporophytic characters,
which is not surprising in view of the fact that the grains are developed
in the midst of diploid sporophytic cells (tapetum, etc.) and are known
to make use of materials derived from them. Color, for example, may
be due to substances produced in the sporophytic cells and deposited in
all the spore coats irrespective of the genetic constitution of the proto-
plasts they enclose. Pollen may therefore exhibit "sporophytic" as
well as "gametophytic" characters, owing to the intimate association of
the two phases of the life cycle.

The above results of researches on monoploid plants afford definite
confirmation of the chromosome theory of Mendelian heredity as origi-
nally developed through studies on diploid organisms. Very striking
additional confirmation will be brought out in later chapters dealing with
unusual types of chromosome behavior.

The Gene Theory. — It is only for the sake of simplicity that Mende-
lian characters have been treated as if they might be due to single genes,
for this is far from what is actually assumed on the gene theory. It is a
well-established fact that the development of a given character involves
the complemental action of two or more pairs of genes; indeed, it is
doubtless due to the interaction of a very large number of genes, known
and unknown. When a single pair of genes is singled out for study in a
cross, it is done with the understanding that other genes affecting the
results are similar in the organisms used; in other words, the one pair is

^^(Enothera (Renner, 1919a6), Oryza (Parnell, 1921), Zea (Demerec, 1924; Brink
and MacGillivray, 1924; Longley, 1925).

'^ Epilobium, Papaver, and Geranium (Correns, 1900/), 1902\ Lathyrus (Bateson,
Saunders, and Punnett, 1905), Nicotiana (Thomas, 1913). See Correns (19286).

CHROMOSOMES AND MEN DELI AN HEREDITY 309

treated as the differential element in a large system of factors. "The
factorial hypothesis does not assume that any one factor produces a
character directly and by itself, but only that a character in one organism
may differ from a character in another because the sets of factors in the
two organisms have one difference" (Morgan et al., 1915).

Bridges (1923) has described the supposed activity of genes and the
principle of "genie balance" as follows:

. . . the genes of the entire complement act together, since all are liberating
their chemical products into the common cytoplasm. But since the products
of the different genes are different, they take effect in different ways upon the
developing organism. Thus some of the genes will have much effect upon one
character but little effect upon another. Each character will be determined
by all the genes, but in each case most of the effect will be produced by a much
more limited number. Each particular character shows a grade of development
corresponding to the number and effectiveness of the genes that are producing
it. In the case of many of the characters there are genes tending to make the
character less pronounced, and the grade realized is that corresponding to the
equilibrium between these plus and minus modifiers. The directions of modi-
fication for each character are in general quite diverse, and it is somewhat for
the sake of simplicity that they are lumped together as plus and minus modifiers.

It is thus thought that the genes affect the characters mainly by
influencing the course of metabolism and the processes of differentiation
during ontogeny. Very little is known on this subject. It is thought
that a few hundred genes can produce a much larger number of distinct
effects upon characters because they act in different combinations and
probably in different ways at different stages of development. Their
actions are in part responses to changing conditions in the cytoplasm
and external environment, i.e., in the other portions of the system of
which they are a part. Still less is known about the functions of genes
in the mature organism, although a beginning has been made on this
problem.

How the influences of genes are transmitted to the cell or tissue in
which they lie is at present wholly a matter of conjecture. It has been
held that certain products of genie activity are liberated into the cyto-
plasm at the time of mitosis; this is suggested by the time of appearance
of differentiated regions in certain animal eggs (p. 419). It has also been
thought that nucleolar matter so liberated may possibly carry such
products (p. ]20). In this connection it should be remembered that
many tissues undergo a considerable amount of growth and differentiation
and perform their characteristic functions long after all the nuclear and
cell-divisions are completed, which strongly suggests that genes exert
influences upon development and behavior while the nucleus is in the
active metabolic stage.

310 INTRODUCTION TO CYTOLOGY

It is usually assumed as a workable hypothesis that a gene may exist
in two or more allelomorphic states. ^^ It is only when at least two
states are available that the function of the gene can be conveniently
studied in crosses. Hence the genes used in genetic studies and appearing
in chromosome maps are "mutant genes," i.e., genes which in some cases
have become "mutated," or altered from a former condition, so that the
effects of two allelomorphic states can be compared. A large share of
the responsibility for the production of a given character may lie with
uniform and unknown genes.

The term mutation may be used in a general sense for all types of
alteration in the genotype aside from that accomplished by normal
meiosis and syngamy, the types being classified on the basis of the
amount of the substance involved (gene; group of genes or section of
chromosome; chromosome; chromosome set) and the nature of the
process causing the alteration (Bridges, 1923). There is a tendency
among some geneticists, however, to restrict the term to gene mutations.
The hypothesis that a comparatively stable gene may under certain
occasional circumstances (perhaps as it reproduces) undergo a qualitative
change with an effect upon one or more characters underlies much of the
genetic investigation now in progress. It is supposed that such an altera-
tion may involve a single locus or gene ("point mutation") or a group of
linked genes occupying a certain region of a chromosome ("regional
mutation," or "complex mutation"); but it is not clear in many cases
whether the change is strictly a qualitative alteration in the gene, and
therefore a true gene mutation, or a mere derangement of a very small
region of the chromosome.

There is genetic evidence to show that gene mutations may occur at
any place in the organism or stage of the life cycle, but they are most
frequent in the germ cells at or near the meiotic period. ^^ Ordinarily,
therefore, only a few of the many reproductive cells transmit the altered
gene. When, as seems to be true of the majority of known cases, the
mutation is from a dominant to a recessive condition, the effect on the
characters of the diploid organism is not fully manifested until two
such recessive allelomorphic genes are brought together. Mutations
occurring in body cells are known as "somatic mutations." Two of the
most conspicuous results of somatic mutation in plants are bud sports
and chimeras. If the mutation occurs in the meristematic tissue of a
very young bud, the product of the bud — branch, flower, or flower cluster
18 When more than two are known, they are called "multiple allelomorphs." In
Phytodeda, for example, the color of the beetle is affected b}^ such a series of four
allelomorphs: N, R, A, L. Each of these is dominant to any one on its right in the
order stated (Zulueta, 1925).

i» Emerson (1914, 1917, 1922), Eyster (1924), Bridges (1919), MuUer (1920),
Blakeslee (1921), Anderson and Eyster (1928), MacArthur (1928), Gowen (1929),
Demeree (1929d).

CHROMOSOMES AND MENDELIAN HEREDITY 311

— may have a new genotypic constitution and exhibit an appearance
often strikingly different from that of the other branches or flowers of the
plant; hence the term "bud sport." Such a mutation may result in a
chimera, in which a distinct portion of the mature structure, commonly
a sharply defined sector, differs constitutionally and in appearance from
the other portions. Analogous changes occur in animals. Such muta-
tional changes are inherited only if they take place in the lineage of the
reproductive cells.

Many "mutations" in both somatic and germ cells are known to be
due to relatively gross alterations in the chromosome complement. On
the other hand, the nature of the alteration in a true gene mutation is
unknown, since the nature of the gene itself is almost wholly a matter of
conjecture. The literature of genetics contains many interesting specula-
tions on this subject, various comparisons with molecules, radicals,
colloidal aggregates, and enzymes being suggested. Whatever their
nature, most genes appear to have a high degree of stability and are not
easily influenced. So far almost nothing is known about the causes of
natural gene mutation. Many environmental factors appear to have
little or no effect upon the process. Its frequency, which in nature is
very low, can be markedly increased by X-rays and radium and possibly
also by certain other agencies, such as abnormal temperature. ^° Often
the mutations so obtained are qualitatively the same as those occurring in
non-treated material. In certain cases it is apparent that the alteration
is a structural deficiency rather than an actual change of the gene, which
raises an interesting question regarding the real relation of minute defi-
ciencies to what have been regarded as mutations in the gene itself.
Whatever may be the ultimate nature of the change whose effects are
observed, it is probable that many variations which constitute initial
steps in species alteration and evolution originate in this manner.-^

Assuming, as many do, that genes are discrete material particles,
tentative calculations place them well below the limit of visibility with
the ordinary microscope and suggest that they are of the same order of
magnitude as certain large protein molecules. ^^ No worker should claim,
however, that any accurate determination of their size is at present

20 X-rays: Muller (1927, 1928a6, 1929c, 1930a6), Weinstein (1928), Whiting (1928),
Stadler (1928a6c, 1929, 193Ca6c, 19316, 1932), Hanson (1928), Patterson (1928, 1929),
Gowen (19296), Goodspeed and Olson (1928a6), Goodspeed (1930a6c), Oliver
(1929), Patterson and Muller (1930), Whiting (19326) and Timof eeff-Ressovsky (1930).
Earth radiation: Olson and Lewis (1928) and Hanson and Heys (1929). Radium:
Gager and Blakeslee (1927), Stadler (19286), Goodspeed (1929), Hanson and Heys
(1928), Hanson and Winkleman (1929), and Buchholz and Blakeslee (19306). Tem-
perature: Muller and Altenburg (1919), Muller (1928a), Goldschmidt (1929a), Jollos
(1930), Rokizky (1930), and Plough and Ives (1932).

21 See Conklin (1919-1920), Muller (1922, 1923), Muller and Altenburg (1919),
Morgan (1922), Castle (1923), Hagedoorn et al. (1921), and Gates (1915, 19206).

22 See Morgan (1922) and Gowen and Gay (1933).

312 INTRODUCTION TO CYTOLOGY

possible. As pointed out in an earlier chapter (p. 141) the chromonema
often exhibits a series of chromomeres arranged in a characteristic
pattern, and it is expected by many observers that these bodies may be
shown sooner or later to have some definite and significant relation to the
genetic units known as genes, as has long been conjectured. Whether
or not improved optical methods will bring visual confirmation of the view
that the gene is a discrete material unit, it will still remain true that it is
a distinct constitutional feature which is definitely localized in the nucleus
and which produces certain specific effects during the life of the organism.
Hence the geneticist can treat it as a unit, whatever its ultimate physico-
chemical nature may be. He may thus make effective use of it, no matter
how he may regard certain speculative hypotheses^^ suggesting that genes
are ultimate living particles which have somehow aggregated and differ-
entiated to form chromosomes, nuclei, and organisms.

The expression "factorial theory" usually has reference to the con-
ception of Mendelian factors or genes, but it should be obvious that any
comprehensive interpretation of organic phenomena in terms of contribu-
tory causes must include the action of other factors as well. It is to be
strongly emphasized that the system in which the phenomena of heredity
and development occur is the organism-environment. There is probably
no character which can be attributed to the organism or to the environ-
ment alone; these two components of the system cannot be separated in
any real sense. What an organism inherits is not a set of characters but a
protoplasmic organization giving it the capacity to react in certain ways
under certain conditions, the developed characters being the result of the
action of the entire system of which the organism and environment are
integral parts. The relative differential effects of genetic and non-
genetic factors may be expected to vary under appropriately varying
circumstances.^*

Summary. — According to the chromosome theory of heredity,
each chromosome carries a linear series of genes, which are units having
specific effects upon the course of development and hence upon the
morphological and physiological characters of the organism. Characters
dependent on genes in the same chromosome tend to be inherited together
as a linked group. A gene may be constant in its composition and effects,
or it may occasionally mutate and therefore exist in two or more allelo-
morphic states. In the latter case its role may be studied in crosses.

Two sets of chromosomes and hence two lots of genes are brought into
association in syngamy. When the resulting diploid organism forms
gametes (in most animals) or spores followed later by gametes (in most
plants), the homologous chromosomes and therefore the corresponding

23 See Alexander and Bridges (1928) and Darlington (1932a, Chap. XVI).
" For discussions of this point, see Emerson (1924), Jennings (1924, 1930), and
Sharp (1925). For a full account of the modern gene theory, see Morgan (1928).

CHROMOSOMES AND MENDELIAN HEREDITY 313

groups of linked genes are segregated, each gamete (or spore) carrying
one chromosome of each homologous pair and hence one linked group
of each kind. Investigation of the individuals of the next generations
shows that two corresponding gene groups may have exchanged some of
their members, this recombination being accomplished by an exchange of
portions between homologous chromosomes. It was this phenomenon
which first made it possible to determine the relative order of the genes
in the linear series in the chromosome.

Because of the distribution of multiplying generations of chromosomes
through successive life cycles and the activity of genes carried by them,
the characters appear in successive generations according to definite
rules first discovered by Mendel, who was not, however, aware of the
cytological reasons for the phenomena he observed. Such recombinations
of genes and Mendelian characters with occasional mutation are plainly
responsible for much of the diversity of type observed among species in
nature. It is accordingly inferred that the prevalence and high special-
ization of that form of reproduction involving gametic union and meiosis,
with its random assortment and crossing-over of chromosomes, are
evidences of its important evolutionary role in producing frequent and
diverse recombinations of hereditary elements. Its full value in this
respect has not been measured.

CHAPTER XVIII

FRAGMENTATION AND TRANSLOCATION

In the foregoing chapters we have described the chromosomes and
their normal behavior through the life cycles of representative organisms,
together with the application of such nuclear phenomena to the problems
of Mendelian heredity. Several chapters will now be devoted to less
common types of chromosome behavior and their genetic consequences.
Such phenomena afford valuable natural checks upon current theories.
Moreover, it has been found that the frequency of their occurrence can in
some instances be markedly increased by artificial
means, enabling the investigator to acquire an abun-
^V> /L^ dance of material for cytogenetic studies. They also
a\ V^^ constitute a basis for alterations of character beyond
^^ *^^D those attributable to gene mutation and Mendelian
•.W^W^^ recombination.^

^^ I \ This is a relatively new field in cytogenetics, and

data as well as interpretations are multiplying very
rapidly. In the following pages will be given examples

• •

DnCo A

Fig. 177. Fig. 178.

Fig. 177. — Translocation induced by X-rays in Crepis tectorum. 1, normal somatic
complement. 2, a portion of a C-chromosome has been translocated to a Z>-chromosome.
{After M. Nawaschin, 19.31c.)

Fig. 178. — Chromosome fragments in Tradescantia. A, bivalent fragment associated
with normal pair in meiosis. B, anaphase of mitosis in microspore, with some of the frag-
ments failing to divide. {After Darlington, 19296.)

of the better known types of aberrant chromosome behavior, the object
being to furnish little more than an introduction to the subject. It
should be remembered that opinions in such a field are subject to frequent
change, and that further refinements in method will doubtless make
necessary a redefinition of the categories into which the observed
phenomena now appear to fall.

1 For references to the literature on the effects of various agencies on chromosome
behavior and gene activity, see footnotes in Chap. XIII and footnote 20 on p. 311.

314

FRAGMENTATION AND TRANSLOCATION

315

Fragmentation of Chromosomes. — A chromosome may sometimes be
"broken" transversely into one or more pieces. In the Hterature there
are numerous reports of small bodies interpreted as such "fragments"
of "normal" chromosomes, and in some of these cases the morphology of
the normal chromosome set is known well enough to render the interpreta-

I

\ Los^-A

Losh-.
•1 Terminal delefion

01

2 In-hercalary dele+ion

01

01

b

c
ol

3 Terminal inversion

4 In-j-ercaloiry Inversion

5 Simple +roinslocc«i'ion 6 Reciprocal +roinslocc5ition

Fig. 179. — Diagram illustrating possible modes of origin of various chromosome abnormal-
ities. Spindle-attachment region indicated. {In part after Serebrovsky, 1929.)

tion valid. The effects of such fragmentation on the appearance of the
chromosome complement are various. Sometimes the chromosome
number is apparently raised by one, since both pieces of the broken
chromosome are present (Fig. 198, F). Or, one of the pieces may be lost
(deleted) or inverted, so that the complement is still normal with regard to
number but abnormal in the morphology of one member. Again, a
fragment may be attached to another chromosome (translocation), so that
the number remains normal while the morphology of two members is

316

INTRODUCTION TO CYTOLOGY

altered (Fig. 177). Finally, one or more fragments additional to a normal
complement may be present after a number of generations (Fig. 178).
Our knowledge of the actual mechanism of fragmentation is rather
meager. Available evidence, including the fact that portions of chromo-
somes are much more often translocated or inverted than left as free frag-
ments, suggests that contacts or entanglements between chromosomal
threads are in part responsible (Fig. 179). It is not uncommon to observe
prophasic threads interlocked and stretched as if a rupture or exchange
were soon to follow at the point of contact. The frequency of transloca-
tion and related alterations can be notably increased by the use of X-rays,
even when the nuclei treated are known to be in the metabolic condition.
For example, kernels of barley and maize, after being irradiated when in
the dormant state, give rise to individuals showing a relatively high

Fig. 180. — Breaking of chromosome after failure of distal ends to disjoin in living spermato-
cyte of Chorthippus. The changes shown occupied 40 minutes. {After B'elaf, 1929a.)

percentage of translocations in the multiplying cells (Stadler, Randolph).
Similar results follow the irradiation of mature pollen. In Drosophila
such aberrations can be induced by irradiating the mature spermatozoa. ^
The natural inference from such data is that the chromosomal threads
persist in some form throughout the entire nuclear cycle, and that X-radi-
ation increases the frequency of fragmentation and the like by inducing
localized alterations in the position, consistency, and tension of these
threads. In Zea certain translocations have been shown to be due to the
occasional association of non-homologous elements in the meiotic pro-
phase (p. 276).

Another mode of fragmentation is that in which a small portion of one
chromosome is torn away by its synaptic mate in the first meiotic ana-
phase. This has been observed in a living spermatocyte (Fig. 180),
and a similar process is strongly suggested by a Zea sporocyte observed by
Randolph ; but it is probable that mitotic derangements of this sort play
only a minor role in the production of alterations in the chromosome
complement.

2 MuUer (1927), Muller and Altenburg (1930).

FRAGMENTATION AND TRANSLOCATION 317

In certain tissue cultures it appears that the cells are especially
susceptible to the disturbing effect of X-rays just before the visible pro-
phasic changes begin. ^ The results of such derangements are sometimes
not evident until the succeeding anaphase, when the lack or abnormal
position of spindle-attachment regions, together with other agencies,
interferes with the regular movement of the affected chromosomes.
Marked chromosomal alterations are obtained in Zea by irradiating the
young ear during fertilization or soon afterward, when the embryos are
beginning their development.* Of special interest is the induction of
aberrations by subjecting the young ears to treatment with heat, since the
temperatures used need not be higher than those occasionally occurring
under natural conditions in the field.

Behavior of Free Fragments. — In the behavior of fragments much
depends upon the spindle-attachment region. Researches on Drosoyhila
and Zea indicate that a fragment not including the attachment region
tends to be lost in mitosis unless it is translocated to another chromosome
with such a region. For example, when a deletion occurs in Zea as shown
in Fig. 179, 2, the rod-shaped fragment with the attachment region sur-
vives and the ring is lost; but when the ring includes the attachment
region, the ring remains and the rod is eliminated.^ One case is known in
which the break passed through the elongated attachment region, both
ring and rod then possessing functional portions of it. In one strain of
Zea a minute chromosome consisting of an attachment region and a single
chromomere has been observed.

Ordinarily deletions tend to affect the viability of the cells or organ-
isms concerned, but this is found to vary with the amount and nature
of the material eliminated; it also varies at different stages of the life
cycle. When viability is not too seriously impaired, it can be shown by
genetical tests that the cells actually lack certain genes; in other words,
the deletion of a portion of a chromosome has created a genetic deficiency.
The first known case of this kind was one in which a normal gene, dominat-
ing one for the waltzing character in certain mice, was lost along with a
portion of a chromosome (Painter, 1927). Some genetic deficiencies
have been interpreted as being due to an inactivation of certain genes
rather than to an actual chromosomal deletion.

The method of determining the location of genes in the chromosome
by means of induced deletions may be illustrated by a case in Zea. It
had been shown previously that the satellited chromosome (number VI)
carries a gene PI, causing a dominant purple color in the plant. Pollen
from homozygous recessive plants {'pl pi), and therefore all carrying pi, was

^Strangeways and Oakley (1923), Strangeways and Hopwood (1926).
* Stadler (1928a, 19306, 1931a), Randolph (1932).

^ The peculiar behavior of such ring-shaped chromosomes has been correlated with
a certain type of variegation (McClintock, 19326).

318

INTRODUCTION TO CYTOLOGY

placed on the silks of homozygous dominant plants {PI PI). Normally all
of the immediate offspring {PI pi) of such a cross are purple, because
of the dominant PI derived from the pistillate parent. When, however,
the young embryos were X-rayed (20 hours after pollination), some of
them developed into non-purple plants. When such non-purple plants
were examined cytologically, it was found that one of the satellited
chromosomes lacked a portion of its longer arm (Fig. 181, £"). From this
it could be concluded that the irradiation had somehow caused the loss

0

0

Fig. 181. — Diagrams of inversion and deletion in Zea. A, the region between the
arrows in a normal chromosome (left) became inverted (right). Synapsis of homologous
regions of an inverted with a normal chromosome gave configuration shown diagram-
matically in B and semidiagrammatically in C; cf. Fig. 182, a; also Fig. 160. D, normal
satellited chromosome synapsed with one lacking most of its shorter arm; cf. Fig. 182, b.
E, normal satellited chromosome synapsed with one lacking a large portion of its longer
arm. Arrow indicates suspected position of gene PI. F, synapsed number VII chromo-
somes, one of which lacks a median portion, leaving the corresponding portion of the other
extending as a loop; cf. Fig. 182, c. The pair in this plant is heteromorphic for the chro-
matic knob, k, chromatic knob, n, nucleolus, s, spindle-attachment region. (After
McClintock, 19316.)

of this portion and that the gene PI had been located in it. Loss of the
dominant PI left the plants with only the recessive pi derived from the
pollen parent ; hence the plants were non-purple. Similarly, it has been
shown in another such test that the gene Ig (liguleless) probably is near
the end of the shorter arm of chromosome II (McClintock, 19316).

Especially instructive are certain cases in Drosophila reported by
Painter and Muller (1929). By the use of X-rays there were obtained
several flies in which one chromosome had undergone "intercalary
deletion," i.e., the middle region had been lost, leaving the two ends as a
single small chromosome (Fig. 179, 2). This small chromosome remnant

FRAGMENTATION AND TRANSLOCATION

319

was of three sizes in three flies, and genetic data showed that in each
successively larger deletion one more known gene had been eliminated.
Moreover, the order of disappearance was in exact accordance with the
order previously assigned to these genes in the chromosome map built up
from crossover data. This amounts to a direct proof of the essential
correctness of the map of this region of the chromosome, so far as the
serial order of the genes is concerned.

Another mode of behavior on the part of free fragments is that in
which they act regularly in the somatic divisions but manifest irregular-
ities at the time of meiosis, in part because of deficient synaptic reaction.
When fragments are present in addition to a fully normal chromosome
complement, they may be eliminated altogether or pass to some of the

a ,.

Fici. 182. — Synaptic configurations after inversion and deletion in Zea. a, after
inversion of median portion of one member; cf. Fig. 181, A-C. b, after deletion of portion
of shorter arm of satellited chromosome; cf. Fig. 181, D. c, after deletion of small median
region; cf. Fig. 181, F. {After McClintock, 19316.)

spores (or gametes) only. In this way gametes with or without extra
fragments may arise. When there are several fragments in the sporocyte
they may sometimes synapse among themselves, as in certain strains of
Tradescantia (Darlington, 19296). In other cells they seem to be
attached to the normal bivalents in various ways. They may be dis-
tributed unequally to the spores, or, because of lagging, they may be
partly or completely lost, especially when unsynapsed. Not infrequently,
however, one or more are transmitted through the gametes to the next
generation.

Finally, fragments may sometimes pass regularly through the entire
life cycle, behaving as extra independent chromosomes. This may be
expected when, for example, there are in the somatic cells two fragments
which are able to react properly in equational nuclear division because
they have spindle-attachment regions and to undergo synapsis regularly
because of their homologies.

The genetic effect of the presence of extra chromosomes or fragments
is known as duplication, i.e., certain genes are present in excess. Con-

320 INTRODUCTION TO CYTOLOGY

sequently the organisms carrying transmissible duplications may be
expected to show unusual ratios for some of their Mendelian characters if
the additional genes concerned are such as to affect the conditions of
dominance. Another general effect is sometimes observed in the size or
habit of the plant. In Matthiola, for example, it has been observed that
the presence of fragments is correlated with small size, the amount of
dwarfing being proportional to the degree of unbalance caused in the
chromosome complement by the fragments (Lesley and Frost, 1928).^

Inversion. — The reversal in position of a portion of a chromosome is
called inversion. The portion inverted may include one end, or it may
involve an interstitial region only (Fig. 179, 3, 4). Several such inver-
sions have been detected in the altered linkage relations of the genes with-
out being visible in the chromosomes themselves. In one of the linkage
groups of Drosophila, for example, the genetic data for certain genes
indicated that a considerable portion of the "right" end of one chromo-
some carrying them had been reversed in position. They indicated fur-
ther that when crossing-over occurred in the left end, none took place in
the right end, presumably because inverted and non-inverted chromosome
sections did not have homologous loci opposite each other. In one case it
appeared that the two chromosomes must have arranged themselves so
as to allow crossing-over in the right end; here none occurred in the left
end.'^

In Zea it has been possible to observe the effect of an inversion on
the synaptic behavior of the chromosomes. In one case, for example
(Figs. 181, A to C and 182, a), a long section of a chromosome was inverted
as a result of X-ray treatment. When this modified chromosome met its
normal synaptic mate, their homologous elements moved together in spite
of the abnormal arrangement in one chromosome and so produced the
peculiar configuration shown. Similarly, the inversion of a terminal
portion resulted in the formation of a loop at synapsis (Fig. 160). Almost
nothing is known about the mechanism of such inversions. It is possible,
as Serebrovsky (1929) has suggested, that at some stage the chromosomal
threads may undergo bending, fusion, and breakage as shown in Fig. 179.
It is probable that some other mechanism accounts for inversions
induced in metabolic nuclei by X-radiation.

It will be readily understood that inversions and other aberrations
involving portions of chromosomes may often alter the position of the
spindle-attachment region. Helwig (1929) believes that in Circotettix

® For further accounts of chromosome fragments, see Lutz (1916) and Hance
(1918a) on (Enolhera; M. Nawaschin (1926, 1931a) on Crepis; Belhng (1925a) on
Uvularia; Morgan, Sturtevant, and Bridges (1928) on Drosophila; Goodspeed (1929a6,
1930c) and Goodspeed and Avery (1930) on Nicotiana; and Lesley and Lesley (1929)
on Lycopersician.

'' Sturtevant (1926a), Sturtevant and Dobzhansky (1931).

FRAGMENTATION AND TRANSLOCATION 321

inversion is responsible for a change to the atelomitic from the telomitic
position, which is regarded as primitive for Acrididae.

Translocation. — The transfer of a piece of one chromosome to another,
aside from that involved in normal crossing-over, is called translocation
(Fig. 179, 5). It seems probable that as a rule the transfer is accom-
plished at one step and does not represent the attachment of a fragment
previously free. Commonly the translocated piece is borne terminally by
the receiving member; rarely it extends laterally from some intermediate
point (Fig. 67, D). The transfer may be to either a homologous or a non-
homologous member of the complement. It has been known to occur
naturally in many instances, but its frequency can be markedly increased
by the use of X-rays and heat. The first known case was discovered
genetically in non-irradiated Drosophila (Bridges, 1919, 1923). The
transfer of a single piece, or "simple translocation," is to be distinguished
from the mutual exchange of pieces known as "reciprocal translocation"
(Fig. 179, 6). The latter type will be dealt with in the following chapter.

Apparently any portion of one chromosome may be translocated to
any other chromosome. Because of the role of the spindle-attachment
region, many translocations must result in mitotic derangements serious
enough to prevent development. Hence in translocations induced by
X-rays it is commonly the "distal" portion without the attachment region
which appears to have been transferred, the "proximal" portion with the
attachment region remaining as an altered independent chromosome.^

Among the most favorable plant species for the study of transloca-
tions are Crepis capillaris and C. tedorum since they normally have
respectively but three and four pairs of easily distinguishable chromo-
somes. The results of many modifications are thus readily detected in
the metaphase^ (Figs. 69, 198). For the investigation of alterations
involving only very minute portions of the chromosomes, reliance must be
placed on such forms as Zea Mays with larger chromosomes exhibiting
individually their characteristic aspects with great clearness in the meiotic
prophase.

Among simple translocations involving only homologous chromo-
somes the first to be worked out both cytologically and genetically was
that in which a portion of the F-chromosome was found to be attached
to the X-chromosome in Drosophila (Stern, 19266, 1927a). Since
that time a number of other examples involving various pairs have
been discovered. The translocations can often be detected in the altered
length of the chromosomes concerned and, when their morphology is
sufficiently well known, in their altered form as well (Fig. 183).

* E.g., Dobzhansky (1931a) on Drosophila, M. Nawaschin (1931c) and Lewitsky
and Araratian (1931) on Crepis.

" M. Nawaschin (1926, 1930, 1931ac), Lewitsky and Araratian (1931).

322 INTRODUCTION TO CYTOLOGY

Among simple translocations involving non-homologous chromo-
somes the first case known both cytologically and genetically was one in
which a portion of the X-chromosome was transferred to one of the long
chromosomes (III) in Drosophila.^^ As an example of this general class of
translocations may be taken one in which the "right" end of chromosome
III was transferred to chromosome II (Fig. 184). By crossing flies
having this translocation with normal ones, " hyperdiploid " flies were
obtained with a normal complement plus the translocated piece. Studies
_ on the linkage relations in these flies showed

^ ^ % between what genes the original break had

^^I^S f /^^^ occurred and also that the hyperdiploid flies

^^^ ^ •^^ j]- possessed an excess of genes belonging to the

^' V^ "right" end of chromosome III (duplication),

as was expected (Painter and Muller, 19296).
Moreover, it is stated that in most such cases
of translocation the crossover frequency is
reduced in the limb of the chromosome in
which the break occurs and in one limb of the
receiving chromosome, whereas in each chro-
», mosome the limb beyond the spindle-attach-

^ ^^^^ ment region is not so affected (Dobzhansky,
193 la6). In flies having an extra fragment
of chromosome II attached to the F-chromo-
some it has been observed that for some reason
2 crossover frequency is reduced between the

Fig. 183.— Translocation of two normal chromosomes II (Rhoades, 1931c).

portion of chromosome 11 to

chromosome IV in Drosophiia. Many such translocations are known in
Shortened chromosome II plants. In Zea, where the miuute morphology

marked jS. 1, metaphase in 1.0./

oogonium; 2, metaphase in of the chromosomes has been studied during

neurocyte. {After Dobzhansky, ^J^g prophase, it is oftcn possible tO reCOguize

translocated pieces at this stage with the
microscope directly, as well as genetically in altered linkage relations.
Thus in one case it has been shown that a translocation which at
first appeared to be simple was in reality reciprocal, one of the exchanged
pieces carrying only a single characteristic chromomere (or at most two)
and apparently being too small to complete the synaptic configuration
ordinarily distinguishing reciprocal translocations (Burnham, 1932).
This naturally' raises a question regarding other supposed simple
translocations.

Certain translocations throw an interesting light upon the problem of
the forces concerned in meiotic disjunction. In Drosophiia it has been
reported that a pair of chromosomes, one of which carried a translocated
piece, did not assort at random with the pair from which the piece was

1" Muller (1926). See Painter and Muller (19296).

0

X 1

FRAGMENTATION AND TRANSLOCATION

323

derived (Muller, 1930c). This indicates that in such cases the disjunctive
force may not be limited to the spindle-attachment region of the chromo-
some, homologous distal portions tending to pass toward opposite poles
even when one of these portions has been translocated (Blakeslee, Darling-
ton, Muller). Many more observations must be made before safe
generalizations can be made regarding these matters.

Bearing on the Chromosome Map. — In some of the foregoing examples
of translocation the abnormalities were detected first in altered genetic
behavior and then confirmed cytologically, while in others they were first
seen cytologically and then confirmed genetically. This is a striking
corroboration of the cytogenetic theory that certain genes are definitely

Nl

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-9I.I(ro)

-70.7(6")^ ^
(ru)

-26.5-
(h)

-44

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100.7-
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Fig. 184. — Chromosome aberrations induced by X-rays in Drosophila. A, a "III
to II" translocation. In the drawing of the chromosome complement at the right the
translocated piece (indicated by arrow) came from the V-shaped chromosome at upper
right. B, hyperdiploidy produced by crossing a fly having the translocation with a normal
fly. {After Painter and Muller, 1929.)

located in certain chromosomes. In each case where the data were
adequate the genetic results of translocation and inversion showed that
the genes must have been arranged in the oi'der previously assigned to
them in the "genetic map" of the chromosome on the basis of crossover
values. On the other hand, they showed that these genes did not
necessarily have the spacing shown in the map. For example, the
translocated piece in Fig. 184, A was actually smaller than would be
expected from the large portion of the genetic map altered. This and
other cases in Drosophila have shown that the genes in the middle portion
of the "genetic map" of chromosomes II and III are represented closer
together than they are in the "cytological map" of the actual metaphase
chromosome (Fig. 185). The reason for this seems to lie in the fact
that in these chromosomes crossing-over is less frequent in the middle
region near the spindle-attachment point than it is toward the ends.
The genetic map was originally built up on the hypothesis that crossing-

324

INTRODUCTION TO CYTOLOGY

over is of about equal frequency in all regions; hence the genes in the
middle region were assigned to loci too close together. In a similar
manner it has been shown that several genes shown very near the "right"
end of chromosome I in the genetic map must lie much farther to the

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a! dp d b prBltkcn c

jOO 110

px sp

ru

D th

IP

a

»J-^

D th St p

coi HI

cu

sr

ca

Fig. 185. — Comparison of " genetical maps" of chromosomes I, II, and III of Drosophila
melanogaster with "cytological maps" of these chromosomes in metaphase as indicated by
translocation data, sp, spindle-attachment region. Cf. Fig. 173. {After Dohzhansky,
1932a, 1930d, 1929a.)

"left," the right end with the spindle-attachment point being for the
most part devoid of known mutant genes. ^^ The older genetic maps still
serve as diagrams of the order of the genes and their crossover values,
but they may not show accurately the true spacing. It is to be remem-

" For chromosomes II and III, see especially Muller and Painter (1929) and
Dobzhansky (1929aft, 1930ad, 19316). For chromosome I (X-chromosome), see
Painter (1931) and Dobzhansky (1932a).

FRAGMENTATION AND TRANSLOCATION 325

bered that the metaphase chromosomes studied in making these cyto-
logical maps have chromonemata within them, so that a map of a
chromonema might show a still different spacing. For chromosomes
appearing clearly in the prophase as long threads with characteristic
chromomere patterns it should be possible to build up more accurate maps
than can be expected for chromosomes which are "good cytological
material" only at the metaphase.

Discussion. — From the facts set forth above may be drawn a number
of interesting inferences, some of which are the following. A chromosome
contains a group of elements (genes) with special individual functions,
and the group may often be enlarged or diminished through translocation
without impairing the ability of the chromosome to behave regularly as
a whole. Apparently one of the chief requirements is the capacity to
react consistently with the spindle mechanism.

The monoploid chromosome set, or genom, is a group of chromosomes
differing among themselves in the number and kind of their component
elements. Ordinarily all or nearly all of the genetic elements (genes)
are probably necessary to the normal activity of the nucleus; in other
words, the genom is a harmonious, differentiated system of elements, the
majority of which are essential parts of the system. Spores or gametes
with extra elements (duplications) are often fully able to function,
although they may not compete successfully with those having normal
sets. Those lacking certain elements (deficiencies) usually tend to be
non-viable unless the deficiency is very small and involves no essential
genes. A spore or gamete carrying a set with a translocation, i.e., a
set in which all of the elements are present but arranged in a new group-
ing in the chromosomes, is ordinarily viable. Hence it appears that the
set functions best when there are present all of its naturally evolved
group of elements and no more, but that the arrangement of the elements
within the group is of somewhat secondary importance.

In the diploid chromosome complements of somatic cells also duplica-
tions are usually less detrimental than deficiencies. Moreover, a trans-
location involving only one of the sets (the individual therefore being
"heterozygous for the translocation") does not interfere greatly with
somatic development,^^ although there are exceptions to this, notably in
Drosophila.^^ In diploid somatic tissues the important consideration is
evidently "balance," i.e., there should be present two elements of each
kind and no more. The complement may be balanced when a deficiency
in one set is offset by a duplication in the other set. The diploid com-
plement must meet stricter requirements at the time of meiosis when
homologous elements undergo synapsis. A complement in which the two
sets have the same elements arranged in different ways, or in which

12 E.g., Crepis (M. Nawaschin, 1931c).

13 MuUer and Altenburg (1930), Dobzhansky (1930a, 1931o).

326 INTRODUCTION TO CYTOLOGY

extra elements are present, forms abnormal synaptic configurations.
These often lead to marked irregularities in chromosome distribution
in the meiotic mitoses and hence to sterility among the spores or gametes.
Thus a complement ordinarily requires a certain structural "symmetry"
as well as numerical " balance " if the organism is to retain its full fertility..

Since it is known that translocations take place from time to time
under natural conditions, and also that some of these, when homozygous,
do not impair the developmental and reproductive capacities of the
organism, one of the reasons why related organisms have chromosome
sets differing in minor details of their morphology should be evident.
Such differences are very common among related species (p. 126).
Even within the same species one may expect to find races which differ
less in the outfit of genes they carry, i.e., in genotype, than they do in the
arrangement of these genes and in chromosome morphology. The
individuals of two such races might look alike, yet show different linkage
relations among their characters when bred. Furthermore, it seems
altogether probable that losses, duplications, and translocations have
played a considerable role in the production of widely different chromo-
some complements and genotypes and therefore in the origin of stable and
fertile types to which specific rank has been assigned. Hence such
cytogenetic phenomena are of great importance to students of phylogeny
and evolution.

Finally, the discovery that certain agencies, such as X-rays and heat,
can be used to increase the frequency with which such chromosomal
changes occur has placed in the hands of the investigator a tool with
which he will be able not only to analyze the functions of chromosomes
in greater detail but also to bring about the production of new types of
plants and animals more rapidly than they would otherwise appear in
nature.

CHAPTER XIX
RECIPROCAL TRANSLOCATION

The mutual exchange of portions of chromosomes known as reciprocal
translocation, or often as "segmental interchange," differs in a number
of respects from that occurring in ordinary crossing-over. In crossing-
over, two homologous chromatids of a tetrad exchange portions which are,
with rare exceptions, exactly equivalent; and this is done with character-
istic frequencies in most of the diploid organisms which have been
adequately studied. On the other hand, in reciprocal translocation,
which is of relatively rare occurrence, the chromosomes involved may be
either homologous or non-homologous, and the exchanged pieces may be of
any relative size. When the exchange is between homologues and
involves approximately equivalent pieces, the effects may resemble those
produced by crossing-over; but ordinarily, especially when non-homo-
logues are involved, the cytological and genetical consequences of
reciprocal translocation are highly characteristic and not to be confused
with those of normal crossing-over. Just how such translocations are
accomplished is not yet known, but processes like those supposed to
bring about simple translocation are suggested. Moreover, it is not
improbable that many supposedly simple translocations are actually
reciprocal, one of the exchanged pieces being missed because of its
minuteness and the consequent failure to form the chromosome rings
characteristic of translocations of the latter type. Just such a case has
been described in Zea (Burnham, 1932).

Origin of the Theory. — In Datura stramonium, Blakeslee and his
associates^ found that any one of the 12 chromosomes might be present
in triplicate in the somatic cells, giving 12 visibly different "primary
mutants" with 25 chromosomes instead of the normal 24. The primary
type due to the presence of an extra chromosome I (the longest of the
set) was called "Rolled." When Rolled plants were bred there appeared
among the offspring four types: (1) normal plants without the extra
chromosome, due to the fact that half of the spores of Rolled do not
contain it; (2) Rolled plants carrying the extra chromosome; (3) plants
of a "secondary" 25-chromosome type called "Sugarloaf"; and (4)
another secondary type called "Polycarpic." Other primary types also
were found to have their corresponding secondaries. The secondaries in

1 For general accounts of the phenomena treated here, see Blakeslee (1928, 1929o,
19316). See also Belling (19276cd, 1928/) and Bergner et al. (1933).

327

328

INTRODUCTION TO CYTOLOGY

turn gave rise to (1) their corresponding primary type, (2) normals, and
(3) plants like themselves.

In studying the chromosomes of these 25-chromosome ("simple
trisomic") mutants, Belling observed that the three members of the
trisome tended to form characteristically different trivalent configurations
at diakinesis and metaphase / in the primary and two secondaries
(Fig. 186). In the primary, Rolled, they most frequently formed either
a V-shaped chain of three or a ring of two with the third one projecting

Normal
^ gamete

Z Z

Normal

0) a

Z Z-

2

Rolled

1 /■ 9 ■()

2 Z

Rolled

Sugarloaf

Gamete with
extra chromosome

01

Pojycarpic

A

a^ /a

ao>

Fig. 186. — Diagram showing chromosome constitutions of the primary Datura mutant
"Rolled" and its two secondaries, "Sugarloaf" and "Polycarpic," as postulated by
Belling. See text.

from one point of union; and when the third chromosome was free from
the others it was straight. In the corresponding secondaries, on the
contrary, the commonest configuration was a closed ring of three, usually
with one of the members sharply bent; and when the third chromosome
was free from the others it formed a small ring by itself. To account for
these configurations and for the characteristic outward differences
between the primary plant and its corresponding secondaries. Belling
and Blakeslee (19246) announced the hypothesis that in some manner
an interchange of unlike terminal segments had occurred between two
chromosomes I, giving a chromosome with two "right" ends and another
with two "left" ends. When the extra chromosome in a 25-chromosome

RECIPROCAL TRANSLOCATION 329

plant was of the former interchange type, the plant was a secondary;
when it was of the latter interchange type, the plant was the other
secondary; when it was of the normal type, the plant was a primary.
The trivalent configurations were explained on the assumption that only
homologous ends are paired in the late prophase and metaphase. As
would be expected, these abnormalities led to a certain amount of sterility
in trisomic plants because of the abnormal chromosome distribution in
meiosis.

In addition to the primaries and secondaries certain "tertiary"
types were discovered. The breeding behavior of the tertiary known
as "Wiry" suggested that both chromosome I (giving "Rolled" as a
primary) and chromosome IX (giving "Poinsettia" as a primary) were
somehow involved. Cytological observations showed that these two
chromosomes actually were connected with each other in meiosis. This
led to the definite formulation of the theory that non-homologous chromo-
somes occasionally undergo reciprocal translocation (Belling and Blakes-
lee, 1926). On the theory that only homologous portions undergo
synapsis, it was found possible to explain the curious configurations seen
at meiosis after various crosses and to account for the unusual genetic
behavior of the plants concerned. The continuation of these investiga-
tions led to results of great importance in the field of cytogenetics.
Reciprocal translocation has since been reported for other organisms also.^
It has received definite cytological proof and promises to explain many
hitherto puzzling phenomena in both plants and animals.

Reciprocal Translocation in Zea. — For a fuller description of recipro-
cal translocation in a diploid plant we may select a particularly clear case
from among several known in Zea (Figs. 187 to 189). This case,^ more-
over, is the one in which the peculiar morphology of the chromosomes
concerned permitted the first complete cytological proof of the correct-
ness of Belling's hypothesis of reciprocal translocation.

In a certain strain of maize known as "semisterile-2" it was observed
that approximately one half of the pollen grains and one half of the ovules
were functionless. Cytological examination of the sporocytes of semister-
ile plants revealed the presence of eight bivalents and a ring of four instead
of the 10 bivalents seen in normal plants. It followed that certain non-
viable chromosome combinations produced by the disjunction of the four

^E.g., Zea (Burnham, 1930; McClintock, 1930; Cooper and Brink, 1931; Brink
and Cooper, 1931); Pisum (H&kansson, 1929a, 1931a, 1932; Hammarlund and
H§,kansson, 1930; E. Richardson, 1929; Pellew and E. Sansome, 1931; E. Sansome,
1932); Campanula (Gairdner and Darlington, 1930); Rhoeo, Tradescantia, and Zebrina
(Darlington, 1929afe; Sax, 1931e; Nebel, 19326); Aucuba (Meurman, 1929a); Droso-
phila (Sturtevant and Dobzhansky, 1930; Muller, 1930c; Dobzhansky, 1933);
(Enothera (see later in chapter); Godetia and Clarkia (H&kansson, 1925, 19316);
Hypericum (Hoar, 1931); and Circoteitix (Helwig, 1932).

3 Burnham (1930), McClintock (1930a6).

330

INTRODUCTION TO CYTOLOGY

r t

S+oindcircl

Recip. Transl.

il

Semi-sfenle

Somot

C. 50°/o alternoil-e dis+nbuhon, giving
gameVes of Z +ypes , bol-h viable

Did kinesis

Selling gives 3 types

C. 50% adjacent distriloution giving
gwmetes of 4 types, all non-viable

t f

Standard

t t

II

■ •

Modified type

t t

Standard

/ \

/ \

/ \

/ \

t t

Standard

\

Semi-sfenle

%
t

)

Sem'i- sterile

t f

II

I •
■ •
I I

Modified type

\

i

Semi -sterile

Fig. 187. — Diagram of reciprocal translocation and its results in the " semisterile-2 "
strain of Zea Mays, based on data of Burnham (1930) and McClintock (1930a6). Chromo-
some VIII represented by solid line and chromosome IX by broken line. For simplicity
the two chromatids of each chromosome are not shown. The rectangles represent the
plants, and the circles their (spores and) gametes. Further explanation in text.

RECIPROCAL TRANSLOCATION 331

members of the ring were responsible for the sterihty and that the
ring itself was a result of reciprocal translocation.^ The chromosomes
concerned were number VIII (carrying the j-wss linkage group) and
number IX (carrying the C-sh-wx group), and these could be distinguished
on the basis of length, position and size of attachment region, and a
terminal knob on IX. The semisterile plant contained (in addition to
eight normal chromosome pairs) one normal VIII, one normal IX, one
interchange chromosome composed of portions of VIII and IX, and one
interchange chromosome composed of the remaining portions of IX and
VIII. The portions interchanged were unequal in length and were
such that each of the modified chromosomes had an attachment region.

In the meiotic prophase the synapsis of homologous portions in such
semisterile plants gives rise to a cross-shaped group of four, the center
of the cross marking the points of interchange in two of the members.
Later in the prophase the four open out, remain attached at their ends,
and shorten to form the conspicuous ring seen at diakinesis and meta-
phase /. In anaphase / the four members pass two by two to opposite
poles. In about half of the sporocytes adjacent members go to one pole,
while in the other sporocytes alternate ones go together. When distribu-
tion is "adjacent," all of the chromosome sets resulting are abnormal,
since they have a certain portion of one chromosome in excess and lack
a portion of the other chromosome concerned. The pollen grains
containing such sets abort: hence the sterility observed. On the other
hand, when distribution is "alternate," all of the resulting pollen grains
contain complete sets and are viable, although in one-half of them the
chromosomal materials have a new arrangement.

When a semisterile-2 plant is selfed or crossed to another of its kind
the progeny includes plants of three different chromosomal types in the
ratio of 1 : 2 :1 : plants with the standard chromosome complement, semister-
ile plants again forming a ring of four in meiosis, and plants with two modi-
fied chromosome pairs but fully fertile because the complement is sym-
metrical and balanced. Had the "modified" type been discovered first,
it might have been regarded as the "standard." Thus in Datura stra-
monium it appears that the standard line lA, which has been so exten-
sively studied, is actually less prevalent in nature than the 5-race, these
two types evidently having been differentiated by reciprocal transloca-
tion. The discovery of such related chromosomal types may be expected
in other genera also, especially among self-pollinated species.

The diagram for Zea (Fig. 187) shows further that in this case stand-
ards give about 50 per cent semisteriles when crossed with semisteriles,
that modifieds give about 50 per cent semisteriles when crossed with

* This explanation of semisterility was first suggested by Belling (1925c) for
SHzolobium. It also applies to certain forms of Pisum sativum (Pellew and E. San-
some, 1931).

332

INTRODUCTION TO CYTOLOGY

semisteriles, and that when standards and modifieds are crossed only
semisteriles result. When selfed, standards and modifieds give only
their own kind. All of these findings are consistent with the conclusion
that sterility here is due to abnormal assortments of chromosomal
materials.

In addition to semisterile-2, described above, there are several other
instructive semisterile races in Zea. Semisterile-4 has a reciprocal
translocation involving chromosome II {B-lg linkage group) and chromo-
some V {Pr-Vi) (Rhoades, 19316). Semisterile-1 involves chromosomes I
and II and accordingly the P-hr and B-lg linkage groups (Brink and
Cooper, 1931), while semisterile-3 involves I and VII. When two such

I

0

N

Fig. 188. — Diagram of reciprocal translocation in "semisterile-2" strain of Zea. a,
normal chromosomes IX (diagonal shading) and VIII (solid black). The clear portions
represent spindle-attachment regions. Arrows indicate location of interchange to produce
condition in h. c, synaptic complex in mid-prophase of meiosis after crossing a normal
plant with one carrying the interchange, d, the ring at diakinesis formed by opening out of
synaptic complex. N, larger normal chromosome (VIII) ; n, smaller normal chromosome
(IX) ; I, larger interchange chromosome (IX-VIII) ; i, smaller interchange chromosome
(VIII-IX). Cf. Figs. 187 and 189. (After McClintock, 1931a.)

races having interchanges involving one chromosome in common are
crossed, a race showing a ring of six at meiosis may result (Fig. 190).
This occurs in crosses between semisteriles- 1 and -5 (Brink and Cooper,
1932) and between semisteriles-1 and -3. The members of the ring of six
are variously distributed in the meiotic divisions, with the result that
about 75 per cent of the pollen aborts. It may be calculated further that
with a ring of eight or a ring of ten the sterility would be still greater.
The useful term catenation has been suggested for such chain formation
by chromosomes (Gates, 19316).

It is an interesting fact that in some cases in Datura and in CEnothera
the distribution of the catenated chromosomes is rather regularly alter-
nate, giving a high degree of fertility, and not so often adjacent as in
the semisterile strains of Zea mentioned above. In semisterile-2 the

RECIPROCAL TRA NSLOCA TION

333

i

B

Fig. 1S9. — Chromosome complexes produced by reciprocal translocation. A, synaptic
complex formed by two normal and two reciprocally translocated chromosomes; cf. key
diagram {B) and Fig. 188. C, ring of four in diakinesis formed by opening out of synaptic
complex; cf. key diagram (D) and Fig. 188. A, X 900; C, X 1800. {From McClintock.)

B

3
t

Fig. 190. — Formation of ring of six lay reciprocal translocation. The translocation
involves chromosomes 1 and 2 in race A, and chromosomes 2 and 3 in race B. In the hybrid
between A and B the six chromosomes tend to form a six-rayed synaptic complex in early
meiotic prophase and a ring of six at diakinesis. For easy interpretation one end of
each chromosome is marked with a knob.

334

INTRODUCTION TO CYTOLOGY

distribution differs significantly from a random one, which indicates
some influence favoring one type of orientation in the spindle rather than
the other. What it is that thus affects the distribution is not yet known.
As observations multiply it will doubtless be found that the ratio of the
various types of distribution varies widely in different cases.

(Enothera. — The genus (Enothera has occupied a prominent position
in genetics ever since de Vries formulated his mutation theory largely

..,ii>.

mm

UWt ■

./

\i

H

'.V

Fig. 191. — Stages in meiosis in the microsporocytes of (Enothera. A-D, CE. francis-
cana: A, prophase showing a ring of 4, and 5 pairs. B, diakinesis, after separation of pairs
from the ring. C, metaphase of /. D, anaphase, showing regular distribution. E-H,
(E. franciscana sulphurea: E, prophase showing ring of 12 and one pair. F, alternate
chromosomes in the ring of 12 passing to the same pole in anaphase; single pair not shown.
G, later stage; all chromosomes shown. H, anaphase of division //, with 8 chromosomes
in one figure and 6 in the other; this is due to an occasional irregularity of distribution in /.
(After Cleland, 1922, 1924.)

on the basis of the peculiar genetic behavior of (E. Lamarchiana. Not
only did this species give rise to occasional "mutants," but it displayed
a number of other genetical peculiarities for which little by way of explana-
tion was available. It was soon found that the Onagra section of the
genus was peculiar cytologically, the chromosomes in meiosis forming
rings or chains with various numbers of members in the different species.^

5 Gates (1907 et seq.), Lutz (1907 et seq.), Geerts (1907-1911), B. M. Davis (1909-
1911), Cleland (1922 et seq.). Later works: S. H. Emerson (1924a, 19286, 1931a6),
Boedijn (1924, 1926), Oehlkers (1926), HEkansson (1926o, 1928a, 19306c, 1931c),
Valkanover (1926), Kihara (1927a), Sinoto (1927), Sheffield (1927, 1929), Schwemmle
(1924 et seq.), Gerhard (1929), Kulkarni (1929a6c), Gates and Sheffield (1929a6),
Illick (1929, 1932), Leliveld (1928, 1931), Weier (19306), Cleland and Oehlkers
(1929, 1930), Catcheside- (1930, et seq.). Gates and Goodwin (1931), Darlington
(1929a, 1931e), and Hedayetullah (1932). For general accounts of research in
(Enothera, see Lehmann (1922), Oehlkers (1924), Renner (1925), and Gates (1928).

RECIPROCAL TRANSLOCATION 335

For example, (E. Hookeri had seven normal bivalents, CE. franciscana
a ring of four and five bivalent pairs, ffi. ruhrinervis a ring of six and four
pairs, CE. ruhricalyx a ring of eight and three pairs, OE. biennis (from
Munich) a ring of eight and a ring of six, (E. strigosa X Lamarckiana
cruciata a ring of ten and two pairs, CE. Lamarckiana a ring of 12 and one
pair, and CE. muricata a ring of 14 with no free pairs. Genetical investiga-
tions showed that the more chromosomes there are in the ring or chain, the
larger the number of linked genes (Cleland and Oehlkers). Of special
importance were the discovery by Cleland of the fact that alternate

(gJ (Le+hal)(6/5 j

^ — / V_y Loim. ( GV

0 X

?

V ) (Le+ho.l)( V,

Fig. 192. — The cytogenetic composition of (Enothera Lamarckiana. A, distribution of
the Renner complexes gaudens (G) and velans (F) in reproduction. Only the heterozygotes
survive. B, the chromosomes at diakinesis. Those carrying the gaudens and velans
complexes are marked G and F, respectively. Interchanged chromosomes indicated by
transverse marks. (Based on data of Renner, Cleland, and Blakeslee.)

chromosomes in the ring as a rule pass to the same pole in anaphase /
(Fig. 191) and his suggestion that each chromosome has a constant posi-
tion in the ring.*^ This results in the formation of spores and gametes
with only two assortments of chromosomes, so far as those in the ring are
concerned. Since certain chromosomes thus tend to remain together,
they function like a single large chromosome as carriers of linked genes.
As soon as the theory of reciprocal translocation had been formulated,
it was evident to those^ who employed it in their investigations that here
was probably one of the principal keys to the CEnothera problem. Its

For lists of chromosome configurations in the various species, see Cleland (1925),
Cleland and Oehlkers (1929, 1930), and Illick {19326).

^ It has since been shown directly in Rhoeo that the 12 chromosomes in the ring do
have constant positions (Sax, 1931e), and furthermore that the direction in which
the chromonemata coil tends to be constant for the given distinguishable members
(Nebel, 19326).

^ Belling, Sturtevant, S. H. Emerson, Meurman. The first discussions of the
question in the literature were those of Hakansson (1928a) and Darlington (1929a,
1931e). That CEnothera Lamarckiana combines unlike chromosome sets was suggested
by Lotsy (1917, 1919).

336 INTRODUCTION TO CYTOLOGY

adequacy was demonstrated in an extensive series of crosses which gave
the chromosome configurations predicted on the basis of the theory.^
Accordingly, the forms of (Enothera with catenated chromosomes are
now regarded as "structural hybrids," i.e., the two sets of chromosomes
in the diploid complement are unlike in the arrangement of the elements
composing them. This, together with the action of factors which are
lethal in certain combinations, goes far to explain the peculiar genetical
and cytological behavior observed in the genus.

The general situation may be illustrated by the case of (E. Lamarckiana.
Some years ago Renner (1915 et seq.) advanced the hypothesis that in
Oenothera there are several different genetic factor complexes which are
combined in pairs in the various species and that these complexes segre-
gate as wholes in meiosis, each gamete carrying one or the other. More-
over, certain complexes are lethal in gametes, while some combinations
are lethal in zygotes. The two complexes in (E. Lamarckiana are called
gaudens and velans. Hence gaudens- and ye/aws-carrying (spores and)
gametes are formed; and by their unions three different combinations
are possible in the offspring (Fig. 192). But both gaudens and velans
are lethal when in the homozygous condition in the zygote, hence the
only surviving plants are Lamarckiana. In other words, these plants
breed true, not because they represent a pure species as supposed by
de Vries, but rather because they are "complex heterozygotes" whose
homozygous offspring do not survive.

It was suggested at once that the two genetic complexes must be
carried by different gametes produced after meiosis,^ but only after
the theory of reciprocal translocation had been developed was it fully
apparent why the sets should segregate as wholes. The make-up of the
gametic sets of seven carrying the gaudens and velans complexes, respec-
tively, is such that, in meiosis, one free pair is formed while the remaining
chromosomes form a ring of 12 with the members of the two sets alternate
in fixed positions (Fig. 192). Since alternate chromosomes of the ring
usually pass to the same pole in anaphase 7, the members of each set
remain together when reproductive cells are formed. The single free
pair disjoins at random; but its two members are similar as to their shares
of the complexes concerned, so that their freedom does not alter the
complexes. Hence the different sets of seven chromosomes, like the
genetic complexes, may be treated as characteristically stable units.

The way in which the various genetic complexes are combined in the
species of Q^yiothera occurring in nature has been extensively studied
genetically, particularly by Renner. In addition, several combinations
not before known in nature have been produced by appropriate crosses.

8 Blakeslee and Cleland (1930), Cleland and Blakeslee (1930, 1931), Emerson and
Sturtevant (1931), Cleland (1932, 1933).

9 Bartlett (1915, 1916), Cobb and Bartlett (1919), Renner (1917).

RECIPROCAL TRANSLOCATION 337

In this way it has been possible to determine the degree of similarity,
or relationship, between the various complexes. In a parallel series of
cytological researches by Cleland and Oehlkers it has been shown that the
chromosome sets carrying the genetic complexes show clearly their degree
of relationship in the configurations produced at diakinesis after two
such sets have been combined in a cross. Complexes which are closely
related genetically combine to form configurations with most or all of
the chromosomes in separate pairs at diakinesis, whereas complexes
which are more distantly related give configurations with more of the
chromosomes involved in circles. The more distant the relationship,
the larger the chains or circles. Plants with identical genetic constitu-
tions tend to show similar configurations at diakinesis.^" The genetical
and cytological data are in striking harmony, which confirms the theory
that in these plants several genetic complexes differentiated by rearrange-
ment and gene mutation are carried by chromosome sets differentiated
largely by reciprocal translocation.

The development of the chromosome ring in the meiotic prophase of
(Enoihera is presumably like that in Zea, where it has been shown that
homologous portions synapse laterally and later open to form the ring
(p. 331). CEnothera is ill adapted to a study of these stages, but aside
from reports of parallelism of prophasic threads^^ there are other indica-
tions of lateral synapsis at some stage earlier than diakinesis. Among
these are interlocking of ring-shaped bivalents and larger rings and the
presence of chiasmata.^^ Moreover, crossing-over has been demonstrated
genetically for chromosomes in the ring,^^ which indicates a lateral
association. In view of the striking way in which parasynapsis with
reciprocal translocation accounts for the phenomena in CEnothera, as it
does for those in organisms {e.g., Zea) whose prophasic changes can be
clearly followed, this is now generally accepted as the proper interpreta-
tion of meiosis in this genus. For many years cytology witnessed a
battle between "parasynapsis" (lateral synapsis) and " telosynapsis "
(synapsis primarily end to end^^), but the battle has now practically
ended with the retirement of telosynapsis from the field as a general
interpretation of the meiotic prophase.

1" See Hoeppener and Renner (1928) and Cleland (1931a) for diagrams of relation-
ship of complexes and of chromosome configurations in crosses.

11 Gates and Goodwin (1931), Weier (19306), S. Emerson (19316).

12 Catcheside (19316), Darlington (1931e).

1^ See S. H. Emerson (1931a). Crossing-over between catenated chromosomes
has also been demonstrated in Zea, where the parasynaptic condition is particularly
clear (Creighton and McClintock, 1931), and in Datura (Blakeslee and Bergner, 1932).

1* Mid-prophasic doubleness was attributed to splitting rather than synapsis.
This interpretation will apply to unsynapsed portions of threads in translocation
complexes, multivalents (Fig. 159) and elsewhere, but not to normal meiosis. "Telo-
synapsis" of catenated chromosomes is but the result of a restriction of parasynapsis
to terminal regions.

338 INTRODUCTION TO CYTOLOGY

(Enothera exhibits other genetic pecuHarities, such as the production
of twin hybrids, unHke reciprocals/^ and a rarity of typical Mendelian
ratios. These find their explanation in the phenomena outlined above.
In contrast to the " superlinkage " displayed by forms with catenated
chromosomes, those with freely assorting pairs (Hookeri; grandiflora
of Davis) show ordinary linkage and typical Mendelian ratios. One
of the most important conclusions to be drawn from these researches is
that (E. Lamarckiana, which de Vries regarded as a pure species giving
rise to mutants by some unknown process, is a "permanent hybrid"
whose constancy is maintained by lethal factors and whose mutants are
due to occasional non-disjunction of some of the catenated chromosomes,
to translocations, to doubling of the chromosome number, and to dis-
turbances of the lethal mechanism by crossing-over. Had modern
cytogenetical work on (Enothera begun earlier, the mutation theory
would have been formulated in a very different manner. Moreover, the
solution of the (Enothera puzzle would not have been possible without the
theory of reciprocal translocation, which has now become more than a
theory.

1* Lehmann (1922) describes these phenomena with the aid of diagrams.

CHAPTER XX
HETEROPLOIDY

The course of modern cytology was markedly influenced by two dis-
coveries made in the early years of the century. Firstly, it was observed
that when Drosera rotundifolia (20 chromosomes) was crossed with
D. longifolia (40 chromosomes), there resulted a hybrid with 30 chromo-
somes, of which 10 were contributed by rotundifolia and 20 by longifolia.
When synapsis occurred in the microsporocytes in this hybrid only 10
bivalents were formed, 10 chromosomes remaining unpaired. Irregular
distribution of these unpaired chromosomes in the meiotic mitoses then
followed (Rosenberg, 1904a, 19096). Secondly, it was found that while
(Enothera Lamarckiana had 14 chromosomes (diploid), its mutant gigas
had 28 (tetraploid) (Lutz, 1907; Gates, 1908a). Since that time the
number and the behavior of chromosomes in related types and their
hybrids have been very extensively studied, especially in plants, where
the phenomena are best displayed. The results of these studies will now
be summarized in three chapters.

Terminology. — A nucleus with some number other than the true
monoploid or diploid number of chromosomes is said to be heteroploid.
This term and others given below are also applied to cells, tissues, indi-
viduals, races, or species with such nuclei. When the number is an exact
multiple of the monoploid, the nucleus (or tissue, etc.) is euploid. The
terms designating the multiples up to 10, beginning with the triple
number, are as follows: triploid, tetraploid, pentaploid, hexaploid, hep-
taploid, octoploid, enneaploid, decaploid. The higher multiples, which
are of rarer occurrence, are usually designated as 11-ploid, 12-ploid,
and so on. Euploid types are often said to be polyploid. In such species
the zygotic and gametic chromosome numbers are, for example, hexaploid
and triploid, or tetraploid and diploid, rather than diploid and mono-
ploid as in the types selected for discussion in foregoing chapters.^
Non-heteroploid groups may be called homoploid.

A nucleus (or tissue, etc.) with some number other than an exact
multiple of the monoploid number is aneuploid. When the number is a
little lower than some multiple it is hypoploid; when it is a little higher it is
hyperploid. Obviously, a number falling between the diploid and triploid
numbers, for example, may be called either hyperdiploid or hypotriploid.

1 It was formerly customary to refer to the zygotic and gametic numbers as "dip-
loid" and "haploid," regardless of the number of chromosome sets actually present.

339

340 INTRODUCTION TO CYTOLOGY

A chromosome complement in which the heteroploidy is due to the
multiplication of a single kind of monoploid set (or of some of its members)
is said to be autoheter opioid; whereas, one in which specifically different
sets or members are combined, as in a hybrid, is alloheter opioid. Although
this distinction cannot always be sharply drawn, it is of considerable
importance, as will appear later.-

-'^^^' Ak Mi

^k

D

Fig. 193. — Somatic chromosome complements of various species of Rosa, illustrating
euploidy. A, R. webbiana, 14 chromosomes. B, R. chinensis, 21. C, "Konrad Ferdinand
Meyer," 28. D, R. tomentosa cuspidatoides, 35. E, R. nutkana, 42. F, an octoploid
hybrid, 56. {After Tackholm, 1922.)

Heteroploidy in Related Species. — Very often the chromosome
numbers in the various species of a given genus form a more or less
complete euploid series (Fig. 193). For example, in Chrysanthemum the
various species have 9, 18, 27, 36, and 45 pairs of chromosomes; hence
they range from diploid to decaploid, with 9 as the "basic" number
(Tahara, 19156, 1921). In Potentilla, with 7 as a basic number, the
species range from diploid to 16-ploid.^ The species of Thalidrum, also
with 7 as a basic number, range from diploid to 12-ploid.'* Such long

2 In many reported cases it is not known which type of heteroploidy is represented.
It is largely for this reason that "heteroploidy" is here used singly and in combination
to indicate number only, without special reference to the kinds of sets concerned. In
this we follow Winkler (1916, 1920). Winkler refers to complements with similar sets
(genoms) as " isogenomatic " and to those with unlike sets as "anisogenomatic."
The terms "autopolyploidy " and "allopolyploidy" were suggested by Kihara and
Ono (1926). Hurst (19276) uses the parallel terms "duplicational polyploidy" and
"differential polyploidy." Tackholm (1922) introduced "euploid" and "aneuploid."
For further discussions of terms, seeLanglet (1927a), Brieger (19276), and von Wettstein
(1927).

3Shimotomai (1929, 1930), Miintzing (1931).

^Langlet (1927a), Kuhn (1928a, 1930c).

HETEROPLOIDY 341

unbroken series may be somewhat exceptional, but series with two
or three members are very common, especially in the angiosperms.
Extremely high multiples are found occasionally, as in Prunus laurocera-
sus with about 176 somatic chromosomes (ca. 22 X 8)^ and Senecio
Roherti-Friesii with about 180 {ca. 36 X S).*^ Euchlcena mexicana has 10
pairs of chromosomes and is annual, while E. perennis has 20 and is
perennial; the same is true of Sorghum sudanensis and S. halepensisJ

*

A ^ B

D

#tt

/\\^1 #•*?# ^•^^'^^^ ^z\^^^

#^^^^ •^•^•#1 ••.••^-.^ ••**^r

/A:;-::- .:v.V;5 o;r:.;: v ;-::•
;r.t:.\* v-vJi» •*-'>'• •.•.•'.*//.'.

• /•;.* V/V/* v»tV ••;•:••♦*

Fig. 194. — The chromosomes in the metaphase of the first meiotic mitosis in the micro-
sporocytes of various species of Car ex, illustrating aneuploidy. A, pilulifera, 9 chromo-
somes. B, sparsiflora, 16. C, montana, 19. D, tomentosa, 24. E, digitata, 26. F,
loliacea, 27. G, caryophyllea, 29. H, punctata, 34. /, distans, 37. /, vesicaria, 41. K,
Goodenoughii, 42. L, hirta, 56. (After Heilborn, 1924.)

A striking example of aneuploidy within a genus is afforded by Carex,
in which the species examined show 22 gametic numbers, all but one of
which lie between 9 and 42 (Fig. 194). Taxonomic relationship is roughly
indicated here by the number and size of the chromosomes.^ Another
example of such marked aneuploidy is Scirpus.^ Heilborn thinks it
probable that this exceptional condition is connected with the peculiar
mode of pollen formation in Cyperacese. Frequently a genus shows two
or more euploid series, or it may have euploid combined with aneuploid

5 Meurman (192%).

« Afzelius (1924).

' Longley (1924o, 1932); see also Huskins and Smith (1932).

« Heilborn (1922, 1924, 1925, 1932).

9 Hakansson (19285), Hicks (1928).

342 INTRODUCTION TO CYTOLOGY

numbers. Thus in Brassica the gametic numbers are 9, 18, 10, 20, and
19.^° In Rumex the species of the Eulapathum section show gametic
numbers of 10, 20, 30, 40, 50, 60, and 100, while those of the Acetosa
section show 7, 8, 9, 10, 20, 21, and 24. ^'^ Another such genus is Viola.'^^

Of special interest is the relation sometimes exhibited between
chromosome number and taxonomic division into subgenera. An
outstanding example is Triticum, in which the gametic numbers are 7 in
the einkorn group of species, 14 in the emmer group, and 21 in the spelta
group. ^^ Similar correlations are shown in a number of other genera. ^^

In contrast with the above are certain homoploid genera, such as
Pinus, with 12 pairs of chromosomes in every species yet studied: Quercus,
also with 12; Lilium, with 12; Philadelphus, with 13; Epilobium, with 18;
and Mecostethus, with 12.^°

Numbers in Related Genera. — Related genera often show "related"
chromosome numbers. In the large systematic group Bicornes (Ericales)
the gametic numbers found in the various genera are 6, 12, 18, 24, 36, 48;
also 8, 16, 13, 23j and 26. In the Antirrhinese the numbers are 6, 7, 8, 9,
and 12; here there appear to be related pairs of genera which differ by
one pair of chromosomes. The Orchidaceae have 8, 11, 12, 14, 16, 17, 20,
and 28, with 16 and 20 most frequent. ^^ Zea Mays and certain species of
Euchlcena and Sorghum have 10 pairs. Perennial species of the latter two
genera are tetraploid, and it is of interest to find that an induced tetra-
ploid from a diploid annual Euchlcena is perennial (Randolph, 1932).

Heteroploidy within a Species. — Individuals or races within a species
often differ characteristically in chromosome number; in many cases such
differences have been seen to arise in the breeding plot. In Zea Mays,
whose normal diploid number is 20, individuals have also been found with

i» Karpechenko (1924a, 1928), Shimotomai (1925), Morinaga (1929), and others.

11 Roth (1906), Kihara and Ono (1926), Ono (1926 et seq.), Jaretzky (1927a6,
19286).

12 J. Clausen (1927, 1929a), Gershoy (1928).

i^Sakamura (1918), Kihara (1919 et seq.), Sax (1918 et seq.), Nikolaewa (1920a,
1924), de Mol (1924), Watkins (1924, 1925, 1927, 1930), Bleier (1926 et seq.), Percival
(1926), Aase and Powers (1926), Aase (1930), Kagawa (19276), W. P. Thompson
(1925 et seq.), and others. Cf. Schulz (1913), Zade (1914, 1918), and Vavilov and
Jakushkina (1925) on relationships. See also footnote 8, p. 366.

" E.g., Valeriana (Senjaninova, 1927a), Gossipium (Denham, 1924o6), Bursa
(S. E. Hill, 1927), Pobjgonum (Jaretzky, 19286).

15 Chamberlain (1899), Ferguson (1901, 1904), and others on Pi7ius; Ghimpu
(19296/, 1930), Jaretzky (1930), Friesner (1930), and others on Quercus; Bangham
(1929) on Philadelphus; H&kansson (19246), Schwemmle (1924), Michaelis (1905),
and Johansen (1929) on Epilobium; McClung (1923, 1924) on Mecostethus. For
Lilium and other cases, see the lists of Tischler (1927a, 1931).

16 Hagerup (19286) on Bicornes, Heitz (1927a) on Antirrhineae, Hoffman (1929) on
Orchidacese. See also Langlet (1927a, 1932) on Ranunculaceae, Jaretzky (1928a,
1932) and Manton (19326) on Cruciferaj, Fernandes (1931) on Liliaceae, Wanscher
(1931, 1932) on Umbelliferae, and Tschechow (1932) on Trifoliese.

HETEROPLOIDY

343

10, 30, 40, 80, and certain aneuploid numbers. Euploid individuals and
races are now known in a large number of species in many groups of
plants. In (Enothera Lamarckiana, where the diploid (2n) number is 14,
some of the well-known mutants have 471, 3w, and 2n + 1 chromosomes.
The primary and secondary mutants of Datura stramonium are 2n + 1
forms. In Thalidrum minus there are three races (species ?) with gametic
numbers of 7, 14, and 21. Vicia grceca has races with 6, 7, and 14. In
Matthiola incana have been seen individuals with 14, 14 + two fragments,
and 7 + one fragment. In Pellia epiphylla and P. Neesiana races with
diploid gametophytes are known. In
Funaria hygrometrica there are races with
14, 28, and 56. A few such cases are
known among the algae. Among grains cer-
tain speltoid wheats, dwarf wheats, and
fatuoid oats may have one or two chromo-
somes more or less than the normal number.
In Artemia salina, a crustacean, there are
diploid, tetraploid, and octoploid races. ^^

Heteroploidy within the Individual. —
Occasionally one region of an individual
differs from the remainder in chromosome
number. Diploid Datura plants, for example,
have been seen to bear 2n + 1, 2n — 1, and
4w branches. Sometimes the modified region
is a well-defined sector of the plant (Figs.

195,204).!^ The differing portions may also somal chimera in Nicotiana.
, , J • 11 • n • • ii Cells at left of heavy line have 24

be arranged concentrically: m Spinaaa the chromosomes, as at a; cells at
plerome and dermatogen may be 2w and the right have 48, as at b. {After
periblem An or 8m. ^^ Such sectorial and " ^'

periclinal types are known as "chromosomal chimeras. " Of very
frequent occurrence are scattered cells with aberrant numbers, especially
in roots or anthers subjected to abnormal cultural conditions. The
formation of tetraploid shoots is sometimes induced from callus tissue

Fig. 195. — Portion of trans-
verse section of root of chromo-

" Randolph and McClintock (1926) and Randolph (1932) on Zea; Blakeslee,
Belling, and Farnham (1920) on Datura; Kuhn (1928o) on Thalidrum; Sweschnikova
(1927a) on Vicia; Lesley and Frost (1928) on Matthiola; Heitz (19276) and Showalter
(1927c) on Pellia; von Wettstein (19246) on Funaria; Winge (1924), Huskins (1928a6,
1931a), Mtintzing (1930a) and Hakansson (1933a) on Triticurn; Huskins (1927, 1928a)
and Nishiyama (1931) on Avena; Artom (1912) and F. Gross (1932) on Artemia. For
(Enothera, see footnote 5, p. 334.

18 Nawaschin (1926, 1930a) and HolUngshead (1930c) on Crepis; Lesley (1925) on
Lycopersicum; Ruttle (1928) on Nicotiana; Jaretzky (1927a6) on Thalictrum. Langlet
(19275) lists known cases.

•' De Litardiere (1923c) and Langlet (19276) on Spinacia and Cannabis.

344 INTRODUCTION TO CYTOLOGY

after grafting or decapitation, notably in Solanacese.^" Another interest-
ing condition is seen in certain gynandromorphs, where portions of the
body differing in chromosome number differ also in sex (p. 381). In
certain Diptera it has been observed that tracheal cells, intestinal cells,
or rectal gland cells may become polyploid while the germ cells retain
the normal number.-^

How Differences in Number Arise. — Sudden alterations in chromo-
some number are brought about by aberrations of mitosis, by the union of
unusual or unlike complements in syngamy, and by a combination of these
two processes. In a number of instances such aberrations have been
directly observed in progress, while in certain others it can reasonably be
inferred that they are responsible for differences in number found in the
field or breeding plot. Moreover, some of them may be induced experi-
mentally, as by means of heat or X-rays. ^^ Some of the more common
phenomena leading to numerical changes are listed below.

JJ.^ JL. ^..^^

? <? ?

Fig. 196. — Chromosome complements of Drosophila melanogaster as they appear
during mitosis in a female, a male, and a non-disjunctional female with an extra X-chromo-
some. {After Morgan.)

Two chromosomes may fail to separate in the anaphase of mitosis
and pass together to one pole. In meiosis this non-disjunction results in
the formation of some spores or gametes lacking one chromosome (n — 1)
and others with both members of the non-disjoined pair (n + 1). Unions
of gametes after this aberration may give rise to new individuals with
2n — 2, 2n — 1, 2n, 2n + 1, or 2?i + 2 chromosomes (Fig. 196). Gam-
etes and zygotes with extra chromosomes are viable more often than those
lacking chromosomes, so that hyperploid types arise more frequently than
hypoploid ones. Sometimes more than one chromosome pair may fail to
disjoin, giving still greater departures from the diploid number in the
offspring. When the halves of a split chromosome in somatic tissue pass
to the same pole instead of separating, hyperploid and hypoploid nuclei
result. Such an aberration may have an immediate visible effect upon

20 Winkler (1916), J0rgensen (1928), F. Sansome (1929), Lindstrom and Koos
(1931).

21 Holt (1917; on Culex), Frolowa (1926, 1929; on Drosophila and other genera).

22 For literature, see footnotes in Chapter XIII.

HETEROPLOIDY 345

the tissue concerned, giving one type of "somatic mutation," but it
affects the next generation only if it occurs in the hneage of the reproduc-
tive cells. -^

Very often, especially in meiocytes, one or more of the chromosomes
may fail to pass far enough toward either pole to be included in one of the
new nuclei. This is known as lagging, and it may play a very important
role in determining the make-up of the chromosome complements of
spores, gametes, and offspring, particularly in hybrids. The extra
chromosome in 2n + 1 types is very often lost through lagging, decreas-
ing the expected number of n + 1 gametes.

Sometimes the entire complement of chromosomes behaves in an
aberrant manner. In the meiocytes the synaptic reaction may be defi-
cient, some of the chromosomes failing to conjugate (asynapsis) or losing
their synaptic association prematurely (desynapsis) . Irregularities in
chromosome distribution naturally follow. In case the whole complement
is involved, complete ameiosis may result; the chromosomes may all
divide equationally in the single mitosis which occurs, so that diploid
spores or gametes are formed.-'* A union of such a gamete with a normal
monoploid gamete results in a triploid individual.-^ When ameiosis
occurs in both the microsporocytes and the megasporocytes, two diploid
gametes may unite to form a tetraploid individual.

Similar results may follow from 7ion-division in somatic cells. Here
the chromosomes split, thus doubling their number, but there is no divi-
sion of the nucleus as a whole. It is probable that such an aberration
occurs frequently in the zygote or young embryo, giving a tetraploid
individual directly. ^^ The formation of a tetraploid plant in this way has
been artificially induced by heating young ears of Zea soon after fertiliza-

22 Non-disjunction, originally discovered by R. Gates (1908) in CEnothera, is respon-
sible for some of the 2n + 1 chromosome mutants of CEvothera and Datura. In
Datura, Belhng and Blakeslee (19246) saw eight cases of it in 1,137 sporocytes; in
Uvularia Belhng (1925a) saw 10 cases in three buds. Other examples are Nicotiana
(Goodspeed, 1923; Ruttle, 1927) and Zea. In Nicotiana tabacum the forms called
"enlarged" and "fluted" have 2n + 1 and 2n — 1 chromosomes, respectively
(Clausen and Goodspeed, 1924, 1926a).

2* This may be the reason why in Zea, for example, tetraploid plants so rarely arise
directly from diploids with aberrant sporogenesis. Aberrations at this stage more
often lead to triploidy.

-* Triploidy was first discovered in CEnothera by Stomps (1912) and Lutz (1912)
and was explained by them in the above manner. Triploids have since been produced
frequently by crossing diploids with forms producing occasional diploid pollen grains,
e.g., in Hyacinthus (de Mol, 1923).

26 Gates (19096, 1913, 1924a) and Davis (1911) for CEnothera and other genera;
Strasburger (19106) for CEnothera and Wikstrannia; Tischler (1910) for Musa; Sax
(1921, 1922) for Triticum; Tahara (1921) for Chnjsanthemum; Afzelius (1924) for
Senecio; Clausen and Goodspeed (1925) for Nicotiana. Winge (1917) attributes such
doubling in hybrid zygotes to chromosomal incompatibility (see p. 369).

346

INTRODUCTION TO CYTOLOGY

tion (Randolph, 1932). It has been observed in roots of Spinacia that
the chromosome halves may separate during the prophase and undergo a
second splitting so that each telophase nucleus receives the tetraploid
number (24) rather than the diploid (12). Repetition of the process may-
give octoploid nuclei." Sometimes diploid plants show tetraploid sporo-
cytes undergoing meiosis along with the normal diploid ones, which sug-
gests the occurrence of non-division in the development of the anther. A
similar condition has been seen in the spermatocytes of Euschistus.-^ In
Zea the occasional appearance of triploid plants strongly suggests that
functional diploid spores and gametes may thus arise and lead to hetero-
ploidy. The origin of tetraploidy through a fusion of two such gametes
would depend on the occurrence of the aberration in the lineage of both
sperms and eggs. In a monoecious plant a single aberration of this type

ABODE

Fig. 197. — " Semiheterotypic " mitosis, with formation of "restitution nucleus" in
Hieracium. A, B, prophase; C, irregular metaphase; D, irregular anaphase. E, polar
view of metaphase of division of restitution nucleus formed when all of the chromosomes
in the preceding anaphase (not all shown in D) reorganize as one nucleus instead of two.
{After Rosenberg, 1927a.)

occurring before the differentiation of the carpellate and staminate por-
tions might result in the production of diploid gametes of both sexes,
whereas in a dioecious plant or in a monoecious one after the differentia-
tion of the carpels and stamens, two similar aberrations would be required
for the production of tetraploidy in the immediate offspring.

Another aberration in sporogenesis is the formation of a "restitution
nucleus" (Fig. 197). Usually after deficient synapsis the chromosomes
are scattered along the first meiotic spindle, and before they reach the
poles a single large nucleus is formed, enclosing all of them. This nucleus
and the sporocyte then divide once, giving two large microspores, each
with the unreduced number of chromosomes. ^^ In several instances
nuclei formed by the meiotic mitoses have been seen fusing in the sporo-

^^ De Litardiere (1923c). Other probable cases of non-division: Cannabis (de
Litardiere, 1924; Langlet, 19276) and Lycopersicum (Lesley, 1925).

2« Randolph (1928) and McClintock (1929a) on Zea; Bowen (1922/) on Euschistus;
Fukushima (1921) on Brassica; Geerts (1909) on megasporocyte in Oenothera.

29 Rosenberg (1917, 19266, 1927a6) on Hieracium^ Kuwada (1928) on Balanophora,
Tischler (1928) on Ribes, Kagawa (19296) on Triticum, Buxton and Newton (1928)
on Digitalis.

HETEROPLOIDY 347

cyte; occasionally it is the mitotic figures themselves which unite. ^^
The result in either case would be unreduced spore nuclei. The role
of the last mentioned aberrations, as well as that of abnormal nuclear
fusions occasionally seen at other stages, in the production of heteroploidy
is problematical. The fusion of two male gametes with the egg (dis-
permy) may possibly lead to triploidy in some cases. ^^

Although there are many ways in which the chromosome number may
be altered, it is probable that tetraploidy arises most often through a
doubhng of the number in a diploid zygote or young embryo, and that
triploidy is usually the result of a union between a monoploid and a
diploid gamete, the latter being formed either after meiosis in a tetraploid
plant or after ameiosis in a diploid one. Further increases in number may
follow. Doubling in a triploid gives a hexaploid; crossing a hexaploid
with a tetraploid may give a pentaploid ; doubling in a tetraploid, or cross-
ing a hexaploid with a diploid followed by doubling, may giveanoctoploid,
and so on. Thus it appears that the origin of tetraploidy is often the first
step in the development of higher euploid types. Aneuploid plants with
one or two chromosomes lacking or in excess are probably due chiefly
to non-disjunction; and since such plants produce spores and gametes
carrying various chromosome numbers, further unions may extend the
aneuploid series. As would be expected, many of the altered types fail
to meet the test of viability; or, if viable, they may fail to compete suc-
cessfully with normal types because of their reduced vigor or fertility.
Nevertheless, the fact that the monoploid chromosome numbers of so few
flowering plants, relatively speaking, are prime numbers indicates the
important role of polyploidy in the evolution of this great group (Winge,
1917).

With regard to the evolution of new "basic" chromosome numbers,
from which new polyploid series may in turn be developed, it seems
improbable that simple additions or losses of whole chromosomes are very
significant in this connection, because of the physiological unbalance
which such changes introduce. If, however, they are accompanied by
compensatory alterations, they may become very important. Thus M.
Nawaschin (1932) cites evidence suggesting the following "dislocation
hypothesis": An extra chromosome is first added in one of the ways
mentioned above, so that the somatic cells of an individual contain three

^ Gates (1915) on (Enothera, Rosenberg (1917) on Hieracium, Blackburn and
Harrison (1921) on Rosa, Ljungdahl (1922) on Papaver, McClintock (1929a) on trip-
loid Zea, Prywer (1931) on Beta. In Nereis oocytes treated with ultra-violet light
both meiotic mitoses occur near the center of the cell; the four resulting nuclei may
then unite with the sperm nucleus and a pentaploid embryo may begin development
(Just, 1933).

" Dispermy has been seen in Gagea (Nemec, 1912), (Enothera (Ishikawa, 1918),
and other plants. It can easily be brought about in echinoderm eggs (Boveri).

348 INTRODUCTION TO CYTOLOGY

chromosomes of one kind (a "trisome"); through ehmination and trans-
location the materials of one member of the trisome, except for the
kinetic body of the spindle-attachment region, are then replaced by some
of the materials of a non-homologous chromosome (or of more than one of
these), so that the materials of the latter chromosome come to be associ-
ated with two kinetic bodies instead of one; through disjunction at
meiosis the normal homologue of the contributing chromosome is elimi-
nated, and gametes with two chromosomes in its place are formed; union
of two such gametes gives an individual having one more chromosome
pair than the original type but with the same assemblage of chromosomal
materials. The basic number may also be changed in the opposite direc-
tion if translocations and eliminations leave a kinetic body with little or
no chromosomal matter, and this body is then segregated out.

Some of the irregularities described in the foregoing pages, notably
asynapsis, lagging, and zygotic doubling, have been observed repeatedly
in interspecific hybrids. The hasty conclusion that all such aberrations
indicate hybridity has been proved erroneous by what has been learned
about the effects of cultural conditions; but it remains true that hetero-
ploidy has one of its chief causes in hybridization,^^ as will be made clear
in a later chapter. In the study of such phenomena and their significance
it therefore becomes necessary to distinguish two kinds of heteroploidy:
autoheteroploidy and alloheteroploidy.

Autoheteroploidy and Alloheteroploidy. — In autoheteroploid types
the chromosomes of only one kind of set are involved. For example, a
plant with three sets which are alike (within the usual specific limits)
is an autotriploid, whereas a plant with two sets from one species and one
set from another is an allotriploid. Similarly, a plant with a single one of
its chromosomes in triplicate is an "autohyperploid, " whereas one in
which the extra chromosome is one from the set of another species is an
"allohyperploid. " In other words, the autoheteroploid types are specif-
ically "pure" as regards their chromosome complements, while the allo-
heteroploid types are "hybrid." It is obvious that such a distinction
cannot always be sharply drawn, since hybridity may exist in so many
gradations; moreover, both conditions may be present together, as, for
example, in a hexaploid having three sets from one species and three from
another. Nevertheless, failure to distinguish the conditions as far as
possible has brought much confusion into the literature on this subject.

When the origin of the heteroploid condition is not directly known,
an examination of the morphology of the chromosomes composing the
complement often yields decisive evidence as to the kind of heteroploidy
represented. For example, in euploid forms of Crepis, whose chromosome

32 Rosenberg (1917), Ernst (1917, 1918), Winge (1917), I. Holmgren (1919),
Tackholm (1920, 1922), Jeffrey et al. (1922), Jeffrey (1925a), Afzelius (1924), Gates
(1924a, 1925, 1929a).

HETEROPLOIDY

349

morphology is well known, inspection of the complement in the root tips
enables one to tell whether a single set has been multiplied to produce an
autoheteroploid type or unlike sets have been combined to make an
alloheteroploid one. Similarly, one may often tell whether an apparently
2n + 1 type has arisen through the duplication of a chromosome by
non-disjunction (Fig. 198, E), or through the fragmentation of a chromo-
some (Fig. 198, F), or through hybridization (Fig. 206, 3). Furthermore,

c, AC,

h

Fig. 198. — Somatic chromosome complements in Crepis, showing autopolyploidy and
other conditions. A, triploid complement in C. capillaris. B, pentaploid complement
in C. capillaris. C, diploid complement in an individual "asymmetrical" for size of
satellites. D, tetraploid complement in C. tectorum. E, hyperdiploid complement in
tectorum plant with extra B-chromosome. F, diploid complement in tectorum plant with
one D-chromosome fragmented into two portions: Do and d. {After M. Nawaschin,
1926.)

a sufficient knowledge of the chromosome morphology in an organism
under investigation makes it possible to detect alterations, such as
deletions and translocations, not affecting the number of chromosomes
present. The occurrence of such alterations makes it necessary to use
the criterion of chromosome morphology with considerable caution.

Other criteria of value in the analysis of heteroploid complements
are the meiotic behavior of the chromosomes and their functions as
indicated by genetic data. Autoheteroploids and alloheteroploids
frequently differ characteristically in their meiotic and genetic behavior.
It is the purpose of the next two chapters to describe some of the most
important of such phenomena.

CHAPTER XXI
THE CYTOGENETICS OF AUTOHETEROPLOID PLANTS

A somatic nucleus in a plant sporophyte or higher animal is auto-
heteroploid when one or more of the chromosomes of the normal set are
present in some number other than two.^ A gamete or gametophyte
nucleus is autoheteroploid when one or more of the members of the normal
set are present in some number other than one. In other words, only one
kind of set is represented, but some or all of its members are present in
unusual numbers. The cytological and genetical behavior shown by
autoheteroploid organisms may be expected to differ from that in mono-
ploid-diploid forms. It is the purpose of this chapter to review some of
the more characteristic types of such behavior.

Tetraploids and Tetrasomics.— A plant with four similar complete
chromosome sets is "autotetraploid." One with a single chromosome in
quadruplicate but all of the others in duplicate is "simple tetrasomic."
It is found that the four homologous chromosomes in the latter type
behave in general like any one of the groups of four in the autotetraploid.
Hence the simple tetrasomic type, when bred, may be expected to show
"tetrasomic" genetic ratios in characters due to mutant factors in one
chromosome and ordinary "disomic" ratios for those due to factors in all
the other chromosomes, whereas in an autotetraploid type the ratios
will be tetrasomic for all characters. To illustrate such ratios, one may
therefore select either a tetraploid or a tetrasomic type.

In autotetraploids and tetrasomics any four homologous chromosomes
ordinarily tend to form a quadrivalent group in meiosis (Figs. 199, g to i;
200). As synapsis begins, it is seen that any one of the four may associate
with any other one in a given region, or with more than one in different
regions. If all four form and retain such synaptic associations a quad-
rivalent chromosome is present at the end of the prophase, hence in a
tetraploid plant there may be the monoploid number of quadrivalents.
Often the synaptic association is such as to group the four members into
two bivalents, or into a trivalent and a free univalent. Thus tetraploid
sporocytes may sometimes exhibit the diploid number of bivalents (the
"double-diploid" condition) or varying numbers of quadrivalents,
trivalents, bivalents, and univalents. The reasons for this variation are
not fully known, but it seems that the manner in which the four members

1 This does not apply to normally unpaired or multiple sex-chromosomes. Cf.
definitions on pp. 340 and 348.

350

THE CYTOGENETICS OF AUTOHETEROPLOID PLANTS

351

happen to associate as synapsis begins, together with the number and
persistence of chiasmata, is an important factor in this connection. The
behavior is apparently influenced in some cases by the relative positions
of the chromosomes in the nucleus before synapsis begins; also, it tends to
differ characteristically in different species or genera.- In addition to the
"primary association" determined by the ordinary synapsis in the early
prophase, there is frequently a ''secondary association" at the end of the
prophase when homologous bivalents previously separate move together
to form loose quadrivalent groups.^

Fig. 199. — Synaptic configurations in heteroploid plants, a-f, trivalent chromosomes
in Hyacinthus. g, h, quadrivalent chromosomes in Hyacinthus. i, quadrivalent in Tulipa.
e, f, and i are postdiplonema stages. {After Newton and Darlington, 1929.)

The phenotypic ratio shown by a pair of Mendelian characters in
breeding tetraploids obviously depends upon the degree of dominance
exhibited, and upon the manner in which the four chromosomes carrying
the four differential factors are distributed in the meiotic divisions. In
tetraploid Primula sinensis* the several combinations, DDDD, DDDd,
DDdd, Dddd, and dddd, give a series in depth of flower color, the first
three being white or faintly tinged, the fourth weakly colored, and the
fifth more deeply colored. Hence various types are to be expected

2 There are sometimes n quadrivalents in Datura tetraploids (Belling and Blakeslee
1923, 1924o; Belling, 1927(i). The number in most cases is smaller, as in Prunus,
Hyacinthus, and Primula sinerisis (Darlington, 19276, 1929c, 1931a; Dark, 1931); also
in Euchlcena perejmis (Randolph, unpubl.) and Dahlia (Lawrence, 1929). In Cam-
panula most of the chromosomes are in pairs (Gairdner, 1926). The "double-diploid "
condition occurs sometimes in Hyacinthus (Belling, 19256) and rarely in Datura. In
Zea there are quadrivalents and bivalents, and the segregation is at random (Randolph,
Rhoades).

^ Darlington (1928) on Prunus, Darlington and Moffett (1930) on Pyrus, Lawrence
(1931c) on Dahlia.

* Gregory (1914), Bateson, Sverdrup, Haldane (1929).

352

INTRODUCTION TO CYTOLOGY

An

among the offspring of plants bearing both D an d. On the other hand,
a single G-factor (for green stigma) is able to dominate three g-faetors
(for red stigma); hence only two types appear among the progeny, so
far as this character is concerned.

The ratios in which the two types may be expected to appear in
tetraploid plants with such strong dominance may be readily computed/
In Primula, for example, only green stigmas are to be expected in the
progeny of a GGGG plant after selfing or back-crossing to gggg, because
every individual has at least one dominant G; whereas in the progeny of a

gggg plant after selfing or back-crossing to gggg,
only red stigmas appear, since all of the factors
present are recessive. In the progeny of plants
with GGGg, GGgg, or Gggg, characteristic ratios
are to be expected, these depending largely upon
the manner in which the four homologous
chromosomes carrying the factors in question
behave during meiosis. Thus when the four
form a quadrivalent with the constitution GGgg

assume'/°bjr^he''"chromo! ^^^ ^^^ disjoined two from two at random, the
somes in the first meiotic ratios wiU not be the Same as when they form

two bivalents arranged Gg and Gg.

In tetraploids and tetrasomics a certain
amount of sterility may be expected to result
from occasional irregularities in chromosome
distribution, but, generally speaking, such plants
are much more stable and fertile than those
having an odd number of certain chromosomes or
chromosome sets as in trisomies, triploids, pentaploids, etc. This is
because elements present in even numbers are more regularly distributed
in the meiotic mitoses than are those present in odd numbers.

Triploids and Trisomies. — In autotriploid plants the chromosomes
most commonly form trivalent groups in the meiotic prophase, although
the number of these is often rather variable.^ As described in an earlier
chapter (p. 274), the synaptic association in a given region ordinarily

5 Muller (1914); Blakeslee, Belling, and Farnham (1923); Haldane (1929, 19306).
Such computations have ordinarily been made on the basis of the distribution of four
chromosomes. Calculations based on the distribution of eight chromatids should
be more accurate; see Haldane.

^ Among researches on the cj^tology of triploid plants are those of Belling and
Blakeslee (1922, 1923, 1924a, 1926) and Belhng (19316) on Datura; Lesley (1926) on
Solarium; Ono (19276) and Tomowo (1927) on Primula; Newton and Darlington
(1927, 1929) and Darlington (1929c) on Tulipa, Belling (1929) and Darlington (19290
on Hyacinthus; Nagao (1929a6) on Narcissus; McClintock (1929a) on Zea; Hftkansson
(1926a), Capinpin (1930), and Catcheside (1931a, 1933a) on (Enothera; and Steere
(1932) on Petunia.

division in diploid, triploid,
and tetraploid sporocytes
of Datura. The lowest two
configurations in the 3n
column are rare. In the 4n
column the commonest types
are the figure of eight (mid-
dle) and the one below and
to the left of it. {After
Belling and Blakeslee, 1923.)

THE CYTOGENETICS OF AUTOHETEROPLOID PLANTS

353

involves a close union of only two of the three homologues, although one
of them may be synapsed with both of the others in different regions
(Figs. 159; 199, a to/). As chiasmata develop, the trivalent may assume
a rather complicated structure. If the three members remain associated
until the metaphase, the trivalent usually appears as a compact but
asymmetrical triple body in the equator of the spindle; but if only two
of the three chromosomes synapse or remain together, one of them may
appear at metaphase as a univalent while the two others constitute a
bivalent (Fig. 201, a). The chiasmata or points of contact between the
members of the trivalent at diakinesis and metaphase may be situated in
various positions along their length in some plants {Hyacinthus, Fig. 199),
while in others the association is practically always terminal {Datura,

Fig. 201. — Chromosomes in heteroploid maize. <i. nataphase /, showing three triva-
lents, seven bivalents, and one univalent. (Spot at upper left is not a chromosome.) b,
three trivalents in metaphase. c, trivalent disjoining two from one. d, tardily split uni-
valents ready to separate at equator of spindle. (After McClintock, 1929a.)

Fig. 200). The genetic data indicate that crossing-over may occur
between all three chromosomes (in different regions), that it takes place
when six chromatids are present, and that crossover values between
certain genes differ somewhat in diploids and triploids.'^

In the first meiotic mitosis the three members of a trivalent tend to
disjoin at random, except in those regions near the spindle-attachment
point where crossing-over may affect the type of disjunction. In the
second mitosis the halves of all of the chromosomes pass to opposite poles.
Often one chromosome of the group lags and is lost. Typically, as in
triploid Zea, the different trivalents are variously distributed in mitosis
/ (Fig. 201), so that spores are formed with chromosome numbers ranging
from the monoploid to the diploid. Although many of the microspores

' Bridges and Anderson (1925) and Redfield (1930, 1932) on Drosophila.

354 INTRODUCTION TO CYTOLOGY

and male gametes with unusual numbers may not function, especially in
competition with normal ones, the megaspores and female gametes are
more successful, so that plants with various chromosome numbers appear
among the progeny of a triploid. Meiotic irregularity may result in
almost complete sexual sterility in some triploid plants; these are often
propagated regularly by vegetative means.^

The behavior of a pair of Mendelian characters when three homologous
chromosomes are present is well illustrated in trisomic maize.^ In Zea
the smallest chromosome (number X) of the set carries a factor R for
colored aleurone; when the factor is recessive (r), it tends to make the
aleurone colorless. In the sporocytes of plants trisomic for this chromo-
some there are usually nine bivalents and one trivalent. The distribu-
tion of the three members of the trivalent is such that somewhat more
than half of the pollen grains carry the normal set of 10 chromosomes,
while the remainder (somewhat less than half because of lagging on the
part of the extra chromosome) carry 11, including two number X's.
However, the 11-chromosome grains do not germinate and develop pollen
tubes as rapidly as the competing normal ones, so that the 11-chromosome
male gametes tend to be eliminated. From this it follows that the extra
chromosome is practically always transmitted to the next generation
through the female gamete alone."'

On the basis of these facts it is possible to calculate the characteristic
ratios ^^ of types expected after selfing and back-crossing plants with
RRR ("triplex"), RRr ("duplex"), Rrr ("simplex"), and rrr ("nulli-
plex"). It is found that the results conform satisfactorily with the
expectations. Moreover, since the elimination of male gametes with an
extra chromosome is much more complete than that of the corresponding
female gametes, the ratios yielded by reciprocal crosses differ. In actual
tests the following results were obtained. When pollen from an Rrr

* E.g., Hyacinthus, Narcissus, Tulipa, Carina, Hemerocallis, and Rosa.

8H. Hill (1930), McClintock and Hill (1931).

1" The same is true in strains trisomic for chromosome II, which carries the B-lg
linkage group (Besley, 1930).

11 Blakeslee and Farnham (1923) calculated the ratios for Datura on the basis of a
random distribution, two from one, of the three members of the trisome concerned.
So calculated, the back-cross ratios for an Rrr maize plant would be IR.lr when the
trisomic plant is used as the female parent, and lR.2r when it is used as the male
parent. The corresponding ratios for an RRr plant would be 5:1 and 2:1. However,
if calculations are made on the basis of the random distribution of six chromatids, the
ratios tend to be 7: 8 and 1 : 2 for an Rrr plant, and 4:1 and 2:1 for an RRr plant. The
degree of approximation to these latter ratios may be expected to vary with the dis-
tance of the genes concerned from the spindle-attachment point, genes near this point
tending rather to give the ratios based on the distribution of three whole chromosomes.
This is because the chromatids in this region do not segregate at random, and show a
relatively low frequency of crossing-over (pp. 302, 323); hence only those genes located
far enough away from the spindle-attachment point to escape these restrictions
actually give the ratios based on random chromatid distribution.

THE CYTOGENETICS OF AUTOHETEROPLOID PLANTS 355

plant was placed on the silks of an rr plant, the ear produced 13 colored
and 27 colorless kernels (expectation, 1:2). Pollen from an RRr
plant on silks of an rr plant gave 646 colored and 355 colorless kernels
(expectation, 2:1). Pollen from a normal rr plant on the silks of an
RRr plant gave 819 colored and 213 colorless kernels (expectation, about
4:1). A certain amount of deviation from expected ratios in such
cases is due to the lagging and loss of the extra chromosome in meiosis,
so that the spores and gametes with n chromosomes actually outnumber
those with n -\- 1. This results in a deficiency of dominant plants among
the offspring.

In the foregoing example one dominant factor (R) is sufficient to
overcome the effect of two recessives (rr). Other genes are known of
which this is not true, the appearance of the triploid tissue depending
rather upon which type of factor outnumbers the other. ^^ In such cases,
of course, a different set of ratios is expected.

5 ^ « i <» M H S

Fig. 202. — Multivalent chromosomes in Prunus laurocerasus. {After Meurman, 19296.)

Other Heteroploids. — The cytological and genetical features of plants
with five or more homologous chromosomes or chromosome sets are not so
well known as those of triploids and tetraploids. The chromosome
configurations in meiosis are very variable. In the pentaploid Tulipa
Clusiana (60 chromosomes) there are univalents, bivalents, trivalents,
quadrivalents, and quinquevalents; but among these the quinquevalents
are least frequent and the bivalents most frequent. In the octoploid
Dahlia variabilis (64 chromosomes) there are bivalents, quadrivalents,
sexavalents, and octovalents, with the last named the least frequent.
In Dahlia Merckii with 36 chromosomes (4n + 4) there are quadrivalents
and two sexavalents, suggesting that the plant is a tetraploid with two
of the eight chromosomes of the set still further reduplicated. In
the 22/1 Prunus laurocerasus there are many multivalent associations,
with trivalents most. common (Fig. 202). Such variations in plants
not known to be truly autoheteroploid may be due in part to incomplete
homology. The genetic ratios observed in such plants will obviously
depend upon the strength of dominance, the manner in which the multi-
valents are distributed in meiosis, and the viability and fertility of the
various heteroploid gametes and zygotes. ^^

1^ East and Hayes (1915) on Zea endosperm, von Wettstein (1923) on triploid
moss gametophytes.

1^ Newton and Darlington (1929) on Tulipa, Lawrence (1929) on Dahlia, Meurman
(19296) on Prunus. Haldane (19306) gives expected genetic ratios for An, 6n, 8n,
lOn, 12/i, and 16« autopolyploid types.

\

^^

356 INTRODUCTION TO CYTOLOGY

Monoploid Sporophytes. — In a number of angiosperm genera,
individual plants have occasionally appeared with the gametic rather than
the zygotic number of somatic chromosomes. ^^ In several of these,
including Datura stramonium, Zea Mays, Crepis capillaris, (Enothera
Hookeri, and Triticum monococcum, it has been shown that the comple-
ment is truly monoploid (Fig. 203). The evidence at hand indicates that
such monoploid sporophytes, which are relatively rare, usually arise as the
result of the parthenogenetic development of the egg. Since only one
chromosome of each kind is present in the sporocyte, there is no normal

synapsis, all of the chromosomes appearing as univa-
^^^ ^^ lents at the end of the meiotic prophase. The dis-
7m^ tribution of these chromosomes is not the same in

• all cases. In Datura they are distributed at random

to the two poles in / and divide in //. Although
the plants are highly sterile as a result of this
irregularity, occasional spores with all 12 chromo-
somes are developed, so that selfing yields a few
diploid offspring. In CEnoihera Hookeri a random
distribution of the seven chromosomes occurs in
_ „„„ „ about one-quarter of the sporocytes; in the remainder

Fig. 203. — Somatic ^ , r

chromosome com pie- there is a Splitting and separation of some or even
ments from roots of ^^l of the chromosomes and a second splitting may

monoploid and diploid .t7-/t^i-\ t -h i-i

plants of Crepis capii- follow m // (Bleier). In the practically monoploid
laris {After Hoiiings- MattUola (7 + a fragment) some of the sporocytes

head, 1930c.) . ,. ., .

show irregular distribution oi the chromosomes,
while the majority show a splitting of all of them in the single
mitosis occurring. The dependence of fertility upon diploidy is well
illustrated by a monoploid and sterile Crepis plant which produced a
diploid and fertile branch. Even in this branch, however, synapsis was
somewhat deficient, indicating that diploidy and homozygosity do not
always insure fully normal meiotic regularity.

Other Features of Autoheteroploids. — Tetraploid mutants are
frequently somewhat larger than the corresponding diploids; this is true

1^ E.g., Datura (Blakeslee et al, 1922; Blakeslee and Cartledge, 1926, 1927; Belling
and Blakeslee, 1923, 1927); Crepis capillaris (Hollingshead, 1928a, 1930c); Matthiola
(Lesley and Frost, 1928); Nicntiana glutinosa (Goodspeed and Avery, 19296); Nico-
tiana tabacum (Clausen and Mann, 1924; Chipman and Goodspeed, 1927; Ruttle,
1928; see our p. 365); Solaniim (J0rgensen, 1928); Triticum (Gaines and Aase, 1926);
Lycopersicum (Lindstrom, 1929; Lindstrom and Koos, 1931); (Enothera (S. H. Emerson,
1929; Gates, 19296; Gates and Goodwin, 1930; Davis and Kulkarni, 1930; Bleier,
1933a; Catcheside, 1932); Zea (Stadler and Randolph, 1929; Randolph, 1932); Oryza
(Morinaga and Fukushima, 19316).

In his paper on (Enothera (1933o; see also 19336) Bleier classifies known sporophytes
with the gametic chromosome number (these he calls "haplodiplonts") according to
whether this number is truly monoploid or not, and discusses the bearing of their
chromosome behavior on certain problems of meiosis.

THE CYTOGENETICS OF AUTOHETEROPLOID PLANTS

357

of the "gigas" forms of Oenothera. Often diploids, triploids, and tetra-
ploids are of about the same size, but monoploids are almost always
noticeably smaller. Tetraploid species may even
be smaller than the related diploid species, as in
Plantago and Alyssum. Silene ciliata has 4n and 16n
races which are practically alike in appearance.
In a chromosomal chimera the portions with differ-
ent chromosome numbers may differ in size (Fig.
204). In some cases gigantism is associated with
an increase in the size of the chromosomes but
not in their number; this is true of Primula sinensis
and Phragmites communis. In moss gametophytes,
diploids tend to be larger than monoploids, and
tetraploids larger than diploids. Here the increase
in plant size is a compromise between a decrease
in the number of cells and an increase in their
volume, which tends to be proportional to the
number of chromosomes. In polyploid tulips the heads borne on mono-
surface area of the pollen grain and of its nucleus P^oid individuals of

p , , i • 11 -.1 ji 1 Crepis capillaris. Top:

is found to vary proportionally with the number monoploid head. Mid-
of chromosome sets. The monoploid, diploid, and die: diploid head. Bot-

, , 1 . 1 11 -1 1 ,- er, ni-r tom: chimeral head, with

tetraploid pollen grams show a volume ratio oi o : 27 : monoploid and diploid

64 (Fig. 205).^" sectors. (After HolHngs-

The histological structure of heteroploids usually
differs in certain respects from that of the corresponding diploids. In

Fig. 205. — Microspores of Tulipa suaveolens with 12 (monoploid), 24 (diploid), and 48
(tetraploid) chromosomes. (After de Mol, 1928d.)

Solanum the cells of the mesophyll, stomates, hairs, and vascular bundles
are all larger in the tetraploids, and the leaves are greener because of the

1^ Sinoto (1925) on Plantago, Jaretzky (1928a) on Alyssum, Blackburn (1927a) on
Silene, Gregory (1909, 1914) on Primula, Tischler (1918) on Phragmites, von Wettstein
(1923 et seq.) and Schratz (1924) on mosses, de Mol (1928d) on Tulipa, de Mol (19326)
on Narcissus.

358 INTRODUCTION TO CYTOLOGY

presence of the larger and more numerous chloroplasts. In Zea the mono-
ploid, diploid, tetraploid, and octoploid plants can be distinguished by
examining the size and distribution of the stomates. In Datura each of the
12 primary 2n + 1 mutants differs characteristically from all of the others
in its histological structure. ^*^ Aneuploid plants usually differ in appear-
ance from the normal diploid much more than do the tetraploids, triploids,
or other euploid forms. There is a "balance" within the complement which
is maintained even when three, four, five, or more sets are present, but
which is disturbed when any set lacks one or more of its members.

The effect of heteroploidy upon sexual fertility has already been
mentioned. Autotetraploids often show comparatively little sterility
because the chromosomes, although present in double the usual number,
are all able to form synaptic groups of pven number (bivalents or quadri-
valents), enabling the meiotic mitoses to be carried out without great
irregularity. In triploids, on the contrary, the odd number of elements in
the synaptic groups (trivalents) and the frequently unassociated univa-
lents interfere with proper meiotic distribution, so that a large proportion
of the spores or gametes are non-functional. In the higher euploid types
such as pentaploids, hexaploids, etc., the meiotic irregularity and sterility
tend to be rather great, especially in the ones with odd numbers of sets.
Thus in Rubus the pollen sterility is very low in in, 6n, and 8n forms, but
very high in 3n and 5n forms (Longley, 1927a). For similar reasons
aneuploid types tend to show considerable sterility. Frequently a change
to the heteroploid condition causes greater sterility in one sex than in the
other. Thus in a triploid (Enothera the eggs are apparently able to
function with any chromosome number from 7 to 14, whereas the only
male gametes functioning are those with either 7 or 14, because the pollen
grains with intermediate numbers abort (van Overeem, 1921, 1922).
In some heteroploids the sterility is so complete in one or both sexes that
the type cannot persist except through asexual propagation. This is
notably the case in heteroploids of hybrid constitution, as will be shown in
the next chapter. Asexual reproduction, however, is not necessarily an
indication of hybridity." The fact that organisms reproducing asexually
without effective meiosis show no Mendelian segregation affords strong
support to the chromosome theory of heredity. The effect of hetero-
ploidy upon the sexual development of the organism will be discussed
further in Chapter XXIII.

i" Winkler (1916) on Solarium, Randolph (1932) on Zea, Sinnott and Blakeslee
(1922) on Datura. See also Tupper and Bartlett (1916) on Oenothera.

'' Tischler (1928c) reviews many cases of spore sterility in angiosperms.

CHAPTER XXII
THE CYTOGENETICS OF HYBRIDS

In modern genetics the principal criterion of hybridity is heterozygos-
ity rather than the relative taxonomic standing of the parents known or
supposed to have been crossed. The union of any two protoplasts
differing in hereditary potency, no matter how slight the difference, con-
stitutes an act of hybridization in the fundamental sense. Accordingly,
a hybrid is defined as an individual arising from the union of genetically
dissimilar gametes^ and maintaining the resulting heterozygosity in its
somatic nuclei. Moreover, its spores and gametes are commonly of more
than one kind.

The degree of heterozygosity differs widely in different cases. It may
involve only one or relatively few genes, as in the ordinary intraspecific
hybrids so widely studied by geneticists; here there is usually no dis-
turbance of the normal pairing and distribution of the chromosomes in
meiosis. As will be shown below, the chromosomes in many interspecific
and even in some intergeneric hybrids may show a high degree of com-
patibility in both somatic development and meiosis, fertility not being
impaired in any considerable measure. In other instances, where the
chromosome sets brought together differ widely in genie composition,
the hybrid may undergo successful vegetative development and then
prove to be sexually sterile as a result of a partial or complete failure of
meiosis. This difficulty at the meiotic period commonly has its chief
visible expression in asynapsis or desynapsis (see p. 345), this being
followed by other irregularities which prevent the formation of func-
tional spores and gametes. Irregularities of this kind are even more
pronounced when the parental chromosome groups differ in number of
members as well as in genie composition. Deficient synapsis is not, how-
ever, wholly responsible for the sterility observed in hybrids, since
degenerative changes often begin well in advance of the synaptic period.

As a general rule, one may expect the difficulty of obtaining a hybrid
to increase with numerical and qualitative dissimilarities in the chromo-
some complements of the parental types. Failure may be due to the
inability of the pollen tube to grow properly in a "foreign" style, to a
lack of gametic interaction, to a developmental incapacity on the part

^ This holds for diploid and most other hybrids but not without qualification for
those of the amphidiploid type (see p. 369). It is understood that a hybrid individual
may also arise from a hybrid parent by vegetative means.

359

360 INTRODUCTION TO CYTOLOGY

of the zygote at some stage, or to unfavorable relations existing between
the embryo and the surrounding tissues. Even when a hybrid is obtained
it may prove to be sexually sterile, as pointed out above, and so fail to
maintain its type.

In earlier chapters we have dealt with ordinary Mendelian hybrids
and with those special cases in which heterozygosity is automatically
maintained by virtue of peculiar meiotic mechanisms and lethal factors
(p. 336). The present chapter is mainly a series of examples of the more
prevalent modes of chromosome behavior which have been observed
in hybrid plants derived from fairly wide crosses. The chief interest
of these phenomena is in the light they throw upon the causes of normal
chromosome behavior and upon the problem of the origin of new stable
and fertile types through hybridization. Most of the researches so
far cari'ied out in this field have dealt with meiotic phenomena and their
genetic results.^ Somatic chromosome complements have also been
studied, but relatively little attention has been devoted to syngamy in
such plants.

Diploid Hybrids with Good Synapsis and Fertility. — When Zea Mays
(n = 10) is crossed with the Durango or the Chalco race of Euchlcena
mexicana {n = 10), the fertile Fi hybrid shows 10 bivalents which behave
regularly in meiosis. In subsequent generations the parental types are
recovered among others, indicating a random distribution of the chromo-
somes and the occasional reconstitution of essentially normal Zea and
Euchlcena sets. Furthermore, some crossing-over occurs between the
Zea and Euchlama chromosomes. This high degree of chromosome com-
patibility, which is somewhat exceptional in interspecific or intergeneric
hybrids, doubtless indicates a close natural relationship between the two
parents. When a Florida race of Euchlcsna mexicana is crossed with
Zea, the hybrid shows some unequal chromosome pairs and considerable
sterility. Triploid hybrids formed by crossing Zea with the tetraploid
Euchlcena perennis show much meiotic irregularity and a rather high
degree of sterility.^

In the Lepidoptera fertile interspecific and intergeneric hybrids are
frequently obtained. For example, a hybrid between Charocampa
elpenor {n = 29) and Metopsilus porcellus (n = 29) shows regular synap-
sis and fertility, as well as the combined characters of the parents. In
moth hybrids the amount of synapsis varies with the closeness of relation-
ship of the parents (Federley, 1923, 1928).

That good synapsis alone does not insure complete fertility is shown
by hybrids between Pisum humile (n = 7) and P. sativum (n = 7).

^ For a more extensive account of chromosome behavior in polyploids and hybrids,
see Darlington (1932a).

^ Data in this paragraph are from Kuwada (1919), Longley (1924c), Beadle (1932c),
and Randolph.

THE CYTOGENETICS OF HYBRIDS

361

Here meiosis is regular in Fi, F2, and F3, but the high sterility and the
appearance of abnormal types in F2 and F3 indicate that many of the
combinations of humile and sativum chromosomes formed by random
assortment function poorly or fail completely in development (Lutkov,
1930). Certain Digitalis hybrids are also sterile in spite of good synapsis
(Haase-Bessell, 1932a).

Partial Asjoiapsis and Its Results. — Some varietal crosses in Viola
arvensis show regular Mendelian segregation, but others exhibit faulty
synapsis coupled with genetic irregularities. When V. arvensis (n = 17)
is crossed with V. tricolor {n = 13), the Fi hybrid shows various numbers
of bivalents and univalents, and some sterility. Later generations include

'A

A

4 ^^-^5 ■ ' 6 7 ^-^ 8

Fig. 206. — Chromosome behavior in F\ hybrid, Crepis capillaris X Crepis tectorum.
1, 2, 3, somatic complements of C. capillaris, C. tectorum, and C. capillaris X tectorum.
4, 5, first meiotic mitosis in hybrid. 6. 7, second meiotic mitosis. 8, group of microspores,
including an extra one formed after chromosome lagging. The satellite on the tectorum
D-chromosome does not show in the hybrid. (After H ollingshead , 1930a.)

the parental types and a number of new ones which are constant and
fertile (J. Clausen, 1924, 1926, 1931c).

Crepis tectorum (n = 4) X C. capillaris (n = 3) gives an Fi hybrid
in which all of the seven parental chromosomes can be distinguished on
the basis of their morphology (Fig. 206). For some reason, however, the
tectorum satellite is not evident in the hybrid. When one strain of
tectorum is used in this cross, three bivalents and one univalent appear
most often in meiosis, but when another strain is used this configuration is
least common. The univalents divide in either meiotic mitosis, and the
hybrid is almost completely sterile (Hollingshead, 1930a; M. Nawaschin,
19276).

Synapsis in Relation to Polyploidy in Hybrids. — Highly characteristic
of many hybrids is the type of meiosis first observed in Drosera by
Rosenberg (1904a, 19096). When Drosera rotundifolia (10 gametic
chromosomes) was crossed with D. longifolia (20 gametic chromosomes).

362

INTRODUCTION TO CYTOLOGY

the 30-chromosome hybrid {D. ohovata) showed 10 bivalents and 10
univalents in meiosis. Two interpretations of such synaptic behavior
were possible: (1) the rotundifolia chromosomes might have paired with 10
of those from longifolia (allosynapsis) , leaving the other 10 of longifolia
unpaired; (2) the longifolia chromosomes might have paired among
themselves (autosi/napsis) because of diploidy in the longifolia gametic
complement, leaving the rotundifolia chromosomes unpaired. Subse-
quent researches on a number of genera have shown that in some auto-

B

Fig. 207. — Chromosome behavior in Rosa hybrids. A, polar view of the chromosomes
in the metaphase of the first meiotic mitosis in the mierosporocyte of R. glanca dilatans,
showing 7 bivalents surrounded by 21 univalents. B, anaphase of mitosis / in R. glauca
plebeia; the bivalents have disjoined and the split univalents lie at the equator. C, late
anaphase in R. pomifcra Grenieri. D, division // in R. Junzillii; chromosomes which failed
to reach poles in I have formed an extra mitotic figure. E, telophase of // in the same,
showing the formation of supernumerary nuclei. F, polyspory (more than 4 spores)
resulting from mitotic irregularities in R. pomifera. {After Tackholm, 1922.)

synapsis, in others allosynapsis, and in still others both types of synapsis
may be the rule. Synapsis is generally regarded as an indication of
homology in the chromosomes involved, and when used judiciously this
criterion is a useful one in the analysis of hybrid chromosome complements.
An example of autosynapsis is afforded by 24-chromosome Crepis
hybrids formed by crossing C. setosa (4 in gamete) with C. biennis (20 in
gamete). In the microsporocytes of this hybrid there are 10 bivalents
and four univalents; this indicates autosynapsis among the chromosomes
of biennis, a polyploid species. Allosynapsis seems to obtain in the
asexually reproducing hybrids in the section Canince of the genus Rosa
(Fig. 207). In these hybrids, which have 28 (tetraploid), 35 (pentaploid),

THE CYTOGENETICS OF HYBRIDS 363

and 42 chromosomes (hexaploid), there are regularly seven bivalents in
the microsporocytes, the other chromosomes (14, 21, and 28 in the three
types) remaining unpaired. Evidently in each case a set of seven
descended from one gamete pairs with a set of seven from the other
gamete, leaving the extra sets unpaired. Both types of synapsis must
occur in hexaploid Papaver hybrids with 42 chromosomes formed by
crossing P. nudicaule (7 in gamete) with P. striatocarpum (35 in gamete).
These hybrids show 21 bivalents in meiosis, indicating a synapsis of all
six sets irrespective of gametic derivation. On the theory that synapsis
is determined mainly by homology, the nudicaule set of seven must be

u' 1^^ (Jar/ V ;^:

ABC B

Fig. 208. — The chromosomes of Triticum. A, metaphase of division / in T. mono-
coccum; 7 chromosomes. B, T. durum; 14 chromosomes. C, T. vulgare; 21 chromosomes.
D, division / in hybrid between members of emmer group (n = 14) and vulgare group
(n = 21); the 14 bivalents have disjoined and the 7 univalents are separating equationally.
(After Sax, 1922a.)

homologous with at least one set in striatocarpum, and the four other
sets of the latter species must be of but one or two kinds. In certain
Digitalis hybrids with 72 chromosomes (48 lutea + 24 micraniha) , 36
bivalents appear at diakinesis, indicating the occurrence of autosynapsis.''
The behavior of the chromosomes in meiosis when both bivalents and
univalents are present varies considerably in different cases. The
bivalents rather regularly disjoin in / and divide in II, but the univalents
behave more irregularly. In mitosis I they may wander at random as
wholes to the two poles {Drosera and some Triticum hybrids) ; or they may
split and occupy the equator, the daughter halves then separating pole-
ward (some Triticum hybrids and microsporocytes of Caninoc roses;
Figs. 207, 208); or some of them may distribute as wholes while the
others split and separate. This variable behavior seems to be associated
with the time at which the division of the univalent chromosome, partic-
ularly its spindle-attachment region, takes place. If the division is
sufficiently early, the univalent reacts by entering the equator and
separating; whereas, if the division is delayed, it fails to behave in such a
manner and tends to be carried toward the pole nearer which it happens

^ Collins and Mann (1923) on Crepis; Tackholm (1920, 1922) on Rosa; Ljungdahl
(1924) on Papaver; Haase-Bessell (1921, 1932a) on Digitalis.

364 INTRODUCTION TO CYTOLOGY

to lie. Rarely all of the univalents may pass to one pole (megasporocytes
of Canince roses). In mitosis II the chromosomes which disjoined as
bivalents in / split and separate, as in normal meiosis. The former
univalents may be distributed at random as wholes, or they may divide
and separate, sometimes even after having divided in /.^ Very often
one or more of the univalents may lag behind and fail to be included in
either daughter nucleus. They may then degenerate, but often they
form small nuclei about which small supernumerary spores ("micro-
cytes") are differentiated (Figs. 206, 207). Such cells are functionless.
Moreover, many of the spores and gametes which are viable carry very
abnormal chromosome complements. Hence plants with such meiotic
irregularities are characterized by considerable sterility and the produc-
tion of abnormal progeny.

The union of gametes with altered complements naturally leads to
diversity in the following generations. Many combinations do not result
in viable forms, but others give rise to types which develop normally until
meiosis, when chromosomal aberrations may again appear. In successive
hybrid generations meiotic irregularity and genetic instability are
observed as long as extra unpaired chromosomes are present. These
tend to be eliminated gradually through irregular mitoses, until relatively
stable types with one or more numbers of regular chromosome pairs are
established. Frequently, in the course of such adjustment through
elimination of extra chromosomes, some members of the complement
become lost while others are duplicated, so that, although the chromo-
some number of one of the original parents may be restored, the assort-
ment is a new one and the plants are correspondingly altered in character.
This again emphasizes the fact that it is the qualitative constitution of the
complement, rather than the mere number of chromosomes, that is of
primary significance in species alteration.

Analysis of Alloheteroploid Types. — The formation of bivalents
rather than multivalents in the euploid plants mentioned above is
attributed to dissimilarities in the chromosome sets, that is, some of the
sets are homologous enough to undergo synapsis, while others are not.
The plants in question are alloheteroploid, at least in part. This con-
dition is generally ascribed to hybridization. It is probable, however,
that in autopolyploid forms differences sometimes develop in the asso-
ciated sets through mutation, translocation, and the like, the differentia-
tion finally being great enough to prevent synapsis between the members
of certain sets. At the same time, there is evidence which points to the

^ Two successive splittings are reported for Hieracium (Rosenberg, 1917),
Raphanus X Brassica (Karpechenko, 19276), and Rosa (Tackholm, 1922; Hurst,
1931). The types of behavior on the part of unpaired elements in / are tabulated by
Tackholm.

THE CYTOGENETICS OF HYBRIDS 365

union of gametes carrying dissimilar sets as a more frequent cause of
allopolyploidy.

Although the degree of validity of this basis for the analysis of
chromosome complements is a subject of debate, certain cases may be
cited to illustrate the method. One of the best known is that of Nico-
tiana tabacum, which has 48 somatic chromosomes. When N. sylvestris
(12 in gamete) is crossed with N. tomentosa (12), the resulting hybrid
shows almost complete asynapsis among its 24 chromosomes. This is
taken to mean that the sylvestris set *S and the tomentosa set T are not
closely homologous. Similarly, the hybrid A'', sylvestris (12) X N.
rusbyi (12) shows no synapsis. When N. labacum (24) is crossed with
N. sylvestris (12), the 36-chromosome hybrid shows 12 bivalents and 12
univalents in meiosis. Also, when N. tabacum (24) is crossed with N.
tomentosa or N. rusbyi (12), the hybrid shows 12 bivalents and 12 uni-
valents. Finally, in the triple hybrid [tabacum (24) X rusbyi (12)] X syl-
vestris (12), there are 24 bivalents. From these data on synapsis it is
inferred that the gametic complement of N. tabacum actually consists of
two sets of 12, one of them being homologous with the tomentosa set {T)
and the other with the sylvestris (S) (or rusbyi) set. Hence N. tabacum
is an allotetraploid hybrid with the somatic composition TTSS, its
gametes carrying TS. It is believed to be a descendant of tomentosa
(or tomentosiformis) and sylvestris or closely related progenitors, the
cross being followed by chromosome doubling and the attainment of
stability and fertility." Other cases of this kind will be described in the
next section.

On the basis of genetic data and synaptic behavior, Hurst has
advanced the theory that in the genus Rosa there are five fundamental
diploid species, each with its characteristic set of seven chromosomes.
The diploid somatic complements of these species may be represented as
A A, BB, CC, DD, and EE. Multiplication of any one of the sets gives
autopolyploid "varieties," such as AAA A or DDD. Hybridization leads
to the establishment of allopolyploid ''species." These may be "regu-
lar," with bivalents only {e.g., A A BB, or AA DD EE); or "irregular,"
with bivalents and univalents (e.g., AA B D E,ov AA CC E). Although
the limits of the applicability of this theory are not agreed upon by all
workers, the responsibility of hybridization for the production of many
known rose types is unmistakable.'^

On similar grounds Morinaga (1928, 1929) postulates the occurrence
of three kinds of basic set in Brassica: A, with 10 chromosomes; B,
with 8; C, with 9. Synaptic behavior in hybrids and the numbers present

«R. E. Clausen and Goodspeed (1925), Goodspeed and Clausen (19276, 1928),
Brieger (1930), Clausen (1932). See the criticism by East (1933).

^ Hurst (1925 et seq.), Erlanson (1929, 1931o6), Harrison and Blackburn (1927),
Blackburn and Harrison (19246), Blackburn (1925).

366 INTRODUCTION TO CYTOLOGY

suggest that the gametic complements of certain species are made up as
follows: cernua, AB; chinensis, A; Rapa, A; Napella, AC. The hybrids
tend to resemble the parent with the higher chromosome number.

Very extensive studies of this kind have been made upon Triticum
and the closely related genus Mgilops.^ In Triticum the three main
groups of species are characterized by different chromosome numbers.
In the einkorn wheats {monococcum, villosum, cegilopoides) the gametic
number is 7; in the emmer wheats {dicoccum, polonicum, turgidum,
durum) the gametic number is 14; in the spelt wheats (vidgare, compactum,
spelta) the gametic number is 21. In many of the hybrids between
members of these groups, as well as in those between Triticum and
^gilops, the chromosomes tend very strongly to form a characteristic
number of bivalents and univalents, as in Drosera and other cases men-
tioned on foregoing pages. There is, however, some variation in behavior
under different conditions.

On the basis of the synaptic relations exhibited, the theory has been
developed'' that the chromosome complements of Triticum and /Egilops
combine in various ways as many as five different but related sets of 7
(A, B, C, D, E). In Thompson's recent tabulation these sets are pres-
ent as follows in the gametic complements: einkorns. A; emmers, AB;
spelts, ABC; /Egilops cylindrica, CD; M. ovata, DE; /E. crassa, C. Other
species of /Egilops have less certain combinations, and Secale (rye) has Z).

Studies on the morphology of Triticum chromosomes suggest that the
species with the larger numbers of sets are not simply autopolyploid
derivatives of some ancestor with two similar somatic sets, for in four
species about 17 different types of chromosome are found (Kagawa).
Some types appear in only one of the species, while others appear in two,
three, or four. This suggests hybridization in the differentiation of
such species. On the other hand, the chromosomes in certain crosses
may undergo synapsis in spite of their differences in type, which points to
translocation and deletions as probable causes of some of the cytological
diversities in the members of this genus. That synaptic behavior is a
reliable measure of relationship in grains is questioned by Bleier, who
lays emphasis on the probable role of the spindle substance in determining
irregular meiosis in hybrids (1930c, 1931a). Furthermore, it is to be
borne in mind that failure to pair may often be due not so much to lack

8 Sax (1922 et seq.), Watkins (1924 et seq.), Kihara (1919 et seq.), Gaines and Aase
(192G), Kagawa (1927afe, 1929ac), Bleier (1928a6, I930acd, I93ld), W. P. Thompson
(1926 et seq.), Melburn and Thompson (1927), Huskins (1928a6), Jenkins (1929),
Percival (1930), Tschermak and Bleier (1926), Tschermak (1929), Kihara and Nishi-
yama (1928, 1930a), Kihara and Katayama (1931). For convenient general accounts,
see Aase (1930), Watkins (1930), and Thompson (19316). See also footnote 13, p. 342.

9 Gaines and Aase (1926), Sax (1928), Kihara (1928), Thompson (19316), Kihara
and LiUenfeld (1932).

THE CYTOGENETICS OF HYBRIDS 367

of homology as to conditions affecting the relative rate of development of
the various chromosomes in the prophase or to one of the modifying
influences mentioned at page 273.

Amphidiploid Hybrids. — Primula floribunda (n = 9) was crossed
with P. verticillata {n = 9), producing a sterile Fi hybrid with 18 somatic
chromosomes. From this plant there arose a bud sport known as P.
Kewensis; this was found to be tetraploid (36 chromosomes) and fertile.
Since the tetraploid condition arose through some form of somatic
chromosome doubling in the Fi, P. Kewensis has
two florihunda and two verticillata chromosome
sets. It is said to be amphidiploid, since it is
diploid for each kind of set present. It is also
said to be allotetraploid, because it has four sets c^
of nine which are in part unlike (see p. 340).
Such forms are called "sexual nuclear chimeras"
by Tschermak. In some such cases the original Fig. 209. — Somatic
parental sets do not have the same number of o^r-TaSdipS c"el!i-*
chromosomes (Fig. 209). For example, Nicotiana capHiaris x c. tectomm
glulinom (n = 12) X N. tabacum (« = 24) gave ^jts"to^* ::Srtr.lZ
in F2 the fertile amphidiploid N. digluta with 72 species. Satellites on tec-

1 rpi • ,1 n J. u I, u -J torum D-chromosomes do

chromosomes. This was the first such hybrid ^^^ g^ow at metaphase in
whose cytological constitution was understood, this hybrid. {After hoI-
Amphidiploidy is one of the most significant of ^^^^ ^^ '
all cytological phenomena in hybrids because of its evident relation to
the origin of new fertile types. Several such fertile amphidiploids are
now known, ^^ among which the following are of much interest.

Raphanus sativus (radish; n = 9) was crossed with Brassica oleracea
(cabbage; n = 9). In some of the sporocytes of the Fi hybrids the 18
chromosomes showed deficient synapsis and other irregularities, giving
various numbers in the spores (Fig. 210). In some of these were all
18 chromosomes, and from the union of such gametes there were obtained
F2 plants with 36. These amphidiploid plants, with two radish and two
cabbage sets, were fertile, and they differed in character from their

^'^ Primula Kewensis (Digby, 1912; Newton and Pellew, 1929); Raphanus X
Brassica (Karpechenko, 1924a6, 1927o6; Karpechenko and Shchavinskaia, 1930);
Triticum X Mgilops (Tschermak and Bleier, 1926; Kagawa, 1928, 1929; Tschermak,
1929, 1930; Taylor and Leighty, 1931); Fragaria (Ichijima, 1926); Nicotiana (Clausen
and Groodspeed, 1925; Rybin, 1927, 1929); Rosa Wilsoni (Blackburn and Harrison,
19246); Brassica (Frandsen and Winge, 1932); Digitalis (Buxton and Newton, 1928;
Buxton and Darlington, 1931); Aquilegia (Skalinska, 1932); Spartina (Huskins, 1931c).
Amphidiploids which are largely or completely sterile are known in Nicotiana (Lam-
merts, 1931, 1932), Solanum (j0rgensen, 1928), Triticum X Secale (Lewitsky and
Benetzkaja, 1930, 1931), Crepis (Babcock and Nawaschin, 1930; Holhngshead, 1930a;
Poole, 1931, 1932), and Saxifraga (Marsden-Jones and Turrill, 1930). Winge (1932)
r^\'i:;ws most of the known cases.

368

INTRODUCTION TO CYTOLOGY

parents. Moreover, only with difficulty could they be crossed with the
parents, and the few offspring obtained were highly sterile; hence they
had the sexual isolation which aids in the establishment of new independ-
ent types. The type was given the new generic name Raphanobrassica.
Other heteroploid types were obtained also; these will be discussed later
in the chapter.

After crossing Triticum durum (n = 14) with /Egilops ovata {n = 14),
it was found that the Fe plants were fertile, genetically stable, and

amphidiploid (56 chromosomes).^^ The
type was named i-Egilotricum (Tschermak
and Bleier). Since the F\ of such a cross
was later found to be diploid (28), it is
probable that it produced diploid spores
through some form of ameiosis (Kagawa).
Certain other Tinticum-Jilgilops hybrids
are more variable in later generations
(Taylor and Leighty). Triticum turgidum
{n = 14) X Triticum villosum (n = 7) gave
a constant and fertile hybrid with 42
chromosomes (Tschermak). By crossing
this hybrid with /Egilotricum, there was
obtained a plant combining the gametic
complements of four species (Berg, 193 1&).
In the notation given on page 366, the
somatic formula of this plant would be
AAABBDE. A fertile, balanced hybrid
between Triticum and Secale is reported
by Lebedeff (1932).

Nicotiana tabacum {n = 24) crossed
-Diagram of mitoses with N. sylvesfris {n = 12) gave a sterile

in microsporocytes of Fi hybrids of
Raphanus sativus X Brassica oleracea.
A, usual course of divisions, form-
ing monoploid spores. B, forma-

B

Fig

tion of diploid spores following
"asynapsis." {After Karpechenko,
1927a.)

Fi hybrid with 36 chromosomes. A
branch of this plant was treated with
chloroform vapor 8 days before the open-
ing of the flower. Self-pollination then
resulted in the production of a single

seed, which grew into a fertile plant with 72 chromosomes. Probably

the chloroform treatment induced ameiosis, leading to amphidiploidy

(Rybin).

The formation of unreduced gametes is also known in moth hybrids.

Pygcera anachoreta {n = 30) X P. curtula (n = 29) gave anFi hybrid with

^^ If, as suggested by the theory mentioned on p. 366. Triticum durum and jEgilops
ovata may be regarded as amphidiploids with the somatic formulae A ABB and DDEE,
respectively, the 56-chromosome hybrid formed by crossing them would be amphi-
diploid in the second degree: it would be an allo-octoploid with the formula
AABBDDEE.

THE CYTOGENETICS OF HYBRIDS 369

little or no synapsis in its spermatocytes. The chromosomes divided in
both meiotic mitoses, giving gametes with all of the 59 chromosomes.
No allotetraploid type was obtained, but allotriploids resulted from back-
crossing the hybrid to one parent. ^^

From the foregoing examples it can be concluded that amphidiploidy
may arise if the two unlike chromosome sets brought together in a cross
are compatible enough to exist together in the zygote and if the chromo-
somes then become doubled in some manner. The role of interaction
of homologous elements in the origin of such alloheteroploid types is
conceived by Winge (1917) as follows. When two specifically different
chromosome sets of like number are brought together, they may some-
times act in complete harmony at all stages of somatic development and
meiosis so that a new sexually reproducing hybrid type results. If the
compatibility of the chromosomes is less, the chromosomes, after having
cooperated throughout somatic development, synapse poorly or not at all
in the sporocytes so that diploid spores and gametes are formed. Finally,
if the compatibility is insufficient for the "action in pairs" favoring the
development of the diploid soma, all of the chromosomes in the zygote
or early embryo may split, the resulting halves then acting as homologous
pairs in the development of the resulting allotetraploid individual. Such
an individual may reproduce sexually as a "permanent hybrid" if it
produces diploid spores and gametes after meiosis. ^^ If meiosis and
sporogenesis fail, the tetraploid type may reproduce by asexual means
alone or disappear altogether. These several conditions are observed
in nature, and the interpretation outlined above harmonizes well with
certain phenomena in apomictic diploid plants (p. 407).

In some cases there is a doubling of the chromosomes of one parent
only. Thus Saccharum officinarum 9 {n = 40) X S. sponianeum cf
(n = 56) gave a fertile hybrid with 136 chromosomes, the set of 40 from
officinarum evidently having doubled in the zygote. When this hybrid
was back-crossed as pollen parent to S. officinarum, the progeny showed
about 148 chromosomes, indicating that the officinarum chromosomes had
again doubled (Bremer, 1928a).

Because of their cytological and genetical constitution, alloheteroploid
plants may be expected to differ in many ways from autoheteroploid ones.
An autotetraploid, for example, may differ from its corresponding diploid
mainly in a quantitative way, whereas an allotetraploid usually shows
qualitative peculiarities of character due to the combination of unlike
elements. Instead of forming quadri valents as in typical autotetraploids,
the allotetraploid types ordinarily form bivalents like a diploid, although

^^ Federley (1913 et seq.). See his general account (1928).

^^ Thus an individual of hybrid constitution may arise from the union of gametes
which are genetically similar (cf. p. 359), but here the gametes themselves are hybrid
in character.

370

INTRODUCTION TO CYTOLOGY

quadruple groupings sometimes occur, particularly when the species
crossed are nearly related. The fertile allotetraploid tends to breed

18 R

9R + 9B

18R + 9B I8R+18B 27R + 18B 24R + 27B

Fig. 211. — Correlation of seed pod characters with chromosome constitution in Rap-
hanus X Brassica. A, Raphanus sativus: upper, non-dehiscent seed-bearing part large;
lower part small and mostly seedless. B, Brassica oleracea: upper part nearly seedless;
lower part much elongated, with seeds. C, diploid Fi hybrid between A and B: upper and
lower parts about equal in size. D, F, triploid and pentaploid types derived from cross
of A and C: each has more Raphanus than Brassica chromosomes, and upper part of pod
is larger. E, fertile tetraploid type {Raphanobrassica) obtained by selfing C: two sets of
chromosomes from each grandparent; capsule parts about equal in size. G, hypohexaploid
type somewhat deficient in Raphanus chromosomes. {After Karpechenko, 1927b.)

true, apparently because of the regular pairing between chromosomes
from similar sets (autosynapsis) and their regular distribution. The
occasional segregation of differing types, as in Primula and Aquilegia, is

THE CYTOGENETICS OF HYBRIDS 371

attributed to the synapsis of chromosomes from dissimilar sets in the
complement (allosynapsis) or to secondary pairing and atypical distribu-
tion of autosynaptic pairs. Studies on such alloheteroploid plants, taken
together with comparisons of the conditions observed in many related
species in nature, have strengthened the theory that amphidiploidy has
played an important role in the differentiation of species.

Parental Characters in Polyploid Hybrids. — There is a marked
tendency on the part of polyploid plants of hybrid origin to show a greater
resemblance to the parent contributing the larger number of chromosome
sets. In crosses between Raphanus and Brassica the sterile Fi hybrid
with one set from each parent (RB) is intermediate in capsule characters
(except size) (Fig. 211). The fertile F2 Raphanobrassica with two sets of
each kind (RRBB) and a hexaploid with three of each kind {RRRBBB)
are intermediate also. A pentaploid form with RRRBB is somewhat
more like Raphanus, while the resemblance is still greater in a triploid
(RRB). Thus is the ratio of parental chromosome sets reflected in
external characters (Karpechenko, 19276).

When Rubus rustica inermis, a diploid species, was crossed with
R. thyrsiger, a tetraploid, three Fi hybrids were obtained. Two of these
were triploid (TTR) and resembled R. thyrsiger, while the third was tetra-
ploid {TTRR) and was more like R. rustica inermis. The tetraploid
probably arose from a diploid egg produced by rustica after some meiotic
aberration (Darlington, 1929/).

Euchlcena mexicana {n = 10) crossed with Zea Mays (n = 10) gave
an intermediate hybrid with one set from each parent {EZ). The tetra-
ploid E. perennis (gametic number = 20) when similarly crossed to Zea
gave a triploid hybrid (EEZ) which was more like Euchlcena. One plant
in the progeny of this cross was considerably more like Zea, and cyto-
logical examination showed it to be tetraploid. Presumably the fourth
set was formed from the Zea set by doubling, giving the formula EEZZ
and a more even balance between the characters of the two parents (R.
Emerson and Beadle, 1930).

The same phenomenon is manifested by polyploid moss hybrids. In
hybrids between Physcomitrella patens and Funaria hygrometrica the
peristome of the capsule becomes less like that of the former genus
(P-) and more like that of the latter {F-) in passing through the series
P\ P^F\ PW\ P^F\ PW\ P^F'', P-F', P'F\ F- (von Wettstein, 1926). In
narrow crosses in mosses the degree of dominance is roughly proportional
to the relative number of dominant genes, whereas in wide crosses (specific
or generic) it may increase up to a certain ratio and then decrease. This
is attributed to differences in the parental cytoplasms (von Wettsiein,
1927).

In hybrids between Crepis capillaris {n = 3) and C. aspera (rv = 4)
where a doubling of one chromosome set has occurred, it is found that

372 INTRODUCTION TO CYTOLOGY

10-chromosome plants with one aspera and two capillaris sets (ACC) are
more like capillaris, while 11-chromosome plants with the formula A AC
are more like aspera. A triple hybrid involving these two species and C.
setosa (ACS) showed certain setosa characters (M. Nawaschin, 19276).
Similarly, in hybrids between C. fectorum and C. alpina the characters of
the achenes vary according to the numbers of parental chromosome sets
involved (M. Nawaschin, 19306).

Segregation of Parental Chromosome Sets. — It frequently happens
that when a hybrid forms spores and gametes, only those which contain
a complete chromosome set from one parental species or the other are
functional. Or, if the gametes carry various combinations, possibly
only those zygotes survive which have two complete sets, be they of one
or of both species. In a Crepis tedorum and C. alpina cross like that just
mentioned, the only three plants obtained in F2 contained, respectively,
two tedorum sets (TT), two alpina sets {A A), and one of each (TA).
Of further interest is the fact that the F2 plant with two alpina sets was
precisely like the original alpina plant, notwithstanding the fact that its
cytoplasm had been derived from tedorum (M. Nawaschin, 1927a).

In a Crepis hybrid containing two capillaris sets and one tedorum
set, the six capillaris chromosomes formed three bivalents at meiosis,
leaving the four of tedorum as univalents. Although most or all of the
female gametes formed by this hybrid were able to function, only those
male gametes with none or all of the tedorum chromosomes were func-
tional. F2 plants with one or more tedorum chromosomes were less viable
than those with capillaris chromosomes only (Hollingshead, 1930a).
These facts all emphasize the importance of "balance" in the chromosome
complement, particularly in the pollen.

A Fertile Tetraploid Obtained through a Sterile Triploid. — In the
genus Galeopsis the gametic chromosome numbers of four species are as
follows: puhescens, 8; speciosa, 8; tetrahit, 16; bifida, 16. In the progeny
of a cross between puhescens and speciosa was an almost completely
sterile triploid plant with 24 somatic chromosomes. When this plant
was pollinated with puhescens pollen, a single seed was obtained; this
grew into a fertile plant with 32 somatic chromosomes, of which 24 were
probably contributed by a triploid gamete from the triploid plant and 8
by the gamete from puhescens. The plant would not cross with either
puhescens or speciosa, although it crossed readily with either tetrahit or
bifida. It was morphologically and genetically indistinguishable from G.
tetrahit, and it had the same chromosome number. It was therefore called
"artificial tetrahit"; and Miintzing (19306) described it as "the first case
where a Linnaan species has been synthesized by means of species
hybridization and chromosome summation."

Conclusions. — The observational and experimental evidence reviewed
in these chapters indicates that distinct heritable changes in the char-

THE CYTOGENETICS OF HYBRIDS 373

acters of organisms may involve Mendelian recombinations of genetic
factors, or genes, actual mutations of these genes, alterations in the
number and assortment of chromosomes as results of aberrations in
mitotic behavior, and hybridization, by which many new combinations
are produced. Any stable sexual type is characterized by a chromosome
complement consisting of a certain number and assortment of elements
showing individual functional and morphological differences; all of them
constitute a balanced, harmonious system. Any change in the constitu-
tion of this system, whether quantitative or qualitative, large or small,
is accompanied by a corresponding alteration of the type, although this
alteration is not always immediately visible.

With regard to the role of genes and their mutation in the origin of
species, Morgan (1923c) points out that the inheritance of the results
of gene mutations as Mendelian characters suggests the origin of
Mendelian differences in general in such mutations. "It is . . . now
clear that these smaller mutant variations must be those small heritable
variations that Darwin himself appealed to as furnishing the materials
for organic evolution. " These must not be confused with non-inherited
environmental variations. In reply to the objection that changes due to
gene mutations are too trivial to be of significance in evolution, Morgan
further points out that the minor superficial characters used by the genet-
icist and the taxonomist may often be secondary results of changes which
have some invisible but more fundamental physiological effects with an
actual survival value. Moreover, "useless" characters may be closely
linked with "useful" ones. The systematist of necessity distinguishes
many species on the basis of characters which have played no part in the
actual production of those species.

Change of type is effected not only by such mutations of genes and
their Mendelian recombination through normal chromosome distribu-
tion but also by more extensive and less orderly alterations in the grouping
and interaction of inheritance materials through abnormalities in chromo-
some behavior. Non-division, non-disjunction, translocation, and other
aberrations all play roles in the production of new chromosome comple-
ments which differ from the original complements in the number, size,
and assortment of their constituent elements. The range of variation is
greatly increased by crossing among the altered types. It seems abun-
dantly evident that hybridization involving types with chromosomes
that are in some measure incompatible is one of the chief causes of chromo-
somal aberrations leading to the establishment of qualitatively new gene
systems. The irregularities in chromosome behavior immediately
following such crossing gradually disappear in subsequent inbred genera-
tions through the elimination of unpaired chromosomes, until there may
remain a chromosome complement whose members act in harmony,
although they may constitute a very new type of interacting system.

374 INTRODUCTION TO CYTOLOGY

In more general terms, hybridization, or outcrossing, plays its chief
role by inducing variabihty in immediately subsequent generations, the
amount of variability depending on the degree of constitutional difference
between the types involved. If free intercrossing with the parental and
other types continues, the variability is kept up. In order for stable
types to differentiate from the series of variants, crossing must be
restricted by some form of isolation, such as natural or artificial selection,
geographic isolation, intersterility, and the like, whereupon some of the
inbreeding types rapidly become stable. The origin of species is thus
frequently conceived as a fixation of stable independent types through
the inbreeding of variable types originally resulting from hybridization.
We have also seen that hybridization, if accompanied by chromosome
doubling, may yield new and stable types almost at once.

Since hybridization has long been recognized as an important cause
of diversity in organisms, it may be well to summarize the contributions
which cytology has made in this connection. Cytology has shown the
close relation between hybridization and heteroploidy, between hetero-
ploidy and certain classes of mutations, and hence between hybridization
and such mutations. In its elucidation of chromosome aberrations in
hybrids it has thrown much light on the curious behavior of inherited
characters in hybrid lines; the apparently non-Mendelian inheritance in
crosses between species, varieties, and mutants, the genetic constancy of
certain hybrids, the unexpected gametic ratios frequently obtained, the
unlikeness of reciprocal hybrids, sterility, and a variety of otherwise
unintelligible phenomena. It has heightened the precision with which
certain changes in character can be attributed to crossing, often affording
real proof in the case of suspected hybrids. It has shown the value of
cytological data in determining taxonomic relationships within narrow
circles of affinity and the prime necessity of utilizing such data in many
problematic cases. It has shown the importance of apomixis and somatic
mutation as factors in heredity and hence their importance to the
geneticist and field taxonomist. In short, cytology has afforded a com-
mon rationale for a great variety of phenomena hitherto studied by dis-
tinct groups of biologists.

CHAPTER XXIII

CHROMOSOMES AND SEX

During the closing decades of the nineteenth century many researches
were carried out in the hope of identifying the controlUng agency in
sex determination with one or more of the environmental factors. The
effects of light, temperature, moisture, and nutrition were examined,
and although a number of workers believed their methods to be in a
certain measure successful, the results were on the whole inconclusive.
The period during which sex was thus looked upon as a character more or
less under the control of the environmental factors was succeeded by one
in which it came to be regarded as something regulated mainly by some
internal mechanism or condition, and as relatively unalterable by external
agencies. This conclusion, definitely reached by Cuenot (1899) for
animals and by Strasburger (1900c) for plants, received the support of a
number of experimental researches on animals and dioecious plants. It
was further strengthened by the discovery that in many organisms males
and females differ visibly in their chromosome complements.

The modern interpretation of sex determination combines the elements
of truth in both of these theories. The course of development in an
organism is dependent on a series of interactions between a protoplasmic
system of a certain kind and a particular group of environmental con-
ditions. It is found that the differentiation of sex, like that of any other
character, involves the action of both internal and external factors. In
some cases the tendency to develop one sex or the other is so strongly
set by the internal factors that it can be modified only with difficulty,
if at all, by altering the external factors; whereas in other cases the
internal factors are so balanced that the course of differentiation can be
thrown toward either sex with comparative ease by altering the environ-
ment in which the individual develops.

Sex-chromosomes in Animals. — In a great many animals it has been
found that the approximate numerical equality of males and females is
related to the fact that the gametes of one sex (more commonly the male)
are of two kinds, the sex of the offspring depending upon which kind
happens to function in syngamy. The difference in the two kinds of
gamete is often due to the meiotic disjunction of the unlike members of a
distinguishable pair of chromosomes which evidently play a special role
in sex determination. Such chromosomes are known as sex-chromosomes;

375

376 INTRODUCTION TO CYTOLOGY

the other members of the complement are called autosomes. Typical
examples of sex-chromosomes in animals are given below. ^

In 1891 Henking noticed that half of the spermatids of Pyrrhocoris
apterus, an insect, contain a body which he thought might be a nucleolus.
It was subsequently shown- that this supposed nucleolus is an "accessory
chromosome" which remains compact while the other chromosomes
become diffused or reticulate in form. That this accessory chromosome
exerts a special influence in sexual differentiation was suggested by
McClung (1901, 1902) and proved by him and many other observers.

When some of the sperms have one sex-chromosome (X) and the
others none, the animal is said to show the " XO type" of sex-chromosome
differentiation. A good example is Protenor helfragei, a bug'' (Fig. 212).
In the somatic nuclei and spermatogonia of the male there are six pairs
of autosomes and a single unpaired X-chromosome. The autosomes
undergo disjunction in / as usual and divide equationally in //, but the
X-chromosome divides in I and passes undivided to one pole in //.
Two sperms of the quartet receive one X each, while the other two
receive none. In the female somatic cells and the oocytes there are two
X-chromosomes besides the autosomes; every egg receives one X.
Fertilization by a spermatozoon with an X results in a female with two
Xs, whereas that by one with no X results in a male with only one. In a
number of insects, domesticated mammals, and lizards, the X-chromo-
some passes undivided to one pole in / and divides in //, the end result
being the same as in Protenor.* The plotted measurements of the
spermatozoa of Canis form a bimodal curve, the indicated size dimor-
phism probably being associated with the chromosomal difference.^

Two variants of the XO type are found in the nematode genus Ascaris.
In A. megalocephala bivalens (Fig. 212) there are in the spermatocyte
four autosomes and a single small X, which is usually attached to the
end of one of the autosomes. The X passes undivided to one pole in /
and divides in //; hence it is present in half of the spermatozoa. In
the oocyte there are two such X-chromosomes, which disjoin in / and
divide in II, every egg thus receiving one. Fertilizations of eggs by
sperms with and without an X result in females and males, respectively.

1 For extensive reviews, see Crew (1927c), F. Schrader (1928), Wilson (1925), and
Witschi (1929). See M. Hartmann (19296, 1930) on Protista.

2 McClung (1899), Paulmier (1899), de Sinety (1901), Montgomery (1901).

3 Montgomery (1901), Wilson (1906), Morrill (1910).

■* The behavior of sex-chromosomes in / and // is tabulated by Wilson (1925). A
tendency on the part of the X to lag may result in both modes of distribution in the
same species (Edwards, 1910).

5 Malone (1918) on the dog. Other reports of XO type: Wodsedalek (1913, 1914,
1920, 1922) on horses, sheep, pigs, and cattle; Masui (1919a6) on horses and cattle;
Painter (1920, 19216) on lizards; GuHck (1911) and Mulsow (1912) on nematodes;
Brauer (1928) on Bruchus; and Mols (1928) on guinea pig. See also next footnote.

CHROMOSOMES AND SEX

377

XO PROTENOR

Y o A5CfM\l5 LUn.

XY DR050PHILA

Fig. 212. — Several types of sex-chromosome behavior in animals with heterogametic
males. For the sake of clearness all are shown with two pairs of autosomes. Sex-chromo-
somes in the female are shown disjoining in the same mitosis as in the male, though this is
not known to occur in all five cases.

378 INTRODUCTION TO CYTOLOGY

A. lumbricoides has in the male an X-complex made up of five elements
(Fig. 212). All five pass to one pole in /, and two classes of spermatozoa
are formed, with 19 and 24 chromosomes respectively. This is some-
times referred to as the " XnO type."^

The "XF type" is well exemplified by Drosophila. In D. melano-
gaster the somatic complement comprises four chromosome pairs, includ-
ing a pair of sex-chromosomes (Figs. 196, 212). In the female the two
members of this pair are alike {XX), while in the male they differ slightly
in size and greatly in function (XF). Owing to disjunction in meiosis,
half of the sperms carry X and half carry Y, while every egg has X.
Fertilization of an egg by an X-sperm results in a female with XX, while
that by a F-sperm results in a male with XYJ In some genera the X
and F divide equationally in I and disjoin in II. It will be shown later
in the chapter that sex is correlated with the ratio of X-chromosomes to
autosome pairs, rather than with the simple presence of X' or F or the
number of X's.

The XF type is the most prevalent form of sex-chromosome differen-
tiation in animals. Like the XO type, it is best known in insects and
mammals,^ including man. In a number of cases the genetic evidence
indicates the presence of an XF pair,^ although it has not been possible
to identify it with the microscope. Apparently the sex-chromosomes
are often not visibly differentiated from the other members of the comple-
ment. A variant of the XF type is seen in Prionidus, in which the X
is represented by three small elements (Fig. 212). In the female there
are six of these X-elements, while in the male there are three X-elements
and a F. In spermatogenesis the X-elements disjoin from the Fin 77. i"

^ Works on sex-chromosomes in Ascaris: Boveri (19096), Boring (1909), Edwards
(1910, 1911), Frolowa (1912), Walton (1918, 1921, 1924). Walton concludes from
his extensive researches on nematodes that each autosome in A. megalocephala is equiv-
alent to 22 somatic chromosomes, and that the X is equivalent to 8. Sex-chromo-
somes attached to autosomes are also reported for Choaborus plumicornis (Frolowa,
19296).

'Stevens (1907, 1908a), Morgan (1911), Metz (1914). In Drosophila Willistoni
it has been shown by Lancefield and Metz (1921, 1922) that the sex-chromosomes are
represented by one of the large bent pairs rather than the shorter rod-shaped pair; and
there is evidence in the linkage of genetic factors that the rod-shaped chromosome of
melanogaster corresponds to one arm of the large bent sex-chromosome in Willistoni
and obscura.

8 Works on mammals: Painter (1921a, 19226) on opposum, (1922a, 19236) on mon-
keys, (1926) on rabbit; Agar (1923), Greenwood (1923) and Saez (1930c) on mar-
supials; Cox (1926) and Minouchi (1928e) on the mouse; Minouchi (1928c) and
Pincus (1928) on the rat; Starks (1928) on the seal; Minouchi (1928a) on the cat.
Winiwarter and Sainmont (1909) reported XO in the cat.

'E.g., in the fish genera Lebistes (J. Schmidt, 1920; Winge, 1922, 1923a, 19276,
19306; Vaupel, 1929; Iriki, 1932) and Aplocheilus (Aida, 1921, 1930; Iriki, 1932).

^° Payne (1909). Several other cases of this XnY type of differentiation are known.
In the Mantidse the X-complex consists of two elements, the male having 24 -|- Xa YXb
and the female 24 + XaXaXbXb (King, 1931; Oguma, 1921).

i

CHROMOSOMES AND SEX

379

The number of chromosomes in man and the make-up of the comple-
ment in the two sexes have long been subjects of controversy.'^^ It has
now been established that there are 24 pairs represented in the comple-
ment. According to most recent workers (Painter, Evans and Swezy,
Kemp), these include an XF pair in the male and XX in the female;
but others (de Winiwarter, Oguma) contend that there is no Y, the sex-
chromosomes being of the XO type. In Painter's material there can be
little doubt that a large, unequal pair resembling XY pairs in other
mammals is present and disjoins in / (Fig. 213).

B

D

jn

Fig. 213. — A, diploid chromosome complement in man. B, metaphase I in spermato-
cyte, showing XY pair about to disjoin. C, the X and Y have disjoined and passed to
poles in advance of autosomes. D, XY pairs in opossum, monkey, and man. {After
Painter, 1923o, 1922a.)

There is considerable evidence for the view that the XO type has been
derived from the XY type through loss of the Y. In different organisms
many stages in the supposed decrease in size and restriction of function
on the part of the Y are known. Moreover, the Y may be either present
or absent in Metapodius, and such an explanation has been suggested
for the divergence of opinion regarding man (Wilson, 19096, 1925).

In all of the foregoing cases it is the male which is "digametic,"
or "heterogametic," sperms of two kinds fertilizing eggs of one kind.
In some groups, notably birds, moths, and butterflies, the female is
digametic. Here the sperms are all alike, while the eggs are of two
sorts. (In such cases the sex-chromosomes are often referred to as Z and
W instead of X and Y.)

" Reports on the chromosomes of man have been made by many investigators,
among whom may be mentioned Flemming (18826, 1898), Moore and Arnold (1906),
Duesbcrg (1906), Guyer (1910), Gutherz (1912), Montgomery (1912), de Winiwarter
(1912, 1921a6), Wieman (1917), Evans (1918), Painter (1921o, 1922a, 1923o, 1930),
Grosser (1921), Rappeport (1922), Oguma and Kihara (1922, 1923), de Winiwarter
and Oguma (1925, 1926), Oguma (1930), Kemp (1929), Evans and Swezy (1928,
1929).

380

INTRODUCTION TO CYTOLOGY

The XO type (Fig. 214) is exemplified by the moth Talceporia tubulosa.
In the female there are 59 chromosomes, including an unpaired X. In
some oocytes the X passes to the first polar body at /, while in others it
remains in the secondary oocyte nucleus. All of the chromosomes
appear to divide in //. Hence there are two classes of eggs, with 29 and
30 chromosomes respectively. In the male there are 60 chromosomes,
including an XX pair, and all of the spermatozoa are alike in having
one A''. Fertilization of the two kinds of eggs would therefore be expected
to give XO (9) and XX (cf ) (Seller, 1917).

zo

Fig. 214. — Sex-chromosome behavior in animals with heterogametic females. Division /
arbitrarily shown as disjunctional in all cases. ZO = XO; ZW = XY.

Another moth, Phragmatobia fuliginosa, exhibits a modified XY
type of sex-chromosome behavior (Seller, 1913). In Abraxas grossulariata
the somatic nuclei of both sexes usually have 56 chromosomes, but the
females of some strains have only 55 and produce two classes of eggs
with 27 and 28, respectively (Doncaster, 1914). It is not unreasonable
to suppose that in the 56-chromosome strains the X is paired with an
inert Y and that the latter has been lost in the 55-chromosome strains
(Agar, 1920).

CHROMOSOMES AND SEX 381

The XO type is found in the chicken, the duck, and the pigeon.^- In
the chicken the number of small autosomes is uncertain, but the largest
chromosome of the complement is represented once in the female and
twice in the male (Fig. 215). In the pigeon the male has 62 somatic
chromosomes, including two large X-chromosomes; every spermatid
retains one X. Some embryos have 62, including XX, while others
have 61, including X. The latter are in all probability females.

^?'<ct ^^v-c iiSUr:ir4 ^i^

01 a

A B C

Fig. 215. — Chromosomes in birds. A, diploid complement in male chicken; two
X-chromosomes (marked A). B, diploid complement in female; one X-chromosome.
{After Hance, 1924.) C, diploid complement in male pigeon, showing a XX pair (marked
aa). D, from a presumably female embryo, showing one X (a). (After Oguma, 1927.)

In a genus of fishes, Platypoecilus, the genetic data indicate the presence
of an XF pair in the female. ^^ The fact that the nearly related genus
Lebistes appears on similar evidence to have the ZF in the male suggests
that one condition may be derived from the other, possibly by crossing-
over or translocation. This is further suggested by the occasional
appearance of XX males in Lebistes (Winge, 19306).

Gynandromorphs afford further evidence of the role of chromosomes
in sex determination. Such individuals, with male characters in certain
parts of the body and female characters in other parts, are known in
several groups of animals which are normally unisexual, but most of them
occur among insects. Such a condition may arise in several ways. In
Drosophila the genetic evidence, including that in X-rayed flies, shows
that it is mainly due to the elimination of one X-chromosome during an
early mitosis in a female embryo (Fig. 216). Thus one part of the
body develops with X and the other portion with XX, the autosomes in
both portions being the same.^^ In the bee it is probable that gynan-
dromorphism results from the entrance of a sperm into one blastomere of
a divided egg.^^ In the Lepidoptera the morphological and genetical
data favor the theory that an egg may sometimes be formed with two
nuclei, with X and F respectively, and that a sperm nucleus may then

12 Guyer (1909, 1916), Stevens (Boring, 1923), Hance (1924, 1926), and Akkeringa
(1927) on the chicken; Werner (1927) on the duck; Oguma (1927) on the pigeon. In
the turkey, Shiwago (1929) reports the XY type, the Y being very small.

" Bellamy (1922, 1924), Gordon (1926, 1927).

"T. H. Morgan (1914), L. V. Morgan (1929), Patterson (1931a).

"Boveri (1888), Goldschmidt (1923a).

382 INTRODUCTION TO CYTOLOGY

fuse with each of them.^^ Binucleate eggs also appear to be responsible
for gynandromorphs in Hahrobracon.^'^ Gynandromorphism in the
katydid (Amblycorypha) may possibly be due to chromosomal elimina-
tion or to the entrance of two sperms, with X and Y, respectively, into
a binucleate egg. Polyspermy is known to occur in Drosophila, but its
relation to gynandromorphism has not been proved. ^^

Certain further facts are also in harmony with the view that the sex
of the individual is dependent upon the genetical constitution of the
protoplast with which development begins. In a number of animals
exhibiting parthenogenesis, sex is correlated with chromosome number
(p. 410). Human twins, if "identical" (produced by the same zygote),
are invariably of the same sex; if "fraternal" (produced by different

A ^- ^ B

Fig. 216. — A, a Drosophila gynandromorph, female on left side and male on right.
B, explanation suggested by Morgan for this condition: in an early cleavage division one
J^-chromosome fails to be included in either daughter nucleus, so that the nuclei in a
portion of the fly have XX while those in the remaining portion have X. (After Morgan
et al., 1922.)

zygotes) they may or may not be of the same sex. In the nine-banded
armadillo one zygote commonly gives rise to four individuals, which
are invariably all male or all female. Similar examples of polyembryony
are known in insects. In the light of what has been set forth in the fore-
going paragraphs it appears probable that the constitutional factors
affecting sexual differentiation are largely in the chromosomes.

Sex-chromosomes in Bryophytes. — In Sphoerocarpos, a genus of
heterothallic liverworts, two spores of a single quartet develop into male
gametophytes while the other two give rise to females. This is associated
with the behavior of a pair of sex-chromosomes, the first to be discovered
in plants'^ (Figs. 218, 219). The sporophyte has eight pairs of chromo-
somes, including a very unequal XY pair. At the time of sporogenesis the
X and Y disjoin in the first mitosis and divide in the second. The two

IS Doncaster (1914), Goldschmidt and Fischer (1927), Goldschmidt and Katsuki
(1927).

" Whiting (1931), Whiting and Stancati (1931).

18 Pearson (1927, 1929) on Amblycorypha, Huettner (1924, 1927) on Drosophila.

" C. E. Allen (1917, 1919). See also Schacke (1919), Wolfson (1927), and Lorbeer
(1930). The sexual tendencies of the four spores were discovered by Douin (1909)
and Strasburger (1909?>).

CHROMOSOMES AND SEX

383

?LAMT LIFE CYCLE

N

\

\

/

CAMLTES ^-

V

hOMOTHALUC BRYOPHYTE

ANIHAL LlfE CYCLL

HLTLBOTHALUC BRYOPHYTEl

^ j niCRo-

HOMOPHYTIC SEED PLANT

HETEROPHYTIC SEED PLANT

Fig. 217.— Diagrams of life cycles of several types. The first diagram is a modification of
one by SchafTner (1923c). {After Sharp, 1925).

384

INTRODUCTION TO CYTOLOGY

spores with 1 -\- X develop into female gametophytes, while those with
7 + F develop into males. The total chromosome volume in a female
gametophyte nucleus is about 1.7 times that in a male, and the volumes
of the cells differ by about the same amount (Lorbeer).

Meiotic

Spore
quartet.

5PHAER0CAHP0S

Female gametophyte

Fig. 218. — Chromosome cycle in Sphcerocarpos. (Based on data of C. E. Allen, 1917, 1919.)

The genus Pellia also shows well-differentiated sex-chromosomes-"
(Figs. 219, 220). In P. Neesiana the male gametophyte has nine chromo-
somes, including a Y with unequal arms. In the female there is an
equal-armed X in place of the F. Considerable portions of the X and F

Fig. 219. — Sex-chromosomes in liverworts. A, B, Sphcerocarpos Donnellii: A, from
apical region of female gametophyte; B, from spermatogenous tissue of male. (After
Lorbeer, 1930.) C, D, Pellia Neesiana: sets from male and female gametophytes. Which
of the nine chromosomes in the male is the Y has not been determined. (After Showalter,
1928.)

remain condensed (heteropyknotic) through the telophase and interphase.
A comparison of the chromosome complement with that of P. epiphylla
brings out the interesting fact that in homothallic species also a specialized
heteropyknotic "M-chromosome" may be present and suggests that the

2" Heitz (1927hc 1928a6), Showalter (1927c, 1928).

CHROMOSOMES AND SEX

385

heterothallic condition may have arisen through the loss of a portion of
this chromosome in some plants. This would give sex-chromosomes of
two kinds: an unmodified X and a shortened Y. It would also give two

JPellia epiphylla.

V

//

■0

w,

V

4»

\-:.
^

■A

■^

Pellia Neesiana,

W

^^

\<i

^ V

X--

c/'

\\

if (\

if

^^^

•if

\\

»

fi

V

Fig. 220. — Diagram of chromosome sets of homothallic and heterothallic species
oi Pellia. The fifth chromosome in each row is the sex-chromosome. At right: metabolic
nuclei, showing heteropyknotic chromosomal regions. Cf. Fig. 80. (After Heitz, 19286.)

sexual manifestations, assuming that the M-chromosome carries factors
specially influencing sexual development.

Sex-chromosomes essentially like those of Pellia Neesiana have been
described in the heterothallic moss Pogonatmn injiexum (Fig. 221).

■fc.

a

Fig. 221. — Chromosomes of Pogonatum inflexum. a, from female gametophyte
(6 + x). b, from male gametophyte (6 + y). c, disjunction of Y and X in first mitosis
in sporocyte. d, e, f, metabolic nuclei from female gametophyte, male gametophyte,
and sporophyte, showing heteropyknotic sex-chromosomes (also nucleolus). (After
Shimotomai and Koyama, 1932.)

In other heterothallic bryophytes, whose chromosomes are not well
known, there is evidence for the meiotic segregation of sex factors. In
certain mosses there are produced in the capsule spores of two kinds which

386 INTRODUCTION TO CYTOLOGY

develop into male and female plants, respectively. ^^ In these gameto-
phytes, which may be reproduced by regeneration, the sexes are very
firmly fixed, but gametophytes produced by regeneration from diploid
tissue of the sporophyte are bisexual. In pteridophytes the sexual tend-
encies of ordinarily heterothallic gametophytes are not so firmly fixed
and can often be readily altered by varying the cultural conditions. ^^
In these forms very little is known about the chromosomes or factor
segregation.

Algae and Fungi. — A series of experiments performed by Klebs
and others many years ago showed that in certain green algse the environ-
mental conditions very largely determine whether the plants shall
grow vegetatively, produce zoospores, or reproduce sexually. The factors
influencing the kind of sex developed have, however, been very little
investigated in the algffi. A great many species are homothallic. In Vau-
cheria it has been found that bisexual plants may be formed by regenera-
tion from the contents of either the antheridium or the oogonium; this
indicates that the differentiation of the sex organs can hardly involve a
segregation of genetical sex factors. In the heterothallic Cladophora
Suhriana it has been reported that the diploid sporangium-bearing plant
has 13 chromosomes, including an unpaired X. In meiosis both halves of
the split X pass to the same pole in the first mitosis and separate in the
second, so that half of the spores and dioecious gametophytes carry six
chromosomes while the other half carry 6 -{- X. In certain red algae, for
example Polysiphonia violacea, the development of distinct male and
female plants from different tetraspores suggests a segregation of sex
factors in meiosis. Studies on diatoms have yielded evidence that such
factors segregate at I in Nitzschia subtilis and at II in Anomoeoneis
sculpta."^

In the fungi comparatively little is known about the chromosomes
aside from their number and the occurrence of meiosis at sporogenesis
in certain groups (p. 281). In many forms there is, however, strong
evidence for a meiotic segregation of factors influencing the course
of sexual reproduction. In Coprinus, Aleurodiscus, Ustilago, Puccinia,
and other genera of basidiomycetes the spores produced by a single
basidium may be of two "strains," as indicated by the behavior of the
mycelia developing from them. Hyphal unions initiating the binucleate
phase of the life cycle take place only when mycelia of opposite strain
are brought together. ^^ In some cases the mycelia from the spores of a

21 El. and Em. Marchal (1906, 1907, 1909), Schweizer (1923), Fleischer (1920).

22 Wuist (1913), Czaja (1921), Mottier (1927, 1931), Nagai (1914, 1915).

23 Von Wettstein (1920) on Vaucheria; Schussnig (1930a6) on Cladophora; Geitler
(19286, 19296) and von Cholnoky (1928) on diatoms.

24 Kniep (1919 et seq.), Vandendries (1923 et seq.), Brunswik (1924, 1926), Hanna
(1925, 1928, 19296), D. Newton (1926), Sass (1928, 1929), Zattler (1924), Craigie

CHROMOSOMES AND SEX 387

quartet are of four types, each one reacting with only one of the other
three.

A parallel situation is found in ascomycetes. For example, in Neuro-
spo7'a tetrasperma the four spores usually developed in a single ascus are
binucleate and produce "homothallic" mycelia, while occasional uninu-
cleate spores produce "heterothallic" ones. In the ascus of N. sitopMla
there are regularly eight spores, of which four are "plus" and four
"minus," as indicated by the interactions of the mycelia they form.
By studying the relative positions in which the spores with the various
tendencies are borne in the ascus, it is possible to show that the factors
concerned in the differentiation of these tendencies may be segregated at
either the first or the second meiotic mitosis and that this segregation is
independent of that of certain other factors. ^^

In certain heterothallic phycomycetes, notably in Phycomyces nitens,
the spores in a germ sporangium develop two kinds of mycelia, zygospores
being formed only when gametangia borne on the plus and minus strains
are brought together. ^^

It has been generally assumed that the plus and minus strains in the
fungi represent the two sexes, the factors segregated at meiosis being
"sex factors" analogous to those in bryophytes. It was to this sexually
dioecious condition that the term heterothallism was originally applied
(Blakeslee, 1906). When it was found that the mycelia in certain basi-
diomycetes were of four types rather than two, some observers concluded
that there must be four grades of sex, this "multipolar" condition being
determined by the independent segregation of two or more pairs of sex
factors in meiosis.

A number of recent researches in this field tend to support another
interpretation of such phenomena. In certain species, representing both
ascomycetes and basidiomycetes, it has been shown that the plus and
minus strains are not unisexual: the mycelium from a single spore bears
functional organs of both sexes," but sexual unions occur only between
those of opposite strain. From this it is inferred that the meiotic segrega-
tion in such cases is not one of sex factors but rather one of factors
inducing self-sterility and cross-fertility between certain classes of

(1927, 1928), R. F. Allen (1929, 1930, 1932). Kniep (1928) and M. Hartmann (19296c,
1930) review the subject of sexuality in lower plants. See also the experiments of
Harder (1927) (p. 419).

26 B. O. Dodge (1927, 1928a6, 19296), WUcox (1928), Lindegren (1932). See also
Dowding (1931) and Ames (1932).

26 Blakeslee (1906, 1915, 19206), Burgeff (1913, 1914, 1915), Couch (1926). See,
further, footnote 28.

2^ E.g. : Antheridia and ascogonia in Ascobolus (Gwynne-Vaughan and Williamson,
1932); spermatia (microconidia) and ascogonia in Pleurage (Ames, 1932) and Sclero-
tinia (Drayton, 1932); and spermatia and receptive hyphae in Puccinia (R. F. Allen,
1932).

388 INTRODUCTION TO CYTOLOGY

individuals. Unfortunately such species have been said to be "hetero-
thallic" along with those showing true sexual dioecism, thus creating a
confusion which should be clarified.

It is evident, therefore, that the problem of sex in fungi is compli-
cated, as it is in higher plants, by factors which render certain bisexual
individuals or strains intersterile. While the differentiation into plus
and minus strains is plainly of this nature in the instances cited above,
there is evidence^^ that in others it may be truly sexual. A full under-
standing of the situation can scarcely be reached until much more has
been learned about the physico-chemical nature of the sexual states
themselves and about the factors by which they are controlled.

Sex-chromosomes in Angiosperms. — There has long been reason to
believe that the heterophytic (dioecious) condition in flowering plants
is related to a qualitative difference among the pollen grains. Correns
(1907) concluded from his work on Bryonia that the eggs all have a
female sex " tendency " ; that there are two kinds of microspores, and hence
male gametes, with male and female tendencies respectively; and that
the male tendency dominates the female, so that half of the sporophytes
are staminate and half of them carpellate. Strasburger (1910a), who
worked with Elodea, Melandrium, and Mercurialis, assumed that the
tendency of all the pollen grains, and hence male gametes, is toward
maleness: some have a "strong" male tendency which dominates the
female tendency of the egg, staminate plants being so produced, while
others have a "weak" male tendency which is dominated by the female
tendency of the egg, carpellate plants so resulting.

The view that the pollen grains are of two kinds with a differential
effect upon the sex of the offspring received cytological confirmation in
1923, when several species of heterophytic angiosperms were shown to
have heteromorphic sex-chromosome pairs. ^^ Not all heteromorphic
pairs in higher plants, however, are sex-chromosomes.

Sex-chromosomes in heterophytic angiosperms are most commonly of
the XY type. In Elodea canadensis (Fig. 222), the first known case in
vascular plants, the microsporocytes show 24 pairs, including an unequal
XY pair. All of the pairs disjoin in the first division, and the second

28 Chemical researches on strains of phy corny cetes (Satina and Demerec, 1925;
Satina and Blakeslee, 1925 et seq.). Vandendries and Brodie (1933) report evidence
for the view that repulsion between certain strains of a basidiomycete, Lenzites betulina,
is due to a radiation under the influence of a Mendelian factor pair and not to chemical
interaction.

2» For lists of known cases, see Kihara (19296) and Sinoto (19296). Correns
(1928a) reviews the subject of sex in higher plants. Yampolsky (1922) lists the types
of sexual manifestation in angiosperms. Lindsay (1930) gives a list of heterophytic
plants whose chromosomes have been studied. Lindsay (1929) and Cooper (1929)
describe a heteromorphic pair in the homophytic Bougainvillea. For a discussion of
the application of terms implying sexuality to sporophytes, see Sharp (1925).

CHROMOSOMES AND SEX

389

division is equational, so that half of the microspores (and hence male
gametes) receive a F-chromosome and 23 autosomes while the other half
receive 23 autosomes and an X-chromosome. In the nuclei of the

Fig. 222. — Diagrams of two types of sex-chromosome beha\'ior in angiosperms. In
each case the upper row represents the staminate plant and the lower row the carpellate
plant. Number of autosomes arbitrarily shown as four.

carpellate plant there are two X-chromosomes, every egg receiving one
of them. It is therefore evident that the union of an egg with a male
gamete carrying a F-chromosome results in the production of a staminate

b c d

Fig. 223. — Sex-chromosomes in heterophytic angiosperms. a, division I in micro-
sporocyte of Melandrium album, showing unequal XY pair about to disjoin, b, Populus
balsamifera. c, Valeriana dioica. d, Rumex acetoselia, showing Mm disjoining from m.
(c after Winge, 19236; b-d after Meurman, 1925.)

plant (46 + XY), while a union with a male gamete with an Z-chromo-
some leads to the production of a carpellate plant (46 + XX) (Santos,
1923, 1924).

390 INTRODUCTION TO CYTOLOGY

In Melandrium album {Lychnis olhaY^ an XF pair behaves essentially
as in Elodea (Fig. 223). This holds also for Ly chilis dioica, in which the
staminate plants have long been known to be heterozygous for sex
(Shull). In seeking an explanation for the preponderance of carpellate
plants in this genus, Correns found that the pollen tubes formed by
"female-producing" grains grow more rapidly than those of the "male-
producing" grains and thus reach a larger proportion of the ovules.
When relatively small amounts of pollen are used, thus lessening the
competition unfavorable to the male-producing pollen, the ratio of
staminate and pistillate plants among the offspring is
changed decidedly toward equality. ^^

A peculiar form of sex-chromosome behavior is
manifested by Rumex acetosa and certain related
species. ^^ In R. acetosa (Figs. 222, 224) the staminate
plant has 15 chromosomes in the somatic nuclei. In

/g the microsporocytes there are six bivalents and a triple
f group composed of a large X with two smaller elements

^ "s^^^^^i^ ^^^ ^^^ ^2-^ attached to its ends. In the first meiotic
^^?o 'pQjT^ mitosis X disjoins from Fi and F2, and in the second
<:^7/ Dl ^ mitosis all of the chromosomes divide; hence two

5;^ microspores of the quartet receive 7 chromosomes

matic chromosome (6 + X) while the Other two receive 8 (6 + F1F2).
complements of car- rpj^^ somatic nuclei of the carpellate plant contain

pellate (XX) and -t^-t^s rr^,

staminate (YXY) 14 chromosomes (12 + XX). Thus it appears that
plants of Rumex fertilization by a male gamete with X results in a

acetosa. Sex-chro- -^ i i i • i Tr t^ •

mosomes in black, carpellate plant and that by a gamete with 1 1F2 in a
(After Ono, 19306.) gtaminate one. This may be called the XYn or YXY
type of sex-chromosome behavior. It is reported that in R. acetosella the
large chromosome and one small one disjoin from the other small one (Fig.
223, d).

A similar triple chromosome group is found in Humulus japonicus.^^
The distribution of the three members differs in the various sporocytes,
giving different chromosomal races (Tuschnjakova). The full sig-

30 Blackburn (1923, 1924), Winge (19236), Heitz (19256). Other cases are Populus
and Valeriana (Meurman, 1925), Moras, Cannabis, and Salix (Sinoto, 1928), and
Silene (Blackburn, 1928, 1929).

31 G. H. Shull (1910, 1911), Correns (19186, 19206, 1921, 19226).

»2 Kihara and Ono (1923o6, 1925, 1926), Ono (1926, 1927a, 1928, 1930a6), Ono and
Shimotomai (1928), Meurman (1925), Kihara and Yamamoto (1931). The presence
of two kinds of pollen was demonstrated by Correns (19226).

33 Kihara (1928, 1929a), Winge (19236, 1929a), Sinot6 (19296), Tuschnjakova
(1929, 1930). It seems probable that more complex configurations observed here
(Kihara, 1929f/) and in H. lupulus (Sinoto, 1929a6) are due to more extensive chromo-
some association (Winge, 19296), possibly through translocation.

CHROMOSOMES AND SEX 391

nificance of this with respect to sex and other features has not been
determined.

The first known case of XF-chromosomes in digametic females in
plants was that of Fragaria elatior. The genetic evidence that the car-
pellate plants in Fragaria produce two sorts of megaspores, and therefore
female gametes, is supported by cytological studies on F. elatior. In the
megasporocyte there are 21 pairs, including an unequal XY pair which
disjoins in the first meiotic mitosis, each member then dividing in the
second. Fertilization of X-eggs and F-eggs by X-sperms thus gives
staminate plants (X'X) and carpellate plants {XY), respectively. The
breeding behavior of Thalictrum Fendleri shows that this species also is
heterozygous for sex in the female. ^"^

Sex-linkage. — As explained in Chapter XVII, characters w^hich are
dependent upon differential genes located in the same chromosome are
"linked" in inheritance. Since the sex-chromosomes carry genes affect-
ing non-sexual characters also, such characters exhibit a peculiar rela-
tion to sex in successive generations: they are sex-linked characters. ^^
The following example will make this clear.

When a red-eyed male Drosophila is mated to a white-eyed female,
the Fi individuals are white-eyed males and red-eyed females; each
eye-color is, as it were, transferred to the opposite sex (Fig. 225). When
the Fi flies are interbred, the resulting F^ generation comprises four
types: red-eyed males and females, and white-eyed males and females.
It is observed that red eye-color appears in every fly, male or female,
which possesses a derivative of the X^-chromosome of the original red-eyed
male ; whereas, white eyes characterize every male deriving the X-chromo-
some from the original white-eyed female, and in every female having two
such chromosomes. This is because the original male's X-chromosome
carries a dominant factor for red eyes, while each of the original female's
X-chromosomes carries a recessive factor for white eyes. This explana-
tion also applies to the reciprocal cross (white-eyed male X red-eyed
female), in which, however, the relative proportions of red-eyed and
white-eyed flies in Fi and /^2 are different: in Fi all flies of both sexes have
red eyes, while in F2 all of the females and one half of the males have red
eyes, white eyes appearing only in one half of the males.

'^ Genetic evidence in Fragaria: C. Richardson (1914), Valleau (1923), Correns
(1928a). Cytological: Kihara (1926, 19306). Thalictrum: Kuhn (1930d).

^^ Sex-linked characters are not to be confused with sex-limited characters. The
latter are those found exclusively in individuals of one sex and are usually called
"secondary sexual characters." In several cases it has been shown that their genes
are located in the autosomes. It is suggested by Winge (1922a) that inheritance of
secondary sexual characters through autosomes be referred to as "sex-limited"
inheritance, that of characters through the sex-chromosome common to both sexes
(X) as "sex-linked" inheritance, and that of characters through the sex-chromosome
occurring in only one sex (F) as "one-sided" inheritance.

392

INTRODUCTION TO CYTOLOGY

The form of human colorblindness known as Daltonism, in which green
and red are not properly distinguishable, is a sex-linked character which
is inherited precisely like white eyes in Drosophila. The presence of
this defect more commonly in men than in women, and its appearance in
so few individuals in affected lines, are due to the fact that it is a recessive
and sex-linked character. It occurs in a woman only if both of her
A^-chromosomes bear factors for it, which means that one such factor
must have been received from each parent; whereas one factor is sufficient

DTIOSQPHILA

0(9 ) (60

Fig. 225. — Sex-linkage in Drosophila. Three successive generations at left; red eyes
shown in black. History of sex-chromosomes through these generations shown at right,
the X-chromosome of the original male in black. {Adapted from Morgan.)

to produce it in a man, because his F-chromosome carries no factors which
might dominate it. Furthermore, since the X-chromosome of the male is
always derived from the mother, a man can inherit colorblindness from his
mother but not from his father. He might appear to do so, however, if
his father were colorblind and his mother apparently normal but carrying
one affected X-chromosome: the defect in this case would actually be
transmitted by the mother, though apparently by the father. In general,
therefore, a colorblind woman transmits the defect to all of her sons and
to half of her grandsons and granddaughters, whereas a colorblind man
transmits it to none of his children and only to one half of his grandsons.
Haemophilia is inherited in a similar manner.^''

Sex-linkage in plants was first observed in Melandrium {Lychnis).^''
The genetic data indicate that the genes for "angustifolia" and "aurea"

^^ For literature on sex-linkage in man, see Davenport (1930).
3^ Baur (1912), G. H. Shull (1914), Winge (1927c, 1930c, 1931).

CHROMOSOMES AND SEX 393

are located in the Z-chromosome, but certain lethal effects of these
genes result in atypical ratios. A gene for "abnormal" may be present
in either the X or the Y (Winge).

Crossing-over is often rare or absent altogether in individuals hetero-
zygous for the sex factors. In Drosophila it is normally only in females
(XX) that crossing-over takes place: new combinations resulting from
this process occur in the eggs but not in the spermatozoa, a fact which
greatly simplifies genetic analysis in this organism. The lack of crossing-
over between X and Y is doubtless associated in some way with their
wide difference in constitution and function, particularly with the large
amount of genetically "inert" material in them.^^ Lack of crossing-over
in the accompanying autosomes as well indicates the action of general
crossover suppressors. The common fowl, in which the female is hetero-
zygous for sex (XY), shows crossing-over only in the male (XX). On
the other hand, the genetic evidence indicates that in the fish genera
Aplocheilus and Lebistes crossing-over occurs frequently between the X
and Y. Thus it was observed that a certain character showing "one-
sided masculine inheritance," presumably because of a gene in the
F-chromosome, suddenly began to behave as though the gene had been
transferred to the X. In a later generation it was apparently returned
to the F by a second crossover (Winge, 1923a). In the related genus
Platypoecilus, which is heterogametic in the female, there is evidence of
crossing-over between the X and F (Gordon, 1927). In many organisms,
crossing-over occurs regularly in both sexes. It seems probable that these
are forms with less highly differentiated sex mechanisms and that lack of
crossing-over in forms like Drosophila is of value in preserving the state of
sexual heterozygosity.

In Drosophila the normal allelomorph for the mutant character
"bobbed" is carried in the F-chromosome. In Phytodecta any one of a
group of four allelomorphic genes (p. 310) may be carried by either the
X or the Y.^^

The general conclusions regarding the function of sex-chromosomes
are amply supported by the results of chromosome aberrations, partic-
ularly non-disjunction.^° In all such cases "an abnormal distribution of
the sex-chromosomes goes hand in hand with an abnormal distribution of
all sex-linked factors" (Morgan).

S8 MuUer (19146, 1918), Muller and Painter (1932).

^^ Drosophila: Stern (1926a). Phytodecta: Zulueta (1925; see Morgan, 1926a);
Galan (1931) on chromosomes.

^^ Non-disjunction of the two X-chromosomes in a normal female is called "pri-
mary" non-disjunction; the separation of XX from Y, or XF from X, in an XX Y
female is called "secondary" non-disjunction. Non-disjimction is also termed
"reductional" or "equational" according as it occurs in a disjunctional or an equa-
tional meiotic division. The frequency of non-disjunction in Drosophila can be
markedly increased by X-rays (Mavor, 1921 et seq.; E. G. Anderson, 1924c).

394 INTRODUCTION TO CYTOLOGY

Heteroploidy and Sex. — A valuable clew to the probable mode of
action of chromosomes in the determination of sex is afforded by hetero-
ploid organisms. It was long supposed that sex in Drosophila, for exam-
ple, was a matter of the X-chromosomes alone, one of these causing
maleness and two, femaleness. In his researches on heteroploid flies,
however, Bridges^^ was able to show that the two sexes are correlated not
simply with the number of X-chromosomes present but rather with the
numerical ratio between these and the autosomes. Individuals in
which the ratio is 1 : 2 (one X to two autosome sets) are male ; those with
2:2 or 3:3 are females (diploid and triploid). An intermediate ratio 2:3
is correlated with the intersexual state, while flies with the extreme ratios
3:2 and 1:3 are " superfemales " and "supermales," respectively. In
certain mosaic individuals the monoploid regions with a ratio of 1:1 are
female in character, although other known monoploid insects are male.

The study of sexual and other characters in such heteroploid flies
led Bridges to adopt the hypothesis of "genie balance," according to
which "each character of an individual is the index of the point of
balance in effectiveness of a large but unknown number of genes, some
of which have a tendency to change development in one direction and
others in the opposite. "^^ With respect to sex itself, it had been suggested
by Goldschmidt (1911) that the sex grade is a sort of balance between
determiners of opposite tendency. As stated by Bridges, both maleness
and femaleness are due to the simultaneous action of two opposed sets
of genes, whose influences on the organism are toward maleness and
femaleness, respectively. These genes, which may affect other characters
also and are regarded as distinct from other genes, must lie in most if
not all of the chromosomes of the complement; the X-chromosome is
peculiar merely in having a preponderance of genes tending to produce
female characters. The balance is such that, if the number of X-chromo-
somes equals the number of autosome sets, the female-producing genes
in the complement as a whole outweigh in effect the genes tending toward
maleness and the individual is consequently female; whereas, if there
are only half as many X-chromosomes as autosome sets, the female-
producing genes present are insufficient to accomplish this result and the
individual is male. Intermediate and extreme ratios would be expected
to produce the results actually observed. Since this is precisely what is
found in the case of characters other than sex, Bridges concludes that
"the conception of the nature and action of genes as gained from the
study of non-sexual characters is valid in interpreting sex phenomena."
This conclusion is borne out by the fact that in strains showing additional
fragments of X-chromosomes, the sexual expression varies with the size

41 Bridges (1921a, 1922, 1925, 1930, 1932).

"^ Genie balance is also correlated with metabolic rate and duration of life by
Gowen (1931a6).

CHROMOSOMES AND SEX 395

of the fragments, indicating the presence of many sex factors located
in various portions of the X.*^

Comparable with the foregoing conception is the "algebraic-sum"
hypothesis of Schrader and Sturtevant (1923), who hold that, although
the determination of sex depends upon a preponderance of the genetic
effect of the factors for one sex over those of the other sex, a certain
threshold degree of preponderance is necessary before there can be clear-
cut determination.*'* The case of Habrohracon, in which the monoploid
parthenogenetically produced males and the occasional diploid biparental
males are similar sexually, appears to require a somewhat different
explanation/^

The effect of heteroploidy on sex in plants is well illustrated by
Rumex and Pellia. In Rumex acetosa, as pointed out in an earlier section,
the diploid somatic complement of the female consists of 12 autosomes +
XX while that of the male consists of 12 + YXY; hence the X: autosome
set ratio is 2 : 2 in the female and 1 : 2 in the male. In a series of hetero-
ploid forms the following conditions were observed:'*^ a triploid plant
with 18 + XXX (ratio = 3:3) was female; a triploid with 18 + XXYY
(ratio = 2:3) was bisexual; a tetraploid with 24 + XXX YY (ratio =
3:4) was bisexual; a triploid with 18 + XYYY (ratio = 1:3) was male;
a tetraploid with 24 + XXYYY (ratio = 2:4) was male.

In Pellia Neesiana, a heterothallic liverwort, the female gameto-
phyte ordinarily has 8 autosomes + X (ratio = 1:1), while the male has
8 + F (ratio = 0:1). A race has been discovered in which the gameto-
phyte is diploid (18 chromosomes) and the sporophyte tetraploid (36);
moreover, this gametophyte is bisexual.*^ Although the mode of origin
and cytological constitution of the original bisexual gametophyte are not
certainly known, it is thought probable that it arose from a diploid spore
formed after ameiosis in a normal sporophyte (16 + XF). If this is
true its X: autosome ratio (1:2) is intermediate between those of mono-
ploid males and females. In Sphferocarpos Donnellii, diploid gameto-
phytes arising from such unreduced spores (14 + XF) are functionally
female but frequently show a male tendency in the structure of their sex
organs.*^ Simple doubling of the chromosome set in the monoploid

■*3 Dobzhansky and Schultz (1931). Other portions appear to be without such
genes. See Muller and Altenburg (1928), Muller and Stone (1930), Patterson (1931c),
and Muller and Painter (1932). For a discussion of the supposed origin of the sex-
chromosome mechanism, see Muller (1932).

*'* See the discussion by Schrader and Schrader (1931).

«P. W. Whiting (1921), A. R. Whiting (1927, 1928), Torvik (1931).

*6 Ono (1928, 1930a6), Ono and Shimotomai (1928), Kihara and Yamamoto
(1931), Ono (1932).

" Showalter (1927c). Also in P. epiphylla (Heitz, 19276).

*8 Lorbeer, 1927; C. E. Allen, 1932.

396 INTRODUCTION TO CYTOLOGY

gametophytes would be expected to have no effect upon the sex expres-
sion, since the ratio would not be altered.

Data such as the foregoing are still rather few, and generalizations
should therefore be tentative. At the same time they show clearly that
the development of the sexual states is a resultant of the activities of
both sex-chromosomes and autosomes. They also suggest one reason
for the rarity of polyploidy among animals as compared with plants
(Muller, 1925). In animals, which are so commonly unisexual with well-
differentiated sex-chromosomes, the addition of a set of chromosomes
seriously disturbs the normal X: autosome ratio, and hence development
and fertility, in the heterozygous sex. This offers a serious obstacle to
the establishment of triploid and other races with odd numbers of chromo-
some sets. On the other hand, in bisexual plants there is no such critical
ratio to be disturbed, so that triploid and pentaploid races are not
uncommon. The origin of tetraploid races directly from diploids in
animals may be expected occasionally through a duplication of all the
somatic chromosomes, since such duplication does not alter the X : auto-
some ratio. Noteworthy in this connection is the fact that heterophytic
plants tend strongly to remain diploid, or, when polyploid, to show only
even numbers of chromosome sets; whereas homophytic plants exhibit
very freely all types of polyploidy, with odd as well as even numbers of
sets. There is also evidence for the view that polyploid races in the
angiosperms tend to maintain their distinctness because of disturbed
relations between embryo, endosperm, and surrounding tissues in back-
crosses to the original parents.*^

Modification of Sex. — Field taxonomists and experimental workers
are well acquainted with the frequent intergrades between the purely
staminate and purely carpellate conditions in normally heterophytic
flowering plants, and with the changes in sex expression which may be
induced in both heterophytic and homophytic forms by appropriate
alterations in the environmental conditions.^'' The effects of age, nutri-
tion, length of day, and other factors have been investigated and shown
to be very marked in a number of plants, including Cannabis sativa,
Morus alba, Salix amygdaloides, Humulus japonica, Thalictrum dasycar-
pum, and Ariscema Dracontium.

In only a few such cases are the cytological conditions known. In
Cannabis, which is normally heterophytic and is reported to have XY
sex-chromosomes,^^ the sex ratio is ordinarily 19 :lcf. When pollen
from anthers appearing on a carpellate plant was transferred to the pistils
of a normal carpellate plant, all of the offspring were carpellate. This

« See Miintzing (1930, 1933), W. P. Thompson (1930a?>), and Watkins (1932).
"•See Schaffner (1919 et seq.); also Correns (1908), Bartlett (1911), Davey and
Gibson (1917), Stout (1919), and Yampolsky (1919, 1920).
61 Hirata (1924, 19276), Sinoto (1928).

CHROMOSOMES AND SEX 397

indicates that all of the pollen grains carried an X, instead of half of them
X and half of them Y. There was also some evidence that a staminate
plant bearing carpels produced some eggs with X and some with Y.
In Melandrium album an exceptional bisexual individual was shown to
have XF in both micro- and megasporocytes. The same is true of a
bisexual Populus tremuloides.^'^ Thus under certain conditions it is
possible for reproductive elements of one sex to develop with the chromo-
some complement ordinarily characterizing the opposite sex.

Such cases of sex modification in plants and animals^^ serve to empha-
size the fact that it is not simply the sex-chromosomes but a complicated
system of which the chromosomes are a part that is responsible for the
development of the sexes. The development of sex, like that of any other
character, depends upon the constitution of the protoplasm concerned
as well as upon the conditions to which this protoplasm is compelled to
react. Although the protoplasmic constitution is directly inherited, its
reactions in the course of ontogeny can be influenced within certain limits
through external agencies. Hence the determination of sex, like that
of other heritable characters, involves the interaction of two sets of fac-
tors: (1) genetic factors (inherited protoplasmic constitution; intrinsic
factors; genes); and (2) non-genetic factors (extrinsic factors; environ-
mental agencies, external and internal).

The state of balance between those genetic factors whose influence
is toward maleness and those tending toward femaleness varies greatly
in different organisms. In bisexual forms it is so delicate that the
two sexes develop in response to different conditions prevailing in different
regions of the same individual, just as other distinct characters develop
near one another. In unisexual forms, especially in those with well-
differentiated sex-chromosomes, two unlike complexes of genetic factors
are established through meiosis and syngamy. The balance of male-
producing and female-producing factors in these two complexes is such
that, under average conditions, one of them predisposes development
toward maleness and the other toward femaleness. In some cases,
notably the bryophytes, this predisposition is very strong and has not
been overcome by environmental alterations so far tried; whereas, in
other cases, such as the angiosperms mentioned above, the natural
predisposition can be overcome more or less easily. In no case can the
action of either genetic or non-genetic factors be denied. It now seems

^- McPhee (1925) on Cannabis, Belaf (1925) on Melandrium, Erlanson and
Hermann (1928) on Populus.

*^ Among the many accounts of sex modification and its physiological significance
in animals may be cited those of Riddle (1912 et seq.; see 1927), Crew (1923, 1926,
1927abc), Banta (1916 ei seq.), Baltzer (1914), F. R. Lillie (1917), Minoura (1921),
Goldschmidt (1911 et seq.; see 1923a, 1927afe, 19286, 19296, 1931), Witschi (1922 et
seq.; see 1929 and 1932), Seller (1920), and Brambell (19305).

398 INTRODUCTION TO CYTOLOGY

evident that all nuclei, monoploid and otherwise, however greatly they
may differ in the proportions of their "male-producing" and "female-
producing" genes, regularly carry both kinds; and it is probable that the
tissues in which they lie might be made to develop either sex if we but
knew how to alter the other factors concerned.

In the evolution of sex-chromosomes organisms have established a
mechanism insuring a degree of sex separation which is sufficient to
confer upon them the benefits of such separation, but the condition has
apparently become rigid and unalterable only in a minority of the cases,
at least among plants. As emphasized by Correns (1926a), the essence
of dicecism is the presence of two genotypes correlated with sex and not
the uniformly sharp separation of the sexes. The role of genetic factors
in sex differentiation is strikingly illustrated in the production of a
dioecious strain of maize by the genetic manipulation of genes previously
known to be associated with male or female sterility in the ordinary
monoecious strains.^*

Only a beginning has been made on the problem of the ontogenetic
development of the sexual states. The influences of genetic and environ-
mental factors are exerted through a long and complicated series of
intracellular and intercellular reactions. The correlation of sexual differ-
ences with metabolic rate (Riddle et at.), chemical composition (Manoilov
et al.),^^ and endocrine secretions (F. R. Lillie, Witschi, et al.) are of
special interest in this connection. Goldschmidt, as a result of his
extensive researches on intersexuality in diploid moths, ^^ has suggested
that the final expression of sexual characters is dependent upon the
relative velocities of the male-producing and female-producing reactions
in the early stages of ontogenetic differentiation. Moreover, the veloci-
ties vary with the amounts of gene substance present. As an embryo
with the male genetic complex begins development, the male-producing
reactions proceed at a faster rate than the female-producing ones, and
this continues throughout development, giving a normal male moth.
When, however, the quantity of the male-producing gene substance
is less, the rate of the male-producing reactions may sooner or later
fall below that of the female-producing ones; if this occurs before the
critical stage of differentiation is reached, female characters develop and
the moth is intersexual. The earlier the turning point with reference to

" D. F. Jones (1931). See Emerson (1924, 1932). For discussions of the factorial
interpretation of sex determination in the life cycles of plant groups, see Correns
(1928a) and Sharp (1925).

" Manoilov (1922 et seq.), Griinberg (1922, 1923), Minenkov (1924), Satina and
Demerec (1925), Satina and Blakeslee (1925, 1926a6, 1927), Joyet-Lavergne (1927
et seq.), Camp (1929), Dahlgren (1929). For general accounts, see Schratz (1928),
Joyet-Lavergne (1928c, 1932), and Abromavich and Lynn (1930).

^^ Sec Goldschmidt's recent review (1931). For a brief summary of work on
amphibians, see Witschi (1932).

CHROMOSOMES AND SEX 399

the critical stage, the greater the amount of sex reversal. The same
interpretation applies, mutatis mutandis, to intersexes beginning develop-
ment as females. In triploid Drosophila, also, the degree of intersexuality
varies with the time of sex reversal, which is influenced by both genetic
factors and temperature (Dobzhansky, 1930c).

These suggestions are of special importance in that they direct atten-
tion to the quantitative and ontogenetic aspects of genie action, a fuller
knowledge of which is prerequisite to a true understanding of the physical
basis of heredity.

The direct control of sex in a given individual is not to be confused
with the control of sex in a population. Nutritive conditions sometimes
influence the form of reproduction and therefore the sex of the animals
resulting; but here the sex of no individual, once decided, is altered."
Abnormal temperatures may prevent the laying of the eggs from which
one sex develops, without interfering with those giving rise to the other
sex.^^ In such cases the environmental influences operate "by affecting
the production and survival of sexually predestined germ-cells" (Thom-
son, 1913).

Conclusion. — In bisexual organisms the gene complexes in all indi-
viduals are nearly enough alike (with respect to genes affecting sex) for
these to show the same sex manifestation under similar environmental
conditions, and the constitution of this gene complex is such as to result
in the production of both sexes as responses to the different special con-
ditions in tissues in different regions or at different stages of development.
Artificial modifiability here depends on the extent to which those partic-
ular special conditions, which are in this case the differential factors, can
be controlled or altered.

In unisexual (dioecious) organisms the gene complexes of some indi-
viduals differ from those of others in such a way that some develop one
sex, and others the other sex, under the same general environmental
conditions and in the presence of the range of special internal conditions
normally prevailing. Under ordinary conditions, therefore, it is the
genetic factors that are differential. In the heterothallic bryophytes the
segregation of genes at meiosis results directly in spores and gametophyte
individuals of the two sexes; in heterophytic seed plants it results in two
sorts of microspores and hence male gametophytes whose respective
gametes cause a difference in the sex expression of the succeeding sporo-
phytes; in animals it results directly in two kinds of gametes of one sex.
Artificial modifiability here depends on the kind and degree of difference
between the male and female gene complexes, and on the extent to which
their differential effect can be overcome by altering controllable extrinsic

5' Whitney (1914, 1916, 1919) on Hydatina senta.
^ Malsen (1906; on Dinovhilus) .

400 INTRODUCTION TO CYTOLOGY

factors of the system, i.e., the extent to which the latter factors can be
made to assume or to share in the differential function.

In many plants and animals the genie sexual differences have been
correlated with visible and constant differences in the chromosomes.
This serves to emphasize the necessity of considering cytological and
genetical data in any attempt to understand sex and its control.

CHAPTER XXIV
APOMIXIS AND RELATED PHENOMENA

The many known kinds of reproduction in organisms are ordinarily
grouped in two main categories, sexual and asexual. In the latter cate-
gory are several modes which seem clearly to represent aberrations or
derivatives of the sexual process in that they involve the structures
commonly concerned in sexual reproduction. Often there is no sexual
fusion whatsoever, in which case the reproductive process is referred
to as apomixis. This is in contradistinction to amphimixis, in which
the new individual arises from the fusion product of two gametes. In
many organisms apomixis recurs regularly in successive life cycles owing
to other compensatory processes. In other instances it may occur occa-
sionally without leading to the establishment of apomictic races.

In this chapter attention will be devoted chiefly to apomixis in its
two principal forms, parthenogenesis and apogamy. The first of these
occurs in both plants and animals, while the second, as well as a related
condition known as apospory, occurs in plants only.i

PLANTS

The life cycle in vascular plants, bryophytes, and certain thallophytes
is characterized by the alternation of two generations differing in chromo-
some number. This is not, however, true of all cases. Many plants are
now known in which the life cycle shows the two generations as usual
but without any changes in the number of chromosomes. This must be
borne in mind in reading the following pages.

Apomixis. — No sexual fusion occurs.

A. Parthenogenesis. — The development of a sporophyte from a
female gamete (or sometimes a male gamete?) without syngamy.

1 The classification employed here for apomixis in plants follows, in the main, that
drawn up by Winkler (1908, 1920) with certain modifications. The classification for
animals resembles that of Prell (19236). To aid the student in interpreting the con-
fused terminology in the literature, the terms of other authors are included in brackets
under each heading. It is because of complications introduced by heteroploidy that
we substitute the words "reduced" and "unreduced" for the conventional terms
"haploid" and "diploid" ordinarily used in such classifications. For discussions
of the phenomena treated in this chapter, some of them with classifications of cases,
see Winkler (1908, 1920), Strasburger (19096), Ernst (1918), Renner (1916), M.
Hartmann (1909), Prell (19236), Vines (1911), P. Hertwig (1920a), Tischler (1921-
1922), Ankel (1927), Rosenberg (1930), and Darhngton (1932a).

401

402 INTRODUCTION TO CYTOLOGY

1. Reduced Parthenogenesis. — The developing gamete has the reduced
(gametic) number of chromosomes.

[Called haploid parthenogenesis by Hartmann (1909) and Renner (1916), generative
parthenogenesis by Winkler (1904, 1908, 1920), and true parthenogenesis by Stras-
burger (1907a).]

For many years no angiosperm sporophytes with the reduced chromo-
some number were known, but during the last decade several cases have
been discovered. They occur in Datura, Nicotiana, Triticum, Crepis,
Zea, and other genera (see p. 356). In some instances it is clear that the
chromosome set is truly monoploid and not merely the reduced comple-
ment of a polyploid race. The origin of such monoploid sporophytes has
not been traced in detail, but the genetic evidence leaves little doubt that
reduced eggs have developed. Mitosis in such eggs has been observed. -
In none of these cases has a regularly apomictic race been established.

This mode of development is known to occur also in thallophytes.
In Fucus the development of the unfertilized egg has been induced by
artificial means (J. B. Overton, 1913), but the cytological features here
are unknown. Motile gametes of certain other algse have been observed
to develop without conjugation, as in Edocarpus (Kylin, 1918). In
Vaucheria (von Wettstein, 1920) the contents of either the oogonium or
the antheridium may be made to regenerate a new individual; what is
virtually "male parthenogenesis" occurs in the latter case. An example
of reduced parthenogenesis in the fungi is afforded by Saprolegnia
(Mackel, 1928; Schlosser, 1929).

2. Unreduced Parthenogenesis. — The developing gamete has the

unreduced (zygotic) number of chromosomes.

[Called diploid parthenogenesis by Hartmann and Renner, somatic parthenogenesis
by Winkler, ooapogamy by Strasburger, Juel, and Ernst, and parthenapogamy by
Farmer and Digby (1907).]

This form of parthenogenesis occurs very frequently in vascular plants
as a regularly recurring reproductive phenomenon. A few representative
cases are listed in the footnote.^ The unreduced state of the egg is due
to a previous failure of meiosis, the sporophytic number of chromosomes
being carried through to the gametophyte. The two sporocyte divisions

2 Kusano (1915) on Gastrodia, Haberlandt (1921, 1922) on (Enothera.

^ Marsilia Drummondii (Strasburger, 1907a); Athyrium filix-foemina, var. claris-
sima and Scolopendrin?n vulgare (Farmer and Digby, 1907); Alchemilla (Murbeck,
1901; Strasburger, 1904c; Boos, 1917, 1920); Antennaria alpina (Juel, 1898?>, 1900);
Archieracium (Rosenberg, 1906, 1917; Ostenfeld, 1910, 1912); Atamosco texana (Pace,
1913); Erigeron arniuus (Tahara, 1915a, 1921; I. Holmgren, 1919); Eujmtornim
glandidosum (Holmgren, 1919); Calycanthus (Schiirhoff, 1923); Taraxacmn (Murbeck,
1904; Juel, 1904, 1905; Osawa, 1913; Sears, 1917, 1922; Stork, 1920a); Chondrilla
(Rosenberg, 1912); Wikstrcemia (Winkler, 1906; Strasl)urger, 1909a); Allium odorum
(Haberlandt, 1923); Humulus lu-pulus (von Wettstein, 1925); Ochna serrulata (Chiarugi
and Francini, 1930). An example among lower plants is Chara crinita (Ernst, 1918,
1921o).

APOMIXIS AND RELATED PHENOMENA

403

may occur, giving unreduced megaspores (Marsilia), or only one division
may take place {Taraxacum), or the gametophyte may arise from the
megasporocyte itself without haplosis (Antennaria) .

B. Apogamy. — The apomictic development of a sporophyte from a
cell or cells of the gametophyte instead of from a gamete.

1. Reduced Apogamy. — The developing cells have nuclei with the
reduced (gametic) chromosome number.

[Called haploid apogamy by Hartmann, generative apogamy by Winkler, haploid
apogamety by Renner, and meiotic euapogamy by Farmer and Digby.]

The development of sporophytes from vegetative tissue of gameto-
phytes with the reduced chromosome number and without nuclear fusion

Fig. 226. — A, nuclear migration in gametophyte cells of Lasiraea. (After Farmer and
Dighy, 1907.) B, section through gametophyte, showing young sporophytic tissue (s)
developing from gametophytic tissue (g). (After Farmer and Digby.) C, sporophyte
arising apogamously from gametophyte in Pteris cretica; b' , first leaf; v, stem apex; w,
root. (After de Bary.)

has frequently been observed among ferns. ^ The process commonly
begins with the division of the gametophytic cells to form a mass of
"engrafted tissue" which then grows into a new sporophyte (Fig. 226, B).
Ordinarily, apogamy is offset in the life cycle by apospory. In Nephro-
dium hirtipes the spores are formed, though in an abnormal manner:
when there are eight sporogenous cells in the sporangium there is an
incomplete nuclear division, each nucleus coming to have the unreduced
number of chromosomes. These eight cells then function as sporocytes

^ E.g.: Lastrcea pseudo-mas, var. cristata apospora (Farmer and Digby, 1907);
Nephrodium molle (Yamanouchi, 1908c); and Nephrodium hirtipes (Steil, 1919o).

404

INTRODUCTION TO CYTOLOGY

and produce 32 reduced spores (Fig, 227, B). The reduced number
here (60 + ) is doubtless a polyploid one.

2. Unreduced Apogamy. — The developing cells have nuclei with
the unreduced (zygotic) chromosome number.

[Called diploid apogamy by Hartmann, somatic apogamy by Winkler and Ernst,
diploid apogamety by Renner, and euapogamy by Farmer and Digby.]

This type of apogamy appears to occur in certain ferns. In one
reported case^ the sporophyte arises from unreduced "engrafted tissue"

Fig. 227. — A, nuclear abnormality in sporangium of Aspidmm falcatum. {After
R. F. Allen, 1911.) B, restitution nucleus in Nephrodium hirtipes. {After Steil, 1919a.)

C, unreduced parthenogenesis and sporophytic budding in embryo sac of Alchemilla
pastoralis. The egg is developing one embryo below and a nucellar cell is forming another
above; two polar nuclei and one synergid nucleus at middle. {After Murheck, 1901.)

D, gametophyte with antheridium and rhizoids arising aposporously from tissue of sorus
in Polystichum; sp., sporangia. E, gametophyte with archegonia arising from tip of
pinnule in Polystichum. {D and E after Bower.)

which develops after a nuclear migration and fusion in certain cells of
the reduced gametophyte (Fig. 226, .4), Such a fusion in cells not
specifically organized as gametes has been called pseudomixis. In angio-
sperms the formation of embryos by unreduced synergids or antipodal
cells has been reported,^ but the cytological data in most such reports are
rather scanty.

C. Sporophytic Budding. — The formation of new sporophytes by
sporophytic cells surrounding the embryo sac, such cells projecting into
the sac and developing into embryos. Commonly the cells in question

^ Lastrasa pseudo-mas, var. polydactyla (Farmer, Moore, and Digby, 1903; Farmer
and Digby, 1907).

« E.g., Alchetnilla sericata (Murbeck, 1902), Burniannia coelesiis (Ernst aiid Bernard,
1912), and Allium odorum (Haberlandt, 1923).

APOMIXIS AND RELATED PHENOMENA 405

belong to the nucellus ("nucellar embryony"), but sometimes they are
integument cells.

This process occurs in a number of angiosperms,''' commonly in species
exhibiting parthenogenesis or apogamy also (Fig. 227, C). The sacs into
which the embryos project may have either reduced or unreduced nuclei.
Embryos may arise from the egg, other gametophytic cells, and sporophy-
tic cells in the same plant, the condition known as -poly embryony often
resulting.* In genetic researches the exact mode of origin of such
embryos is a matter of considerable moment.

Apospory. — The development of a gametophyte from a cell (or
cells) other than a spore (in plant groups normally developing gameto-
phytes from spores).

As a rule both the sporophyte and the aposporous gametophyte arising
from it have the unreduced chromosome number. In several genera of
ferns^ gametophytes may develop as buds on the sporophyte, commonly
from the leaf margin or the meristematic tissue at the base of the sorus
(Fig. 227, D, E). Such aposporous development of diploid gametophytes
can be induced by cultural means, and this may be followed by the
production of tetraploid sporophytes.^" Ordinarily, apospory is balanced
by apogamy, the chromosome number remaining the same throughout the
life cycle. In mosses^^ also the development of diploid gametophytes
from portions of the sporophyte can be induced in this way. In some
cases these diploid gametophytes produce diploid gametes which fuse
and give rise to tetraploid sporophytes bearing diploid spores. In
Amhlystegium a tetraploid gametophyte has been obtained. Von
Wettstein (19246) reports the production of octoploid gametophytes in
certain intergeneric hybrids.

Apospory may also occur in angiosperms. In such cases^^ an unre-
duced female gametophyte develops from a cell of the nucellus or integu-
ment, often in addition to the gametophyte arising normally from the
megaspore (Fig. 228, D, E).

False Hybrids. — After cross-pollination individuals sometimes
develop which are not true hybrids because they carry nuclear factors
from only one of the parents. Such "false hybrids" are metromorphic

7 E.g., Alchemilla (Murbeck, 1901), Citrus (Osawa, 1912), Rosa (Tackholm, 1922),
Spathiphyllum (Schilrhoff and Jiissen, 1925), Nigritella (Afzelius, 1928), Artemisia
(Chiarugi, 1926), and Ochna (Francini, 1928).

8 For cases of polyembryony in angiosperms, see Ernst (1918, p. 436).
^ Pteris, Asplenium, Athyrium, Poly stick urn, Scolopendrium, Lastrcea.

"Lang (1924) and Manton (1932o) on Osmunda; Lawton (1932) on Aspidium
and Woodwardia; Andersson-Kotto (1931, 1932) on Scolopendrium.

" Mnium, Bryum, Phascum, Amhlystegium (El. and Em. Marchal, 1909, 1912;
Schweizer, 1923).

12 Hieracium flagellare and H. excellens (Rosenberg, 1906, 1907a; see 1930), Arte-
misia (Chiarugi, 1927), Oxyria (Edman, 1929).

406

INTRODUCTION TO CYTOLOGY

(like the mother) or patromorphic (Uke the father), according to the
derivation of their genetic factors ;^^ hence two main processes may be
distinguished: pseudogamy and androgenesis.

A. Pseudogamy. — The development of metromorphic offspring
induced by pollination, but without complete syngamy. The possible
explanations are several:

1. Offspring with the reduced chromosome number may arise by (a)
reduced parthenogenesis, the male gamete not entering the egg; or
(6) gynogenesis, the male gamete entering the egg, but playing no further
role; or (c) reduced apogamy.

Fig. 228. — A-C, gynogenesis in Solanum nigrum. A, embryo sac, with curved male
nucleus near egg nucleus. B, male nuclear matter degenerating in egg. C, young embryo,
with male matter still evident in upper cell. (After C. Jdrgensen, 1928.) D, E, apospory
in angiosperms. Z), nucellar cell {Ap) beginning development of aposporous embryo sac
in Hieracium flagellare. E, aposporous embryo sac (Ap) outgrowing a normal one (e)
in H. excellens. (After Rosenberg, 1930.)

2. Offspring with the unreduced chromosome number may arise by (a)
reduced parthenogenesis followed by chromosome doubling; or (6) unre-
duced parthenogenesis; or (c) unreduced apogamy; or (d) sporophytic
budding.

Examples of some of the above modes of behavior are the following:
Datura stramonium 9 X D. ferox cf yielded a metromorphic monoploid
plant, in all probability as a result of reduced parthenogenesis (explana-
tion, la) (Belling and Blakeslee, 1927). Solanum nigrum 9 X S.
luteum cT yielded a few plants with the maternal gametic chromosome
number, and cytological study showed that the male nucleus degenerates
after entering the egg (explanation, lb) (Fig. 228, A to C) (J0rgensen,
1928). Fragaria vesca 9 X F. chiloensis cf gave metromorphic offspring
with the maternal zygotic chromosome number (probable explanation,

" Millardet used the term "false hybrids" for actual hybrids which were strongly
metroclinous or patroclinous, but Renner (1929) and Kuhn (19306) employ it only
for individuals arising apomictically. We follow Kuhn in using the terms pseudo-
gamy (Focke, 1881) and androgenesis (Kuhn).

APOMIXIS AND RELATED PHENOMENA 407

2a) (Longley, 1926a; East, 1930). In Atamosco the male nucleus entered
a diploid egg and later degenerated, the embryo continuing development
with maternal chromosomes only (explanation, 26) (Pace, 1913). In
certain species and biotypes of Potentilla pollination is necessary for the
setting of seeds, but the offspring of crosses are purely maternal in
characters and chromosome number (Miintzing, 1928).

B. Androgenesis. — Development of offspring with the paternal
chromosomes only. How the condition arises is not yet known.

Examples: Tripsacum dadyloides 9 X Euchlcena mexicana cf yielded
a plant which was morphologically and genetically like the male parent,
although the seed from which it arose was outwardly like that of the
other parent (Collins and Kempton, 1916). Nicotiana digluta 9 X N.
tabacum c^ yielded, among other types, one plant which was morphologi-
cally and cytologically like other tabacum plants with the reduced chromo-
some number (Clausen and Lammerts, 1929). Similarly, N. tabacum
macrophylla 9 X N. Langsdorffii cf gave a typical monoploid Langsdorffii
individual (Kostoff, 1929).

C. Merogony. — Similar in some respects to androgenesis is merogony,
in which an egg fragment without a nucleus develops after the entrance of
a sperm. This has been induced in the brown alga Cystosira barbata by
Winkler (1901) and in several animals (p. 412).

Causes of Apomixis. — It is a noteworthy fact that apomictic plants
are usually characterized by various irregularities in sporogenesis. The
megasporocyte, for example, may form a quartet of unreduced spores, a
pair rather than a quartet, or no spores at all. Similar irregularities in
microsporogenesis lead to the production of varying numbers of function-
less pollen grains; in extreme cases no pollen is formed.

It is evident that abnormal chromosome behavior is largely responsible
for such defective sporogenesis. In the megasporocyte of Marsilia
Drummo7idii the chromosomes undergo synaptic pairing but then
dissociate and split longitudinally as in a somatic mitosis. In Antennaria
the meiotic phenomena are fewer, and the mitosis passes sooner into the
vegetative form. In Wikstroemia there is no trace of synaptic association,
the mitosis being purely vegetative in character; here only two cells are
formed. Finally, in Elatosiema sessile there are no meiotic phenomena
and no cell-division; the sporocyte forms the female gametophyte directly.
These cases^^ illustrate a series of transitional conditions between normal
meiosis associated with sexuality on the one hand and the failure of
meiosis associated with apomixis on the other.

The situation is better known in microsporogenesis, where a series of
increasingly aberrant modes of chromosome behavior may be seen within
a single genus, notably in Hieracium (Rosenberg, 1917). In Hieracium

"Strasburger (1907a, 1904c, 1909a), Modilewski (1908).

408 INTRODUCTION TO CYTOLOGY

pilosella, which is not apomictic, normal synapsis and disjunction are
constant in both megasporocytes and microsporocytes. In the species
horeale, Icevigatum, and pseudoillyricum, all of which belong to the sub-
genus Archieracium, are seen three stages in the transition from normal
meiosis with sexual reproduction, such as occurs in H. pilosella, to ameio-
tic sporocyte divisions with apomixis. These cases show clearly that
there is a connection of some sort between apomixis and a weakness
or absence of the synaptic attraction between homologous chromosomes.

Another notable fact is the common association of apomixis with
polyploidy. When the chromosome number of an apomictic species is
compared with that of a nearly related sexual species, it is commonly
found that the former is larger. In about one-half of the known cases
in angiosperms the apomictic species have twice the numbers found in
the related sexual species, and in some cases the multiple is still larger.
Furthermore, polyploid forms, like apomictic forms, are often character-
ized by conspicuous irregularities in chromosome behavior at the time of
meiosis. A common cause underlying meiotic irregularity, polyploidy,
and apomixis has consequently been sought.

That a primary cause of these chromosomal aberrations, together with
the associated substitution of apomictic for sexual reproduction, is
hybridization, is a theory which has been supported by a number of
students of such phenomena. ^^ The phenomena in question are so
exactly paralleled in hybrids of known origin that little doubt can be
entertained regarding the essential correctness of the theory, though
the limits of its application cannot be stated at present. The importance
of deficient synapsis in bringing about polyploidy and apomixis has been
emphasized by Winge in a special hypothesis involving the synaptic
reaction (see p. 369). The sexual sterility so common in hybrids and
polyploid forms is largely a result of the incompatibility of chromosomes
of unlike origin; indeed, it is highly probable that many apomictic forms
have arisen through the crossing of normally sexed forms, as Ernst
maintained. In certain moss hybrids apomixis is believed to be due to
the action of genes which are freed for action by hybridization or
polyploidy. ^^

The advocates of the hybridization theory do not hold hybridization
to be the sole cause of apomixis. There is evidence that sexual sterility
with apomictic development may also be the outcome of nutritive dis-
turbances set up by other causes, such as abnormal cultural conditions,
parasitism, and wounding. The cells involved in sexual reproduction
seem to be especially sensitive to unfavorable environmental influences,
so that they can easily be made to undergo abnormal development or

1* Ernst (1917, 1918), Rosenberg (1917 et seq.), Winge (1917), I. Holmgren (1919),
Tackholm (1920, 1922), Ostenfeld (1921), Turesson (1930).
16 Von Wettstein (1927). See Zattler (1924).

APOMIXIS AND RELATED PHENOMENA 409

degeneration. In (Enothera, Haberlandt (1921, 1922) finds that wound-
ing brings about the formation of adventitious embryos and he attributes
this to the action of a wound hormone originating in the injured tissue.

The importance of apomixis to the geneticist and field taxonomist
is well illustrated by the condition in the Canince section of the genus
Rosa (Tackholm, 1920, 1922). Among these roses there are types which
had long been regarded as distinct species because of their remarkable
constancy in external characters and the lack of intermediate types.
Tackholm found that the section includes tetraploid, pentaploid, and
hexaploid forms, and that they all show most strikingly the Drosera
type of chromosome behavior in meiosis. As a result the microspores
and male gametes in the pentaploid forms, for example, contain from 7
to 22 chromosomes, while the eggs usually have 28. These facts clearly
indicate the hybrid nature of the Canince roses. They are stable geneti-
cally because they are apomictic : the embryo arises not from sexual cells
but by budding from the nucellus. They are therefore not pure species
but asexually reproducing clones which maintain their hybrid chromo-
some complements and the same external characters from generation to
generation because the reassorting of chromosomes and genes at meiosis
plays no part in determining the make-up of the next generation. Apo-
mixis obviously retards the process of forming new combinations, but it
preserves new types once they are formed, just as in other vegetatively
propagated plants. The importance of such facts for students of the
origin of species and varieties can scarcely be overestimated.

ANIMALS

The best know^n examples of natural parthenogenesis in animals are
found among the rotifers, crustaceans, and insects, this being the regular
mode of reproduction in some species. Other modes may also occur in
such organisms under certain conditions or after a certain number of
generations. Some species produce parthenogenetic and sexual eggs
which show conspicuous structural differences. Moreover, parthe-
nogenesis may be artificially induced in the eggs of other animal groups,
notably echinoderms, mollusks, and amphibians. Around this fact
centers much significant work in modern experimental biology. ^^

Parthenogenesis. — In true parthenogenesis the egg develops without
syngamy or other nuclear fusion.

1. Reduced Parthenogenesis. — The developing gamete has the reduced
(gametic) chromosome number, two maturation divisions having effected
haplosis as usual.

" Robertson (19316) introduces the useful term parthenote for an individual derived
from an egg with only one gametic nucleus.

410 INTRODUCTION TO CYTOLOGY

The type case of this category has long been the honey bee Ayis
mellifica, in which the eggs may develop parthenogenetically into drones
or, after syngamy, into females. ^^ Such a development of males with the
reduced chromosome number has also been demonstrated in a number of
other insects^^ (Fig. 229). In such males the divisions differentiating
the spermatids are purely equational in character; often there is but one
mitosis. It is probable that in certain rotifers also the male parthenotes
have the reduced chromosome number. 2*^

In addition to the foregoing cases in which the reduced chromosome
number is retained to sexual maturity, there are others in which the
number somehow becomes doubled during ontogenesis. Investigators
have repeatedly found that the larvae of echinoderms, insects, amphibians,

and other animals, whether produced by
inducing the parthenogenetic development
^S) \ \iy^ I of reduced eggs or by causing the insemina-

..^/ Q^ tion of enucleate egg fragments, soon show

a characteristic inability to continue very
far with their metamorphosis. For example,
_ when frogs' eggs are induced to develop by

: iKN : ■• /\i^ '■ artificial means, mitoses with both the
■•; '. fV-' .'V''^^. ') : , gametic and zygotic chromosome numbers
'• .•■■•..\-I*i/ .;*' can be seen in the cleavage stages and in

.•.•.\...-- ...,.■• ■"••••■ ■ the tadpoles. The adults all have the

Fig. 229.— Chromosomes of zygotic number.^i As in plants, there may
Icerya littoraiis. a, in partheno- be animals in which the somatic number is

genetically produced male (mono- ,.,i i ..i i-ii.-

ploid). fe, in sexually produced gametic though uot truly monoploid; but m
female (diploid.) {After Hughes- Tetranychus Mmaculatus, with three chromo-

Schrader, 19306.) i • r ? • -ji ^

somes, and in Icerya purchasi, with two,
differing in size, true monoploidy cannot be doubted.-^ Nevertheless,
viable monoploid offspring are not, so far as known, produced by
animals normally diploid in both sexes.

2. Unreduced Parthenogenesis. — The unfertilized egg develops with
the unreduced (zygotic) chromosome number.

18 Petrunkewitsch (1901), Meves (19046, 1907c), Doncaster (1906, 1907), Mark
and Copeland (1906), Nachtsheim (1913).

1^ E.g.: Tetranychus, Trialeurodes, Icerya, Paracopidosomopsis (Schrader, 1920,
1923c; Thomsen, 1927; Hughes-Schrader, 1925, 1926, 1927, 1930a6; Patterson, 1917,
1921; and others). In their useful review of haploidy in Metazoa Schrader and
Hughes-Schrader (1931) list the cases in which the reduced chromosome number in
the male has been demonstrated, as well as those in which the evidence is not con-
clusive. See also the discussion by Metz, Moses, and Hoppe (1926).

20 Whitney (1909, 1924, 1929), A. F. ShuU (1921), Storch (1924).

21 Parmenter (1920, 1925, 1926). See G. Hertwig (1918), Goldschmidt (19206),
and the discussions by P. Hertwig (1920a), Morgan (1924/), and Bosaeus (1926).
Doubling also occurs in Apoteitix and Paratettix (W. Robertson, 1925, 1930).

22 Schrader (1923c), Schrader and Hughes-Schrader (1926).

APOMIXIS AND RELATED PHENOMENA 411

In some cases^^ it is reported that two maturation divisions occur
without accompHshing haplosis. More commonly there is but one
division, a single polar body being formed with no haplosis. ^^ In
Rhabditis monohystera, a nematode worm, the 20 chromosomes in the
oocyte form 10 synaptic pairs and separate in the single meiotic mitosis
which occurs. During the telophase the chromosomes appear double as
in ordinary meiosis, but since there is no second mitosis to separate them
the egg retains the diploid number, 20. This egg develops without
syngamy into a diploid animal. Apparently in rare cases there may be no
maturation divisions. In Neuroterus lenticularis, a gall-fly, the nucleus in
certain eggs approaches the surface as if to produce a polar body but then
returns to the middle of the egg and divides equationally. Development
then proceeds with the unreduced chromosome number, 20 (Doncaster,
1910, 1911, 1916).

Parthenogamy. — Under this heading may be placed those compara-
tively rare cases in which an egg develops without union with a male
gamete but after a fusion of two nuclei. For example, it has been
reported that a polar body nucleus may sometimes fuse with the egg
nucleus, after which development proceeds." In Mactra, after the forma-
tion of the two polar bodies has been induced by treatment with salt
solutions, the nucleus of the egg divides into two which t-hen fuse, and
development proceeds (Kostanecki, 1911). The fusion of cleavage
nuclei at later stages has been observed in certain species of Solenobia
(Seller, 1923).

False Hybrids. — As in plants, so in animals there are rare instances
of the development of an embryo which, though supposedly the offspring
of two parents of the same or different species, contains the functional
nuclear factors of only one of them. Cases like that of Nereis (p. 242),
in which the egg can be activated by a sperm without the latter's entrance,
may be included here. Those in w^hich entrance occurs may be grouped
under the following heads.

A. Gynogenesis. — Here the male nucleus degenerates in the cyto-
plasm of the egg, development proceeding with maternal nuclei alone.
This appears to occur normally in Rhabditis, a genus of nematodes. The
eggs form only one polar body and retain the unreduced chromosome
number. They are then penetrated by the sperm, which degenerates

"^^ Rhodites rosce (Henking, 1892; Schleip, 19096; Hogben, 1920a), Nematus lacteus
(Doncaster, 19076).

■^^ Phylloxera (Morgan, 1906), Aphis (de Baehr, 1908-1912, 1920a), Daphnia
(Kiihn, 1908), Miastor (Kahle, 1908), Simocephalus (Chambers, 1913), Lecanium
(Thomsen, 1927), Rhabditis (Belaf, 1923), Aspidiotus (Schrader, 1929), probably
Tettigidae (Robertson, 1930).

25 Artemia (Brauer, 1894; F. Gross, 1932), Asterias (O. Hertwig, 1890; Buchner,
1911).

412 INTRODUCTION TO CYTOLOGY

without fusing with the egg nucleus. In one species the sperm is
necessary for activation, although it does not participate further in
development.^^

Similar phenomena are frequently encountered in the course of
hybridization experiments and in pathological material. The degenera-
tion of the sperm nucleus in the egg cytoplasm has been observed in a
cross between a sea urchin and a mollusk.-^ In certain other crosses the
paternal nuclear matter is extruded from the fusion nucleus or during the
early cleavage mitoses. ^^ Such elimination during cleavage results
largely from the lagging of the paternal chromosomes in mitosis; in fish
hybrids this appears to be related to the viscosity of the egg cytoplasm
(Pinney). Embryos formed by gynogenesis are maternal in character.
Gynogenesis has been induced in amphibians and echinoderms by treating
the sperm with radium.-^

B. Androgenesis. — The development of embryos with the paternal
chromosomes alone has been induced by incapacitating the egg nucleus
with radium before syngamy.^" In Chcetopterus it has been shown that
such larvse have the monoploid chromosome number, 9. Whether such
larvae may develop into adults or not is unknown.

C. Merogony. — The development of an enucleate egg fragment
which has been entered by a normal sperm may be induced more or less
readily in a number of animals. Such enucleate fragments are obtained
by shaking the eggs^^ or by cutting them in two with a knife or hair
noose. ^'- The development of merogonic individuals usually does not
continue beyond the larval stage.

Many such experiments have been made with the idea of testing the
nuclear theory of heredity. The results have varied with the species
used, the methods, and the direction of the crosses, but, when all things
are considered, they have tended to support the nuclear theory. The
evidence in such cases is often inconclusive because larval characters,
which must be chiefly depended upon, are not widely different in the
species crossed and may begin their differentiation in the egg cytoplasm
before syngamy (p. 419).^^

26 Kriiger (1913), P. Hertwig (1920a). See Wilson (1925, p. 460).
-' Echinus 9 X Mylilus d" (Kupelwieser, 1912).

28 Godlewski (1911), Baltzer (1910), Kupelwieser (1912), Tennent (1912), Pinney
(1918, 1922).

2»0. Hertwig (1910 et seq.), G. Hertwig (1911 et seq.), P. Hertwig (1911 et seq.).
^^ G. Hertwig (1911, 1913; on amphibians), Packard (1918; on Chcetopterus).

31 O. and R. Hertwig (1887), Boveri (1889 et seq.), and Godlewski (1906) on
echinoderms.

32 Wilson (1903), Yatsu (1904, 1910), Zeleny (1904), Spemann (1914, 1919; hair
noose) and Baltzer (1921) on nemertines, mollusks, and amphibians.

33 For more extensive accounts of experiments of the kind cited in this section, see
Morgan (1924o-ff), Conklin (1924), G. Hertwig (1920a6), P. Hertwig (1923), Stomps
(1923), Wilson (1925), and Brachet (1927).

APOMIXIS AND RELATED PHENOMENA 413

Parthenogenesis and Heteroploidy. — Although heteroploidy occurs
much less commonly in animals than in plants, there is some evidence
that here also a causal relationship often exists between apomixis,
heteroploidy, and hybridization. In Tephrosia the crossing of two non-
parthenogenetic species resulted in intermediate hybrids which produced
parthenogenetic eggs. A race of Daphnia, in which the egg forms only
one polar body without haplosis and develops parthenogenetically, is
evidently hexaploid. In Trichoniscus provisorius there is a diploid race
with normal sexual reproduction and a triploid race showing unreduced
parthenogenesis. ^'*

As in the case of plants (p. 407), one may arrange a series of instances
in animals illustrating a transition from normal meiosis with sexuality
to the absence of meiosis with parthenogenesis, one of the characteristic
features of the abnormal cases being a weakness or absence of synaptic
interaction of chromosomes in the meiotic prophase. ^^ To what extent
this abnormal synaptic behavior is due to hybridity in the animals
concerned, as it often appears to be in plants, remains to be determined.

^^ J. Harrison (1920) and Harrison and Peacock (1926) on Tephrosia; Schrader
(1925) on Daphnia; Vandel (1928) on Trichoniscus.

^^ See de Baehr (1920a) on Aphis and Fries (1909) on Artemia.

CHAPTER XXV
CYTOPLASMIC HEREDITY

In the foregoing discussions of heredity attention has been limited
to those characters which develop anew in successive generations under
the differential influence of nuclear factors. Since these factors are
carried by chromosomes, which are distributed in a definite manner
through successive life cycles, the characters dependent upon them are
inherited according to Mendelian rules. The characters in which
crossable organisms differ appear to be mainly of this kind (c/. p. 286).
In addition, there are some characters whose inheritance is non-Mende-
lian and depends rather directly upon peculiarities of the cytoplasm or
something it contains. Among these the best known are certain chloro-
phyll characters of plants.

Chlorophyll Inheritance. — It is obvious that two successive genera-
tions of cells reproducing by division resemble each other partly because
the organs of a given cell may actually become the corresponding organs
of its daughter cells. Thus, in the case of a unicellular green alga the
daughter individuals are like the mother individual in being green because
the chloroplast of the mother cell is divided and passed on directly to
them. In those algae in which a swarm spore germinates to produce a
multicellular individual or associates with others of its kind to form a
colony, the color of the successive colonies or multicellular individuals
is a "metidentical" character transmitted directly by the repeated divi-
sion of chloroplasts.^

A similar interpretation has been placed upon the inheritance of
chlorophyll characters in the higher plants, the supposition being that
plastids, multiplying only by division, are responsible for the distribution,
in the individual plant and through successive generations, of those
characters which manifest themselves in these organs. Abnormalities
in chlorophyll coloring, such as pale greenness, whiteness, and variegation,
are accordingly attributed to an abnormal condition or behavior of the
chloroplasts. Since the color itself is not present in the plastids of
angiosperm gametes, this character may resemble ordinary Mendelian
characters in being developed anew in each generation, but it differs from
them in depending upon the reproduction and distribution of differenti-
ated cytoplasmic organs, the plastids. Indeed, it has been shown that
the various known chlorophyll characters, even those appearing much

' See Harper (1906, 1918a6) on Hydrodictyon and Pediastrum.

414

CYTOPLASMIC HEREDITY 415

alike, fall into two categories: (1) those inherited according to ordinary
Mendelian rules, which is taken to mean that in such cases the processes
concerned in their development are under the influence of differential
nuclear factors; and (2) those not so inherited and therefore seeming to
have their differential basis in the cytoplasm. Both types may appear in
the same genus or species, e.g., in Zea Mays. It is to be emphasized
that the characters in both categories are developed under the influence
of both nucleus and cytoplasm, but that they differ with regard to the
location and nature of the factors acting differentially in the developing
system. Only the second category — the "non-Mendelian" chlorophyll
characters — will be considered in the following classification of the
best known cases. ^

1. The Inheritance Is Maternal. — a. The variegated plants when
selfed or crossed produce variegated, green, pale-green, and white
offspring.

The classic example of this type is Mirabilis jalapa albomaculata,
described by Correns (1909a). Plants of this race have some branches
with normal green leaves, some with white leaves, and some with varie-
gated leaves. Flowers are borne on branches of all three types. Crosses
between unlikes result in seedlings with the color of the maternal parent.
For instance, if a flower on a green branch is pollinated with pollen from
a flower on a white branch, the offspring are all green. In the reciprocal
cross the offspring are all white and soon die because of the lack of chloro-
phyll. If flowers on variegated branches are pollinated, offspring of all
types may result. In no case does the pollen affect the color of the
progeny.^

b. The variegated plants produce only variegated progeny, irrespec-
tive of the type of pollen used: Humulus japonicus albomaculata (Winge,
1919a).

c. The affected plants produce only self-colored (green or pale-green)
progeny: Glycine hispida (Terao, 1918).

2. The Inheritance Is Biparental. — Crosses between flowers on the
green and the white parts of the variegated plant may result in green,
white and variegated offspring; selfing variegateds results only in white
offspring. The type case in this class is Pelargonium zonale albomarginata

2 This classification was drawn up by Demerec (unpubl.)- See also Winge (1919o)
and the recent reviews by Correns (19286) and Chittenden (1927o). For ferns, see
Andersson-Kotto (1931). Kiister (1927) describes the anatomy of variegated leaves.
The relation of chlorophyll inheritance and other genetic phenomena to pathology is
discussed by Link (1932).

3 Other cases: Stellaria, Senecio, Taraxacum, Hieracium, Arabis, and Meseynbry-
anthemum (Correns, 1919, 1922, 19286, 1931); Antirrhinum (Baur, 1907, 1910);
Melandrium (G. H. ShuU, XQIZ); Primula (Gregory, 1915); Zea Mays (E. G. Anderson,
1923; Demerec, 1927); Viola (J. Clausen, 1927), Oryza (Kondo, Takeda, and Fujimoto,
1927); and Sorghum (Karper and Conner, 1931).

416 INTRODUCTION TO CYTOLOGY

(Baur, 1909, 1919). This form, which is characterized by white-mar-
gined leaves, often has pure green and pure white branches, as does
Mirahilis. Crosses either way between flowers on these two kinds of
branches may result in variegated offspring; inheritance is here not
purely maternal as in Mirahilis.'^

Theories of Chlorophyll Inheritance. — It has been suggested that
there are two types of non-Mendelian chlorophyll inheritance, biparental
and maternal, because the male gamete in some cases introduces cyto-
plasm into the egg while in others it does not. Maternal inheritance
would also occur if the male cytoplasmic elements were functionless after
entering the egg. Such explanations do not seem improbable in view of
the available descriptions of syngamy in angiosperms (p. 236), but
nothing can be stated with assurance until much more has been learned
concerning the history of cytoplasm and cytoplasmic inclusions through-
out the life cycle.

With regard to the " albomaculata type" of variegation (la), it is
the hypothesis of Correns that the condition is due to a cytoplasmic
disease which prevents the normal development of the chloroplasts. It
is therefore delivered directly to the next generation through the egg
cytoplasm and is not transmitted by the male parent because the male
gamete introduces no cytoplasm into the egg. If it were due solely to
nuclear factors, it would be transmitted equally by both parents, since
the nuclear contributions of the two are equivalent. The variegation
is the result of different reactions in the unstable affected cytoplasm
during the development of the tissues in various portions of the leaf.
Winge contends that in types giving greens, whites, and variegateds (la)
the defect is in the plastids themselves, whereas in those giving rise
to variegateds only (16) it is in the cytoplasm in which the plastids lie.
For the " albomarginata type" (2) Baur holds that the appearance of
green and white tissues is due to a sorting out of two distinct kinds of
plastids or their primordia, green and white, as the cells multiply by
division.^

That variegation may be due to nuclear genes is suggested in the
hypothesis of Demerec (1927), who assumes the presence of a gene which
is highly mutable when associated with the cytoplasm of another plant,
and also in the hypothesis of Eyster (1928), who postulates a gene
composed of a number of "genomeres" assorting at random as the gene

^ Other cases: probably (Enothera (Stomps, 1920; see Renner, 19246, on hybrids);
probably Viola (J. Clausen, 1930a); Hypericum perforatum (Correns, 1931). A blotch-
ing of the leaves in Avena is inherited in a similar manner (Ferdinandsen and Winge,
1930).

^ This hypothesis is adopted by Gregory (1915) for Primula, E. G. Anderson (1923)
for Zea, Clausen (19276) for Viola, and Yasui (1929) for Hosta. These are examples
of class la.

CYTOPLASMIC HEREDITY 417

divides in somatic mitosis. When the genomeres of a gene are unHke
with respect to their effect upon chlorophyll development, their segrega-
tion results in variegation.

The cytological evidence bearing on the foregoing theories is as yet
rather meager. Green, yellowish, and colorless plastids have frequently
been observed in variegated plants, but too little is known about their
origin and behavior to warrant generalizations. In normal plants and in
several Mendelian and non-Mendelian abnormal chlorophyll types of
Zea Mays, Randolph (1922) found the same kind of visible structure in
the meristematic cells: all contain very minute proplastids (plastid
primordia) which, so far as the microscope shows, are of one kind. In
normal plants the proplastids develop into large green chloroplasts,
whereas in pale-green, yellowish, or white plants, or in the various regions
of variegated plants, they fail to attain the normal color, the normal size,
or both. No evidence was found that green and colorless plastids
represent fundamentally distinct types; they appear rather to be end
results of different modes of development of one type of initial body.
Moreover, they are connected by a series of all conceivable intermediate
conditions, particularly in cells on the boundary between green and white
areas in variegated leaves. Hence no support is found for the hypothesis
that plastids of two initially distinct types undergo a sorting out during
the development of the tissues. Why it is that the primordia develop so
differently in different cells can only be conjectured, but it appears
probable that their peculiar behavior is an indication of some invisible
differentiation being carried out in the cytoplasm. In Abutilon, Tsinen
(1923, 1924) attributes variegations to alterations occurring in the
plastids before, during, or after their development from primordia.
Although the green, yellow, and colorless plastids in variegated individ-
uals of Hosta japonica are indistinguishable in the primordial stage,
Yasui (1929) is inclined to regard them as initially unlike.

The full evaluation of the various theories of non-Mendelian chloro-
phyll inheritance must await a fuller knowledge of the cytoplasm and its
many differentiations. When certain variegation patterns are compared
with the patterns assumed by the leaf-cells as a result of their lineage
(Noack, 1922), it is difficult to regard a simple sorting out of plastids or of
genomeres in successive cell-divisions as an adequate explanation of the
variegation. It seems more likely, in some cases at least, that the peculiar
behavior of the plastids is associated causally with less evident conditions
in the cytoplasm. Such conditions arising during the course of tissue
differentiation might well affect the growth and greening of plastids, as
they do other developmental processes, and so result in the appearance of
''chlorophyll characters." The development of all such characters
doubtless involves the interaction of both nuclear and cytoplasmic ele-
ments, but in the non-Mendelian category the latter elements exert a more

418 INTRODUCTION TO CYTOLOGY

pronounced differential influence than is usually the case. It remains for
future studies to reveal the nature of these extra-nuclear elements or
conditions and to demonstrate their location with respect to the plastids
manifesting the characters for which they are responsible.

Mosses. — In bryophytes and vascular plants most if not all of the
cytoplasm of a given individual is derived from the mother, since the
male gamete brings little if any cytoplasm into the egg at the time of
syngamy. Hence it should be possible to detect any differential effect
of the cytoplasm upon inherited characters by comparing the results of
reciprocal crosses between unlike individuals. When the cross is made
in one direction the cytoplasm is contributed by one parent, while in
the reciprocal cross it is derived from the other; the nuclear constitution
after both crosses is the same. In general, it is found that reciprocal
crosses between races or Mendelian forms within the same species give
similar progeny, which is taken to mean that the cytoplasm is alike in the
parents, or that any slight differences are neutralized or dominated by the
nucleus in the offspring and therefore exert no differential influence upon
characters.^ In interspecific and intergeneric crosses, on the other hand,
it is often found that cytoplasmic differences are not thus neutralized, so
that it becomes possible to relate these to certain differences in character
exhibited by the reciprocal offspring.

These principles are well illustrated by extensive researches on mosses
carried out by F. von Wettstein (1926, 1928, 1930). When two races of
Funaria hygrometrica are crossed, the reciprocals^ are alike; hence the
cytoplasms of these races are similar so far as genetic effects are con-
cerned. When F. hygrometrica is crossed with F. mediterranea, and
especially when it is crossed with the more distantly related Physcomi-
trium piriforme, the reciprocals differ and tend to be almost wholly like
their respective mothers in certain characters. Furthermore, such
differences persist through repeated back-crossing to the paternal species,
indicating that they are related to some stable element in the cytoplasm
which does not become altered by the paternal nuclear elements.

This genetic element always present in the cytoplasm is called by
von Wettstein the plasmon.^ Hence the entire genetic complex consists
of factors in the chromosome set (the genom) and the plasmon. In the
interspecific crosses it is found that the relative effects of these two ele-
ments are not the same for all character differences. Thus paraphysis
form appears to be controlled wholly by the genom, the shape of the leaf

^ Chlorophyll characters treated in the preceding section are not to be included
here.

^ I.e., the gametophytes produced by spores from the reciprocal capsules. Certain
sporophytic characters have also been studied.

8 Correns (19286) has employed Strasburger's term "cyto-idioplasm." It does
not include the results of previous nuclear influence nor ergastic materials.

CYTOPLASMIC HEREDITY 419

tip by both genom and plasmon, and the length of the mid-rib almost
wholly by the plasmon.^

Other Cases. — In a few higher plants it has been shown that certain
characters, notably sterility, are determined in part by some element or
condition in the cytoplasm. For example, certain reciprocal hybrids in
Epilobium show differences in fertility which indicate an interaction of
genes and unlike maternal cytoplasmic elements.^" A somewhat similar
situation is found in Linum. In crosses between two varieties of Vicia
Faba, major and minor, certain genes are found to produce different
effects in the cytoplasms of the two varieties. This is also observed in
reciprocal crosses of Nicotiana Langsdorffii and N. Sanderce.'^^ In a
certain race of Zea Mays wdth pollen which degenerates, usually after the
division forming the generative cell, it has been shown by an extensive
series of crosses that the peculiarity is due directly to something in the
cytoplasm and is not affected differentially by known genes in the various
linkage groups. Moreover, the sterility is not transmitted by pollen
from partially sterile plants. The cytoplasm in the sporocytes differs
visibly in sterile and non-sterile individuals, but the real nature of the
difference is not known. ^^ In a fungus, Pholiota mutahilis, mycelia may
be obtained from a cell having a nucleus of one strain in a mixture of
cytoplasms from two strains, and these mycelia may produce fruit
bodies. The form of these fruit bodies is affected by the cytoplasm, the
various gradations between the forms of the parental strains varying
apparently with the proportions in which the parental cytoplasms are
mixed (Harder, 1927).

The larval characters of certain animals should be mentioned here.
The mature egg, notably in echinoderms, ascidians, and certain other
groups, exhibits a visible cytoplasmic differentiation, and by virtue of
this fact develops for a time in a definite manner irrespective of the type
of sperm causing its activation. Among the characters appearing in the
early stages of embryogeny are some which are inherited in each genera-
tion from the mother only, since their differentiation is actually under
way in the cytoplasm before syngamy occurs. If this " promorphology "
of the egg and therefore such embryonic characters are under the differen-

^ When the effect is produced chiefly by the genom, the genom is said to be ante-
cedent and the plasmon recedent; when it is due mainly to the plasmon, the latter is
antecedent and the genom recedent (von Wettstein, 1926; p. 260).

i^Lehmann (1918 et seq.), Schwemmle (1924), Lehmann and Schwemmle (1927),
Renner and Kupper (1921), Michaelis (1929).

" Chittenden and Pellew (1927) and Chittenden (19276) on Linum, Sirks (1931)
on Vicia, East (1932) on Nicotiana.

12 Rhoades (1931a, 1933). The distribution on the cob of kernels producing sterile
and non-sterile plants rules out the hypothesis of a somatic segregation of a small
number of elements (c/. Anderson, 1923, and Demerec, 1927, on chlorophyll
characters).

420 INTRODUCTION TO CYTOLOGY

tial control of genes, these characters, although inherited "maternally"
in any particular first-generation hybrid because of the late addition of the
male nucleus, should show biparental inheritance through subsequent
generations.

Certain evidence obtained on this point is in accord with these expec-
tations. For example, in cross-fertilized sea urchin or fish eggs the rate
and the type of cleavage are the same as in the mother, no matter what
the direction of the cross; they are characters impressed upon the egg
during its ovarian history, and the male nucleus fails to change the
condition already induced in the egg by maternal nuclear factors. When
the hybrid matures and produces eggs, however, it is found that these
all show the dominant rate and type of cleavage, no matter which parent
contributes the dominant factor. This shows that the male does affect
the character in the second generation. ^^ Breeding experiments with
moths and butterflies have given similar results with respect to some
embryonic characters. ^^ The conclusion is that many embryonic char-
acters whose differentiation is initiated in the egg cytoplasm before
syngamy, although fundamentally Mendelian in their inheritance, may
be peculiar in that the visible effect of the male gamete is delayed for
one generation.

Conclusions. — The phenomena described in this chapter serve to
emphasize the fact that the differential factors responsible for those
differences in heritable characters which constitute the materials for
genetic study are not all similarly located in the protoplasmic system.
In crosses between nearly related types it appears that the differences
in character are due mainly if not entirely to differences in the genetic
factors in the chromosomes, i.e., to the genes. Such characters show
Mendelian inheritance because the genes are distributed in a character-
istic manner by the chromosomes through successive life cycles. In
crosses between more distantly related organisms there may be, in addi-
tion to genie differences, cytoplasmic differences which are sufficiently
great and persistent to reveal their influence on the development of
hereditary characters. When the cytoplasmic differences are the only
ones, as may be the case in reciprocal hybrids, the development of the
persistent diversities in character may be said to be "controlled" by
these differential cytoplasmic conditions, just as the genes "control"
the development of Mendelian characters in narrower crosses.

It should be recognized that in all cases the development of the
inherited characters involves the activity of both nucleus and cytoplasm.
The characters are brought to expression through the action of the entire

13 See Conklin (1915, 1917, 1924), Morgan (1924a/g), Wilson (1925), and Brachet
(1927).

'^ Toyama (1913), Tanaka (1916), Uda (1923). See Morgan et al. (1922) and
Morgan (1924a^).

CYTOPLASMIC HEREDITY 421

protoplasmic system, this including its interaction with the environment.
If we define heredity as "the occurrence of related but not necessarily
identical conditions, events, or characters in successive generations of
organisms as a consequence of their protoplasmic organization" (p. 285),
we must regard the entire protoplasmic system as the "physical basis of
heredity." The nuclear theory of heredity, properly conceived, does not
attribute the existence of a given character wholly to nuclear action,
although it rightly explains many of the differences between related
individuals (probably all of such differences in many cases) as results of
diversities in nuclear constitution. It is such differences which have been
studied most in modern cytogenetics, but the striking success attending
these studies should not obscure the fact that any complete explanation
of the phenomena of heredity must include much that lies outside of the
nucleus.

It should now be more plainly evident why we have stated (p. 284)
that the problem of development cannot be entirely divorced from that of
heredity. Much has been learned about the transmission of hereditary
elements through successive generations, but the manner in which these
elements function in the actual development of the characters remains to
be discovered. This is one of the major biological problems of the future,
and not before it has been solved can we be satisfied with our conceptions
of the mechanism of either development or heredity.

CHAPTER XXVI
HISTORICAL SKETCH

Cytology is about a century old. Before protoplasm had come to be
recognized as the physical basis of life, and the cell as essentially a proto-
plasmic unit, cytology as a distinct branch of biology scarcely existed,
although important investigations of the structure and development of
plants and animals had been in progress for many years. The course
followed later by the growing science was so profoundly affected by some
of these early investigations that they will be set forth below as a part
of the background of our subject. It will be seen that the discovery of the
cellular organization of most organisms, and the formulation of an influ-
ential theory based on the cell as a unit of cardinal importance in develop-
ment, long antedated a proper conception of the true significance of
protoplasm. As a result, cytology has not only derived its name from
the cell, but it has been dominated by the cell concept from the first,
notwithstanding the fact that many of the fundamental problems
confronting the cytologist are presented by organisms which do not have
what is ordinarily regarded as cellular organization.

The investigation of such protoplasmic structures as nuclei and
plastids was begun a century ago, long before their constitutional rela-
tionship was suspected, but most of our knowledge of these and other
kindred elements has been acquired during the past 50 years. The
last quarter of the nineteenth century witnessed an intensive study of
the behavior of cells, nuclei, and chromosomes in the various processes
involved in the growth and differentiation of the organism. Among the
noteworthy results of this study w^as the theory that the phenomena of
inheritance are in some way closely dependent on the activities of the
nucleus, a theory which received striking support after the principles
of Mendelian heredity were rediscovered in 1900. This rediscovery has
very largely determined the character of cytological research so far in
the present century. It has brought cytology into intimate association
with genetics and taxonomy, while a renewed study of living protoplasm
has resulted in similar alliances with physiology and biochemistry. One
of the most conspicuous and encouraging tendencies of the present day is
this closer correlation of the various subdivisions of biology.

The Discovery of the Cellular Organization of Plants and Animals. —
A perusal of Aristotle's De Partibus Animalium and the Historia Plan-
tarum of Theophrastus serves to show that the ancients had considerable

422

HISTORICAL SKETCH 423

knowledge of the organs and tissues of which organisms are composed.
The cells, however, escaped observation until many centuries later, when
suitable lenses became available. The first compound microscope^
appears to have been produced in about 1590 by Jans and Zacharias
Janssen, spectacle makers of Middleburg in the Dutch province of
Zeeland, and during the first part of the seventeenth century other
improved models were designed by other workers. These instruments in
the hands of men with scientific curiosity soon led to many significant
discoveries. A new world was opened to the eye of science, and the
compound microscope has since remained an indispensable instrument
in many branches of biological research.

The first description of the cellular organization of plants w^as given in
1665 by Robert Hooke (1635-1703), a resident of London. Hooke's
interest in optics led him to examine all sorts of objects with the compound
microscope. In charcoal, and later in cork and other plant tissues, he
found small cavities like those in a honeycomb; these cavities he called
"cells." He had no distinct notion of the cell contents but spoke of a
"nourishing juice," which he inferred must pass through pores from one
cell to another. His many observations were embodied in his Micro-
graphia (1665). The chapter containing his remarks on cells is entitled,
"Of the schematisme or texture of cork and the cells and pores of some
other such frothy bodies." Quaint and crude as it now appears to us,
the Micrographia will always be of special interest because it was the
earliest work to deal wdth cells, which were to become the subject matter
of a new science.

Nehemiah Grew (1641-1712), an English physician and botanist,
began a careful study of plant structure in 1664; in 1670 he read his first
important paper before the Royal Society. Further contributions
followed at intervals until 1682, when all of them were published under
the title The Anatomy of Plants. Like Malpighi, an abstract of whose
first work on plants was presented to the Royal Society in 1671, Grew
was interested in tissues and gave particular attention to the combinations
of these tissues in different plant organs. He was strongly impressed by
the manner in which the cells, which he also called "vesicles" and
"bladders," appeared to make up the bulk of certain tissues: " . . . the
parenchyma of the Barque," he said, "is much the same thing, as to its
conformation, which the froth of beer or eggs is, as a fluid, or a piece of
fine Manchet, as a fixed body." He further believed the walls of the
cells to be composed of numerous extremely fine fibrils; in the vessels or
longitudinal elements these fibrils were wound in the form of a close spiral,
while the vessels themselves were bound together by a transverse series
of interw^oven threads. He accordingly compared the structure of the

^ For the early history of the microscope, see Disney (1928).

424 INTRODUCTION TO CYTOLOGY

plant with that of a basket, also with "fine bone-lace, when the women
are working it upon the cushion."

Marcello Malpighi (1628-1694), an Italian physiologist and professor
of medicine, is best known for his important pioneer work in anatomy and
embryology. Most of his observations on plants were included in his
Anatome Plantarum (1675) and had to do largely with the various kinds of
elements making up the body of the vascular plant. A foreshadowing of
the cell theory is seen in his remarks concerning the importance of the
" utriculi " in the structure of the body. At Pisa, Malpighi was associated
with G. A. Borelli, w^ho was one of the first to use the microscope on the
tissues of higher animals.

Antoni van Leeuwenhoek (1632-1723) of Delft is remembered for his
pioneer researches in the field of microscopy. He constructed a number
of simple lenses of high power, and with these he was able to see for the
first time certain Protozoa, bacteria, and other minute forms of life.
In the course of his investigations he observed the cells ("globules")
in the tissues of higher organisms.

Preformation and Epigenesis. — After the death of the above named
observers there ensued a period during which the actual investigation
of the structure of organisms remained practically at a standstill. There
was, however, considerable indulgence in speculation; this should be
recorded here, not because it can be regarded as scientific cytology, but
because of the influence it exerted upon the formulation of many cyto-
logical problems in later years. Such speculation resulted in the division
of the biologists of the day into two schools, the main controversy being
over the manner in which the embryo develops from the egg. The two
theories formulated in answer to this question were called the 'preformation
theory and the theory of epigenesisr

According to the preformation theory, the basis for which was laid
in the seventeenth century works of Swammerdam, Malpighi, and van
Leeuwenhoek, the egg contains a fully formed miniature individual, which
simply unfolds and enlarges as development proceeds. Because of this
unfolding, the theory was also known as the "theory of evolution," an
expression which has a quite different connotation today. In the
eighteenth century the preformation idea was carried to an absurd
extreme by Bonnet (1720-1793) and others, who argued that if the egg
contains the complete new individual, the latter must in turn contain
the eggs and individuals of all future generations successively encased
within it, like an infinite series of boxes one within another. The pre-
formationists soon became separated into two groups: the spermists, or
animalculists, and the ovists. By the former the new individual was
supposed to be encased in the spermatozoon, and figures were actually

2 See the account by Cole (1930).

HISTORICAL SKETCH 425

published showing a small human figure, or "homunculus," within the
sperm head. The ovists, on the contrary, held that the individual is
encased in the egg. A bitter strife was carried on over this question by
the two groups and various interesting compromises were made, but all
extreme forms of preformationism were to disappear in the light of more
critical investigations, which went far to support the opposing theory of
epigenesis.

Two of the early champions of the theory of epigenesis were William
Harvey (1578-1667; Exercitationes de Generatione Animalium, 1651), and
Caspar Friedrich Wolff (1733-1794; Theoria Generationis, 1759). As the
result of many careful observations on the embryogeny of the chick,
Wolff was able to show beyond question that development is epigenetic:
neither egg nor spermatozoon contains a formed embryo; development
consists not in a process of unfolding, but in "the continual formation of
new parts previously non-existent as such" (Wilson). Here was room
for the principle of true generation, or "the production of heterogeneity
out of homogeneity." Wolff also discovered the vegetative growing-
point of plants and described the new formation of the successive lateral
members. The Theoria Generationis is to be regarded as one of the really
great contributions to biological science, for the theory of epigenesis, to
which it furnished substantial support, later became established with
modifications as a fundamental principle of embryology, particularly
through the work of Karl Ernst von Baer (1792-1876) in the nineteenth
century.

In commenting on preformation and epigenesis Whitman (1894)
emphasizes the fact that the tendency of modern biology has not been to
show the entire falsity of either of these views, but to seek out the germs of
truth possessed by each, and to relate them to modern biological concep-
tions. Our present position, although it excludes both views in their
crude original form, involves in a new sense both conceptions. When we
say that the egg is organized, possessing an architecture or mechanism
in its cytoplasm or nucleus which largely predetermines the course of
development, we are making a modernized statement of the preformation
idea. When we say that the parts of the individual are in no way
delineated in the egg but are mainly determined by external conditions
during the course of development, we are speaking in terms of modern
epigenesis. "The question is no longer whether all is preformation or all
postformation; it is rather this: How far is postformation to be explained
as the result of preformation, and how far as the result of external influ-
ences?" (Whitman). When, therefore, it is borne in mind that one of the
outstanding problems of modern cytology is that of identifying the factors
involved in the development of an organized and highly differentiated
individual from an organized but relatively undifferentiated egg, it is
evident that any sketch of cytological history would be incomplete

426 INTRODUCTION TO CYTOLOGY

without some reference to the early theories of preformation and
epigenesis.

The Renewal of the Study of Organic Structure. — The researches of
Hooke, Grew, and Malpighi in the seventeenth century had made it
apparent that "cells," or "globules," are important structural elements
in organisms. When attention was again directed to such matters toward
the end of the eighteenth century, a number of interesting suggestions
were offered regarding the origin and significance of these elements.

One of the earliest theories of cell-formation was that which had been
put forward by Wolff in his Theoria Generationis (1759). According, to
Wolff, every organ is at first a clear, viscous fluid with no definite struc-
tural organization. In this fluid, cavities ("Blaschen," "Zellen") arise
and become cells or, by elongation, vessels. These may later be thick-
ened by deposits from the " solidescible " nutritive fluid. The cavities, or
cells, are not to be regarded as independent entities: organization is not
effected by them, but they are rather the passive results of an organizing
force {vis essentialis) inherent in the living mass.

K. Sprengel (1766-1833) stated that cells originate in the contents
of other cells as granules or vesicles which absorb water and enlarge.
This theory, in spite of its poor observational basis, was upheld by L. C.
Treviranus (1779-1864) in a work appearing in 1806, and both men
fought many years for its support. Kieser (1812) further developed the
idea that granules in the latex are "cell germs" which later hatch in the
intercellular spaces to form new cells. With a much clearer understand-
ing of the nature of the problems involved, a number of excellent observa-
tions were made by J. J. Bernhardi in 1805, by H. F. Link and K. A.
Rudolphi in 1807, and by J. J. P. Moldenhawer in 1812. It is to be
regretted that the deserved attention was not given to their results, for
they promised to lead in the right direction.

Because of their relation to the cell theory, which is soon to be dis-
cussed, special consideration should be given the views of J. B. P. Lamarck
(1744-1829), C. F. Mirbel (1776-1854), and R. J. H. Dutrochet (1776-
1847). As emphasized by Gerould (1922), certain aspects of the cell
theory were taught in Paris at the opening of the nineteenth century,
40 years before the publication of the works which brought it into
prominence.

The famous French biologist Lamarck, in his Philosophie Zoologique
(1809), strongly emphasized the fundamental importance of "cellular
tissue" in the structure and development of organisms. In his own
words, "... cellular tissue is the matrix in which all the organs of
living bodies have been successively formed, and . . . the movement of
fluids through it is nature's method of gradually creating and developing
those organs out of this tissue" (Elliott's translation, p. 230). He adds
in a footnote that he had been teaching this doctrine since 1796. By

HISTORICAL SKETCH 427

"fluids" he evidently means subtle influences of undetermined nature.
With regard to the internal structure of plants, he says: " ... all that
we can find is, among the simplest, a cellular tissue without vessels but
variously modified and stretched or compressed according to the special
shape of the plant; and in the more complex, an assemblage of cells and
vascular tubes of various sizes, mostly with lateral pores, and a varying
number of fibers, resulting from the compression and hardening that a
portion of the vascular tube has undergone" (p. 235).

As Gerould points out, Lamarck's cellular-tissue theory, like his
theory of evolution, was not supported by a body of well-authenticated
published facts. It was rather Mirbel (1808) who attempted to furnish
such observational data. In a work on Marchantia (] 831-1833) Mirbel
distinguished three modes of cell-formation: the formation of cells on
the surface of other cells, the formation of cells within older cells, and the
formation of cells between older cells. The first mode apparently
represented the budding of the germ tube arising from the spore, while
the second and third modes were formulated as the result of a misinter-
pretation of the process of cell multiplication in growing gemmae. Special
notice should be taken of the fact that by both men it was cellular tissue,
and not the individual cell, that was regarded as fundamental. Both
looked upon the organism as a cellular whole rather than an association
of elementary unicellular organisms.

It was Dutrochet (1824) who first insisted upon the primary impor-
tance of the cells as individuals. This was largely because he was able
to resolve plant tissues by maceration into distinct cell units. Of the
cell he writes, "this astounding organ is truly the fundamental element of
organization; everything, indeed, in the organic tissues of plants is
evidently derived from the cell, and observation has just proved to us
that it is the same with animals." This is the essential point of the cell
theory; but before proceeding to a discussion of this theory we should call
attention to the discovery of the nucleus.

Although nuclei were occasionally seen by earlier observers, the
major share of the credit for its discovery goes to Robert Brown (1773-
1858), for it was he who was first impressed by its probable importance
and emphasized it as a normal constituent of cells. Brown, a British
botanist celebrated chiefly for his taxonomic monographs and morpho-
logical researches, announced his discovery in a paper read before the
Linnsean Society in 1831. It was in leaf-cells of orchids that he saw the
nuclei most clearly. Concerning these observations he wrote as follows :

In each cell of the epidermis of a great part of this family, especially of those
with membranaceous leaves, a single circular areola, generally somewhat more
opaque than the membrane of the cell, is observable. This areola, which is more
or less distinctly granular, is slightly convex, and although it seems to be on the
surface is in reality covered by the outer lamina of the cell ; it is not unfrequently

428 INTRODUCTION TO CYTOLOGY

however central or nearly so. . . . This areola, or nucleus of the cell as perhaps
it might be termed, is not confined to the epidermis, being also found not only
in the pubescence of the surface, particularly when jointed, as in Cypripedium,
but in many cases in the parenchyma or internal cells of the tissue, especially
when these are free from the deposition of granular matter.

After Brown's announcement, observations on nuclei in various
tissues multiplied rapidly, and it was not many years before nuclei
came to be recognized as important components of practically all
organisms.

The Cell Theory. — The generalization that the bodies of organisms
are regularly composed of cells and their products, and that the cell
units are of prime importance in determining growth and differentiation,
was made by R. J. H. Dutrochet (1776-1847) in France and by M. J.
Schleiden (1804-1881) and T. Schwann (1810-1882) in Germany. In
addition to the statement quoted in an earlier paragraph, Dutrochet
says in his Recherches Anatomiques et Physiologiques sur la Structure
Intime des Animaux et des Vegetaux et sur leur Motilite (1824):

. . . The globular corpuscles which make up all the tissues of animals are
really globular cells of an extreme smallness, which are united only by cohesion.
. . . This uniformity of ultimate structure proves that organs really differ one
from the other only in the nature of the substances which are contained in the
vesicular cells of which they are composed. . . . Growth results from the
increase in the volume of the cells, and from the addition of new little cells.

Dutrochet noted that certain structures, notably feathers, are made up
of dead cells, and that others represent cell secretions. Moreover, he
recognized the cell as a unit of physiological function. He did not, how-
ever, make a clear distinction between true cells and other globules
visible in tissues (see Rich, 1926).

Schleiden and Schwann made their formulation of the cell theory more
or less jointly after comparing their observations on plants and animals.
In his Beitrdge zur Phytogenesis (1838) Schleiden says,

, . . every plant developed in any higher degree is an aggregate of fully
individualized, independent, separate beings, even the cells themselves. Each
cell leads a double life: an independent one, pertaining to its own development
alone; and another incidental, in so far as it has become an integral part of a
plant. It is, however, easy to perceive that the vital process of the individual
cell must form the first, absolutely indispensable fundamental basis, both as
regards vegetable physiology and comparative physiology in general. . . .

Schwann stated the theory in concise form in 1838, and 1839 he pub-
lished a full account under the title, Mikroskopische Untersuchungen
iiber die Uebereinstinimung in der Struktur und dem Wachsthum der
Thiere und Pflanzen. In this classic work a great variety of animal cells
are carefully described and figured, and the cell stands forth as an indi-

HISTORICAL SKETCH 429

vidual unit with a clearness unapproached in any earlier treatise. This
was due in part to Brown's discovery of the nucleus, which enabled
Schwann to surpass his predecessors in distinguishing true cells from other
elements with which they had long been confused. With regard to the
general significance of cells Schwann says:

The elementary parts of all tissues are formed of cells in an analogous, though
very diversified manner, so that it may be asserted that there is one universal
principle of development for the elementary parts of organisms, however different,
and that this principle is the formation of cells. . . . All organized bodies are
composed of essentially similar parts, namely, of cells. . . . The whole organism
subsists only by means of the reciprocal action of the single elementary parts.
[And further:] The development of the proposition that there exists one general
principle for the formation of all organic production, and that this principle is
the formation of cells, as well as the conclusions which may be drawn from this
proposition, may be comprised under the term Cell Theory. . . .

It should be carefully noted that the essential point in this theory
was that cells, no matter how diverse they may be in appearance, are all
morphologically equivalent and are elementary living units whose action
determines the development of the organism ; the cell is the primary agent
of organization. It is an observable fact that most bodies are composed
of cells and their products, and that the life cycles of such organisms may
be described as cell successions, but the theory lies rather in the concep-
tion of the cell individual as the leader in the development of organic
structure and in function. With Lamarck and Mirbel, even as with
Wolff, cells were not very definitely individualized and were more or less
passive in the formation of organs in the fundamental cellular matrix;
theirs was a tissue theory rather than a cell theory. With Schleiden and
Schwann, on the other hand, cells were definite elementary organisms
primarily responsible for the development and activity of the body.
Dutrochet seems to have been the only one to approach this conception
previously.

Interesting consequences followed from the extension of the cell
theory to the Protozoa. The protozoon was found usually to be a uni-
nucleate individual not greatly unlike one of the cells of a larger animal or
plant. It was therefore concluded that Protozoa are primitive one-celled
organisms that in the course of evolution somehow aggregated to form
cell republics, or multicellular organisms; and this was further taken
to mean that the protozoon was to be homologized with a single cell of
the multicellular body. This conception of the Protozoa and of the phy-
logeny of multicellular organisms has been justly criticized by many
biologists, who hold that if multicellular animals have evolved from
Protozoa it has been by developing internal cellular structure rather
than by colonial aggregation, and that the protozoon is therefore homol-
ogous with the entire multicellular individual (see Dobell, 1911a).

430 INTRODUCTION TO CYTOLOGY

None of the observers named above knew how the cells multiplied.
In his Beitrdge zur Phylogenesis, which dealt largely with the origin of
cells, Schleiden set forth his theory of "free cell-formation," which was
essentially as follows. In the general cell contents or mother liquor
("cytoblastema") there are formed, by a process of condensation, certain
small granules (later called "nucleoli" by Schwann). Around these
many other granules accumulate, thus forming nuclei ("cytoblasts").
Then, "as soon as the cytoblasts have attained their full size, a delicate
transparent vesicle appears upon their surface." This vesicle in each
case enlarges and forms a new cell, and, since it arises upon the surface
of the cytoblast (nucleus), "the cytoblast can never lie free in the interior
of the cell, but is always enclosed [i.e., imbedded] in the cell wall. ..."
Cell-formation was thus regarded as endogenous ("cells within cells")
rather than the result of cell-division. This erroneous idea was adopted
by Schwann, and although it detracted little from the value of his
histological work, it required correction before cytology could develop
further along progressive lines.

Cell-multiplication. — The cell theory as outlined above was at
once adopted as a fundamental proposition in biological research, though
in certain of its aspects it underwent considerable modification as knowl-
edge increased. It was especially desirable to clear up the question of
cell origin, and to this task a number of able observers addressed them-
selves. Among these should be mentioned Hugo von Mohl (1805-1872),
Wilhelm Hofmeister (1824-1877), F. J. F. Meyen (1804-1840), Franz
Unger (1800-1870), and Carl von NageH (1807-1891). The multipUca-
tion of cells by division was observed by several investigators between
1830 and 1840, von Mohl being the first to describe the process in some
detail.

As Sachs has pointed out, Schleiden's strange theory of cell-formation
could hardly have been developed if the true relation of cell-division to
what various workers had called free cell-formation had been recognized
earlier. Von Mohl (1835, 1844) maintained that there are two modes of
cell-formation: by division and by the formation of cells within cells;
but considerable uncertainty remained regarding the behavior of the
vacuolated protoplast ("primordial utricle") during these processes.
At the same time Nageli (1844) produced an exhaustive treatise on the
nucleus, cell-formation, and growth. In algse and the microsporocytes
of angiosperms he clearly showed that cells multiply by division, and
Schleiden was forced to admit that this might be "a second kind of cell-
formation." The continuation of Nageli's researches in 1846 completely
overthrew Schleiden's conception of free cell-formation, establishing the
significant fact that practically all vegetative cell-formation is by cell-
division. Many similar observations had been made by Unger and
von Mohl, but Nageli elaborated a broad theory which took into account

HISTORICAL SKETCH

431

all of the data at hand. He distinctly defined cell-division and free
cell-formation, and showed that what had been taken for the latter might
be regarded as a special case of the former. Nageli's conclusions were
supported by new evidence furnished by other investigators, who further
held that not only vegetative cells, but also those reproductive cells (in
thallophytes) which Nageli thought in some cases might be formed freely,
originate by a modified process of cell-division. It now seemed clear to
these men that cells arose only from preexisting cells, a conception which
had been emphasized by Remak (1841), and which Virchow (1855)
expressed in the dictum, omnis cellula e cellula. This dictum is frequently
employed today, but it is obvious that some qualification should be made
for the origin of cells in plasmodial masses.

Fig. 230. — Figures of division of Tradescantia microsporocyte drawn by Wilhelm
Hofmeister (1848) many years before chromosomes were recognized as definite nuclear
units.

Opinions concerning the origin of the nucleus and its role in cell-divi-
sion varied greatly among these workers, reliable observations being
insufficient to allow any definite conclusion. In 1841 Henle believed with
Schleiden that the nucleus was formed by the aggregation of "elemen-
tary granules," and that it was not constantly present. Better observa-
tions soon showed the falsity of this view. Von Kolliker (1845) asserted
that nuclear division precedes the division of the cell. Hofmeister,
studjdng embryo development in angiosperms, reported "that the nucleus
of the mother-cell divides into two; that one half of the contents of the
cell collects around each of the daughter-nuclei ..." (1847). It
was commonly believed at this time that the nucleus actually dissolved
just before cell-division, new nuclei being formed in the daughter cells;
but Hofmeister, although he described the dissolution of the nuclear
membrane and the nucleoli (1848), held that the main bulk of the nuclear
material actually separated into two masses. At this early date he

432 INTRODUCTION TO CYTOLOGY

clearly observed the poleward migration of what we now call chromo-
somes^ in fresh microsporocytes of Tradescantia (Fig. 230). Remak, as a
result of his observations on blood cells in the chick embryo, formulated a
definite theory of cell-division (1841, 1858). He believed cell-division to
be a "centrifugal" process: the nucleolus, nucleus, cytoplasm, and cell
membrane were supposed to divide in turn by simple constriction. Von
Mohl, who in the main agreed with Hofmeister, wrote as follows (1851) :

The second mode of origin of a nucleus, by division of a nucleus already
existing in the parent-cell, seems to be much rarer than the new production of
them. . . . [And again] ... it is possible that this process [nuclear division]
prevails very widely, since ... we know very little yet respecting the origin of
nuclei. Nageli thinks that the process is quite similar to that in cell-division,
the membrane of the nucleus forming a partition, and the two portions separating
in the form of two distinct cells.

It was not until many years later, in connection with researches upon
syngamy and embryogeny, that the behavior of the nucleus in cell-
division became known in detail and its probable significance pointed out
(p. 441). In 1879 Eduard Strasburger (1844-1912) announced definitely
that nuclei arise only from 'preexisting nuclei. W. Flemming was led to
the same conclusion by his studies on animal cells and expressed it in the
dictum, omnis nucleus e nucleo (1882a).

The Protoplasm Doctrine. — The cell theory and all of its corollaries
were placed in a new light with the development of a more adequate
conception of the significance of protoplasm. A number of early investi-
gators had seen protoplasm and had been impressed by certain of its
activities. As early as 1772 Corti, and a few years later Fontana (1781),
saw the rotation of the "sap" in the Characefe and other plants. After
being long forgotten, this phenomenon was rediscovered by L. C.
Treviranus (1811) and G. B. Amici (1819). The cell to its discoverers
meant nothing more than a wall surrounding a cavity; they spoke only in
the vaguest terms of the "juices" present in cellular structures. The
founders of the cell theory held a position but little in advance of this;
they observed the cell contents but regarded them as of relatively slight
importance.

Felix Dujardin (1801-1860) in 1835 described the "sarcode" of the
lower animals as a substance having the properties of life. Von IVIohl had

' Concerning the behavior of these bodies in the formation of daughter nuclei,
Hofmeister says: "Ich kann die Bildung der Tochterkerne in keiner andern Weise
mir denken, als dass die im Centrum der Mutterzelle angesammelten eyweissartigen
Stoffe, aus zur Zeit unbekannten Ursachen in zwei Gruppen sich sondern, die in Form
abgeplatteter elliptischer Spharoide sich individualisieren; spater nach Aussen sich
mit einer Membran bekleiden und im Innern Bildungen aus dichteren Stoffen erzeugen
konnen." Similar statements accompany his figures of Psilotum in Die Lehre von
der Pfianzenzelle (1867).

HISTORICAL SKETCH 433

seen a similar substance in plant-cells; in 1846 he called it "Schleim," or
"Protoplasma," the latter term having been used shortly before by
Purkinje in a somewhat different sense. Nageli and A. Payen (1795-
1871) in 1846 recognized the importance of protoplasm as the vehicle of
the vital activity of the cell, and Alexander Braun (1805-1877) in 1850
pointed out that swarm spores, which are cells, consist of "naked"
protoplasm. An important point was reached when Payen (1846) and
Ferdinand Cohn (1850) concluded that the "sarcode" of the animal and
the "protoplasm" of the plant are essentially similar substances. In the
words of Cohn:

The protoplasm of the botanist, and the contractile substance and sarcode
of the zoologist, must be, if not identical, yet in a high degree analogous sub-
stances. Hence, from this point of view, the difference between animals and
plants consists in this; that, in the latter, the contractile substance, as a primordial
utricle, is enclosed within an inert cellulose membrane, which permits it only to
exhibit an internal motion, expressed by the phenomena of rotation and circula-
tion, while, in the former, it is not so enclosed. The protoplasm in the form
of the primordial utricle is, as it were, the animal element in the plant, but
which is imprisoned, and only becomes free in the animal; or, to strip off the meta-
phor which obscures simple thought, the energy of organic vitality which is
manifest in movement is especially exhibited by a nitrogenous contractile sub-
stance, which in plants is limited and fettered by an inert membrane, in animals
not so.

Protoplasm was now studied more intensively than ever. H. A.
de Bary (1831-1888), working on myxomycetes and other plant forms,
and Max Schultze (1825-1874), investigating animal cells, demonstrated
the correctness of Cohn's view. The work of Schultze (1861) was espe-
cially important in that it firmly established the protoplasm doctrine,
namely, that the units of organization are masses of protoplasm, and that
this substance is, in general, siynilar in all living organisms. Schultze
described the cell as a mass of protoplasm containing a nucleus, both
nucleus and protoplasm arising through the division of the corresponding
elements of a preexisting cell. The cell wall, upon which the early
workers had focused their attention, turned out to be of secondary
importance. The cell was thus seen to be primarily the organized proto-
plasmic mass, to which Hanstein in 1880 applied the convenient term
protoplast.

Extensive studies on the physical nature of protoplasm were soon
undertaken. Briicke (1861), who was one of the first to lay emphasis on
the fact that protoplasm is an organized substance, looked upon it as a
contractile, semisolid material through which there streams a fluid
carrying granules. Similar to this was the idea of Cienkowski (1863),
who believed he saw in the protoplasm of myxomycetes two fluids, one
of them hyaline and only semifluid (the "ground substance"), and the

434 INTRODUCTION TO CYTOLOGY

other a more limpid fluid with granules suspended in it. De Bary
(1859, 1864), on the other hand, regarded protoplasm as a single semi-
fluid substance, contractile throughout, but showing many local differ-
ences due to varying water content. Probably the first man to recognize
the importance of the colloidal state of matter, newly distinguished by
Graham, in the study of protoplasm was W. Hofmeister (1862, 1867),
but many years were to elapse before such studies could be effectively
pursued.

More influential for a time were the structural theories associated
with the names of Klein, Flemming, Altmann, and Blitschli, and known
respectively as the "reticular," "fibrillar," "granular," and "alveolar"
theories. The reticular theory, which was formulated by Frommann
(1865, 1875, 1884), was developed especially by Klein (1878, 1879) and
supported by van Beneden, Carnoy, Leydig, and others. These workers
saw in protoplasm a reticulum or fine network of a rather solid substance
(spongioplasm) which held a fluid and granules in its meshes.

The fibrillar, or filar, theory announced by Velten (1873, 1876), as
a result of his observations on Tradescantia and other forms, stated that
protoplasm is composed of fine fibrils, which, though often branched, do
not form a continuous network. This idea was developed mainly by
Flemming (1882), who called the substance of the fibrils mitome and the
fluid bathing it paramitome. Some observers asserted that the fibrils
were in reality minute canals filled with a liquid, the granules seen by
others being merely sections of these canals.

According to the granular theory, protoplasm was a compound of innu-
merable minute granules which alone form the essential active basis for
the phenomena exhibited; the observed fibrillar and alveolar structures
were of secondary importance. For Altmann (1886 et seq.), who was the
most prominent exponent of the theory, the granules were actual elemen-
tary living units, or "bioblasts," the liquid containing them being a
non-living hyaloplasm. The cell was therefore looked upon not as a
unit but as an assemblage of bioblasts, "like bacteria in a zoogloea,"
and the bioblasts were believed to arise only by division of others of their
kind {omne granulum e granulo!).

The alveolar theory, also known as the emulsion, or foam, theory,
was elaborated principally by Blitschli (1892 et seq.), and is of special
interest in view of certain present-day notions of protoplasmic structure.
According to Blitschli, protoplasm consists of minute droplets (averaging
Ijj. in diameter) of a liquid "alveolar substance" (enchylema) suspended
in another continuous liquid " interalveolar substance." The structure
is, therefore, that of an extremely fine emulsion, and the appearances
described by other workers are due to optical effects encountered in
examining the minute alveolar structure. Blitschli supported his theory

HISTORICAL SKETCH 435

by making artificial emulsions with soaps and oils which showed amoeboid
movement and other striking resemblances to living protoplasm.

The modern studies discussed in Chapter II have placed a new evalua-
tion on these early structural theories. What their proponents saw was
not the fundamental structure of protoplasm but secondary structural
modifications and differentiation products. Thus Biitschli's alveoles
were innumerable minute masses of various vacuolar and other sub-
stances. Any distinction between large vacuoles, alveoles, and ultra-
microscopic colloidal masses of the same material is more or less arbitrary,
though the physico-chemical properties of the system may be expected to
vary with the degree of subdivision. It is now evident that it is mainly
in the hyaline "ground substance" that fundamental structure is to be
sought, and that the appearances observed by the above pioneers do not
have the significance originally attributed to them.

It would be difficult to overestimate the value, both practical and
theoretical, of the protoplasm doctrine, for its establishment has not only
led to knowledge by which the conditions of life have been materially
improved but has also been an important factor in assisting man to a
modern, rational outlook on organic nature. It is not too much to say
that the identification of protoplasm as the material substratum of the
life processes was one of the most significant events of the nineteenth
century. The doctrine was furnished with a popular expression by Hux-
ley in his well-known essay, The Physical Basis of Life (1868).

The Organismal Theory. — The conception of the cell had by this
time developed into something quite different from what it had been in
the minds of the founders of the cell theory. The cell was now recognized
as a protoplasmic unit, and the ideas of these men concerning the origin
of cells had been overthrown. Future researches were to show more
clearly the role of cells in connection with development and inheritance,
and certain limits were to be set to the conception of the cell as a unit of
function and organization. To Dutrochet and Schwann the multi-
cellular plant or animal appeared as little more than a cell aggregate, the
cells being the primary individualities; the organism was looked upon as
something completely dependent upon their varied activities for all its
phenomena. "The cause of nutrition and growth," said Schwann,
"resides not in the organism as a whole, but in the separate elementary
parts — the cells." This elementalistic conception of the organism as an
aggregate of independent vital units governing the activities of the whole
dominated biology for many years, nowithstanding its severe criticism
by Sachs, de Bary, and many other later writers who pointed out that,
owing to the high degree of physiological differentiation among the various
tissues and organs, the cell cannot be regarded merely as an independent
unit but as an integral part of a higher individual organization, and that

436 INTRODUCTION TO CYTOLOGY

as such the exercise of its functions must be governed to a considerable
extent by the organism as a whole.

That it is thus the living system as a whole, and not the individual
cell, that is the "primary agent of organization" was definitely main-
tained by a number of biologists, who, unable to accept the orthodox
cell theory, developed and supported the "organismal theory."^ Accord-
ing to this theory, evidence for which was cited in Chapter I, the multi-
cellular plant or animal is not a colony or republic of elementary cell
individuals but rather a more or less continuous mass of protoplasm
which has become incompletely subdivided into subordinate centers of
action, the cells, during the course of ontogenesis; the many cells are an
accompaniment or a result, rather than the cause, of development and
differentiation. In the words of de Bary, "die Pflanze bildet Zellen,
nicht die Zelle bildet Pflanzen." The phylogenetic corollary of this
theory is that multicellular organisms have evolved not by an aggregation
of many individuals but rather by the growth, differentiation, and
septation of one, i.e., by just such a process as is observable in ontogeny.
This general theory has made slow progress in competition with the
descriptively convenient cell theory, but the tendency at the present
time is to give it increasing recognition in discussions of the organism and
its activity,

Syngamy and Embryogeny. Plants. — Although it was known to the
ancients that there is in plants something corresponding to the sexual
reproduction seen in animals, their ideas of the organs and processes
involved were very vague. Like Grew and others in the seventeenth
century, the botanists of antiquity were aware of the fact that the pollen
in some way influences the development of the ovary into a fruit with
seeds. That this involves a sexual act was clearly shown by the observa-
tions and experiments of R. J. Camerarius (1694), C. Mather (1716,
1721), T. Fairchild (1717, 1724), P. Miller (1721), J. Logan (1735),
and others,^ but in spite of these and the subsequent researches of J. G.
Koelreuter (1761), C. K. Sprengel (1793), and K. F. Gaertner (1849) the
idea of sexuality in plants was vigorously opposed in certain quarters for
many years.

An important step in advance was made when G. B. Amici (1830)
followed the growth of the pollen tube from the pollen grain on the

* Here may be mentioned the names of de Bary (1862), Hofmeister (1863, 1867),
Sachs (1882), Rauber (1883), Heitzmann (1883), O. Hertwig (1884), Whitman (1893),
A. Sedgwick (1894), Heidenhain (1902, 1907), Schlater (1911), Dobell (1911a), Gur-
witsch (1913), Ritter (1919), and Rohde (1885 et seq.; see 1923). See the recent
discussions by Ritter and Bailey (1928) and Russell (1930). The theory has also
been known as the plasma theory, tissue theory, and plasmodial theory.

^ For an account of these early investigations, see Zirkle (19326). See also Roberts
(1929).

HISTORICAL SKETCH 437

stigma to the ovule. Schleiden (1837) and Schacht (1850, 1858) took
up the study and made a curious misinterpretation: they regarded the
ovule as merely a place of incubation for the end of the pollen tube,
which they thought entered the ovule and enlarged to form the embryo
directly. The work of Amici (1842), Tulasne (1849), and others showed
the falsity of this notion, but an acrimonious discussion raged about
the subject for a number of years. After W. Hofmeister (1849) and
Radlkofer (1856) had followed the process with their characteristic
thoroughness, there could remain no doubt concerning the error of
Schleiden and Schacht. Hofmeister clearly demonstrated that the
embryo arises, as Amici contended, not from the end of the pollen tube,
but from an egg contained in the ovule, the egg being stimulated to
development by the pollen tube. He was wrong, however, in supposing
that the tube did not open and that a fertilizing substance diffused
through its wall.

It was in the algse that the union of the sperm cell with the egg cell
(syngamy) was first seen in the case of plants. In 1853 Thbret saw
spermatozoids attach themselves to the egg of Fucus, and in 1854 he
showed that they are necessary to its development. The actual entrance
of the spermatozoid into the egg was first observed in 1856 by Nathanael
Pringsheim (1824-1894) in (Edogonium. The fusion of the parental
nuclei was seen by Strasburger (1877) in Spirogyra, but he thought they
thereupon dissolved. This error was corrected shortly afterward by
Schmitz (18796), who was thus the first to show clearly that the central
feature of the sexual process in plants is the union of two parental nuclei
to form the primary nucleus of the new individual. The demonstration
of such a nuclear fusion in a number of algse and fungi soon followed (see
Tischler, 1921-1922, p. 462).

The fusion of the gametic nuclei in bryophytes and pteridophytes was
first seen by Kruch (1890) in Riella, and by Campbell (1888) in Pilularia.
That the same process occurs in syngamy in the seed plants was demon-
strated by Strasburger, who in 1884 described the union of the egg nucleus
with a nucleus brought in by the pollen tube (c/. 1877, pp. 56, 76). In
1898 and 1899 S. Nawaschin and L. Guignard completed the story by
describing "double fertilization," w^herein one male nucleus unites with
that of the egg while a second male nucleus unites with the two polar
nuclei to form the primary endosperm nucleus. The subsequent work of
Strasburger and others on the gymnosperms and angiosperms greatly
cleared up the whole matter of syngamy and embryogeny in these plants.

Animals. — It is probable that the spermatozoon was first seen in
1677 by Ludwig Hamm, a pupil of Leeuwenhoek. The credit for the
discovery is, however, usually given to Leeuwenhoek, since it was he who
brought the matter to the attention of the Royal Society and pursued
such studies further. He asserted that the spermatozoa must penetrate

438 INTRODUCTION TO CYTOLOGY

into the egg, but it was thought at the time and for many years afterward
that they were parasitic animalcules in the spermatic liquid; hence the
name "spermatozoa."

Although L. Spallanzani (1786) is usually said to have shown by a
filtration experiment that the spermatozoon is the fertilizing element,
it is pointed out by Lillie (1916) that Spallanzani did not draw the
correct conclusion; he even denied that the spermatozoon is the active
element, holding rather that the fertilizing power lies in the spermatic
liquid. It was Prevost and Dumas who corrected this mistake and
demonstrated the true role of the spermatozoon (1824). The spermato-
zoon was later shown by Schweigger-Seidel (1865) and La Valette St.
George (1865) to be a complete cell with its nucleus and cytoplasm, as
von Kolliker had maintained. That Schwann (1839) had been right in
regarding the egg as a cell was shown by Gegenbaur in 1861. The polar
bodies formed at the time the egg matures are said to have been first
seen by Carus (1824). Biitschli (1875) showed them to be formed in
connection with the division of the egg nucleus, and Giard (1877) and
Mark (1881) interpreted them as abortive eggs.

The penetration of the spermatozoon into the egg was not actually
seen until Newport (1854) observed it in the case of the frog. In 1875
O. Hertwig (1849-1922) announced the important discovery that the two
nuclei which fuse in the fertilized egg are furnished by the egg and the
spermatozoon. The role of the nucleus in syngamy was thus demon-
strated in animals only shortly before it was in plants, and it is interesting
to note that the first complete description of the union of the germ cells
in animals was given by H. Fol in the same year (1879) that Schmitz
described clearly the process in plants. It was now evident that syngamy
in both kingdoms consists in the union of two gametes which are ordi-
narily single cells, one from each parent (in dioecious forms), and that the
central feature of the process is the union of two gamete nuclei, the new
individual therefore deriving a portion of its nuclear substance from
each parent.

Although the cleavage of the fertilized animal egg in the development
of the embryo had been seen many years previously, it was first definitely
described by Prevost and Dumas in 1824 for the frog. At that time
neither the egg nor the products of its division were clearly recognized as
cells. The true meaning of cleavage was elucidated by M. Barry, who
held that the blastomeres are cells and that their division is preceded by
the division of their nuclei; also by a number of later writers, including
A. von Kolliker, Whitman and Rabl, who traced in detail the long series
of changes undergone by the multiplying embryonic cells as the various
tissues and organs are differentiated. Embryogeny was thus shown to
involve the division and differentiation of cells, the fertilized egg initiating
a series of divisions giving rise to all the cells of the body and to the germ-

HISTORICAL SKETCH 439

cells. It was now possible to describe the life cycle in terms of cell
successions; and since the egg was seen to be a descendant of the egg of the
previous generation, it became evident that there has been an uninter-
rupted series of cell-divisions from the remote past down to the organisms
in existence today. The statement of this conception, without, however,
any necessary emphasis on cells rather than protoplasm itself, is known
as the law of genetic continuity. In the words of Locy (1915):

The conception that there is unbroken continuity of germinal substance
between all living organisms, and that the egg and the sperm are endowed with
an inherited organization of great complexity, has become the basis for all current
theories of heredity and development. So much is involved in this conception
that ... it has been designated (Whitman) "the central fact of modern biol-
ogy." The first clear expression of it is found in Virchow's Cellular Pathology,
published in 1858. It was not, however, until the period of Balfour, and through
the work of Fol, Van Beneden (chromosomes, 1883) Boveri, Hertwig, and others,
that the great importance of this conception began to be appreciated, and came
to be woven into the fundamental ideas of development.

Mitosis and Meiosis. — We have pointed out that cells were once
believed to arise de novo from a mother liquor, or "cytoblastema," This
misconception was removed by later investigations in which it was shown
beyond question that cells arise in general by the division of preexisting
cells. By several early observers the nucleus was seen to have a more or
less prominent part in the process, its division preceding that of the cell;
but, in the words of Wilson (1900),

... it was not until 1873 that the way was opened for a better understanding
of the matter. In this year the discoveries of Anton Schneider, quickly followed
by others in the same direction by Biitschli, Fol, Strasburger, Van Beneden,
Flemming, and Hertwig, showed cell-division to be a far more elaborate process
than had been supposed, and to involve a complicated transformation of the
nucleus to which Schleicher (1878) afterward gave the name karyokinesis. It
soon appeared, however, that this mode of division was not of universal occur-
rence; and that cell-division is of two widely different types, which Van Beneden
(1876) distinguished && fragmentation, corresponding nearly to the simple process
described by Remak, and division, involving the more complicated process of
karyokinesis. Three years later Flemming (1879) proposed to substitute for
these terms direct and indirect division, which are still used. Still later (1882a)
the same author suggested the terms mitosis (indirect or karyokinetic division)
and amitosis (direct or akinetic division), which have rapidly made their way
into general use, though the earlier terms are often employed. Modern research
has demonstrated the fact that amitosis, or direct division, regarded by Remak
and his followers as of universal occurrence, is in reality a rare and exceptional
process; ... it is certain that in all the higher and in many of the lower forms
of life, indirect division or mitosis is the typical mode of cell-division.

The chromosomes appeared in published figures long before their
significance was appreciated. Thus in 1848 Wilhelm Hofmeister exam-

440 INTRODUCTION TO CYTOLOGY

ined Tradescantia sporocytes in water and described " spherical droplets
of a strongly refractive substance" formed by a "slow coagulation of
albuminoids in the cell contents" (see p. 431). They were more ade-
quately described a quarter of a century later by the investigators named
in the preceding paragraph. Waldeyer (1888) gave them their name.
The longitudinal splitting of the prophasic chromosomal threads was
discovered by Flemming in 1879; shortly thereafter (1884) van Beneden
and Heuser showed in animals and plants, respectively, that the daughter
halves pass to opposite poles in the anaphase. That they maintain their
individuality through the nuclear cycle was maintained by van Beneden
(1883), Rabl (1885), and Boveri (1887 et seq.). Drawings of the achro-
matic figure were published by Kowalevsky (1871) and Fol (1873), but
Biitschli (1875) was the first to describe it in detail.

The reduction of the number of chromosomes was discovered by van
Beneden (1883), who announced that the nuclei of the egg and sperma-
tozoon of Ascaris each contain one half the number found in somatic
cells. Strasburger (1888) showed that in angiosperms the number of
chromosomes in the egg and male nuclei is fixed by a reduction occurring
in the megasporocyte and microsporocyte, respectively. This was at once
confirmed by Guignard (1889, 1891). E. Overton (1893) found that the
female gametophyte cells in a cycad, Ceratozamia, have half the number
present in the cells of the sporophyte. He further suggested that reduc-
tion probably occurs in the sporocytes in mosses and ferns. In a liver-
wort, Pallavicinia, Farmer (1894) found the gametophyte cells to have
four chromosomes and the sporophyte cells eight. That Overton's
theory of reduction in the sporocytes of bryophytes and pteridophytes
was correct was demonstrated by Strasburger (1894), who postulated the
occurrence of a periodic reduction in the number of chromosomes in all
organisms reproducing sexually.

How the reduction is accomplished was not at first apparent. The
formation of functionless polar bodies by animal oocytes suggested that
the change in number is brought about by the simple casting out of half
the chromosomes during the development of the reproductive cells. This
view proved to be incorrect when it was shown (1890-1893) by Henking,
Riickert, Haecker, vom Rath, and others that the double chromosomes
appearing in the reduced number in the first meiotic mitosis are
really pairs of chromosomes. These bivalent pairs were seen to arise
by a synapsis of chromosomes two by two, the members of each pair then
disjoining in one of the meiotic divisions. Thus it became evident that
reduction is effected by a redistribution of the chromosomes to different
nuclei and cells and that the degeneration of the polar bodies is a phe-
nomenon without any general significance in meiosis. Studies on meiosis
in many groups of organisms were soon undertaken, and no department
of cytology has witnessed the development of a larger or more contro-

HISTORICAL SKETCH 441

versial literature. Interest in the subject was greatly accentuated by the
suggestion that the mode of chromosome reduction affords a key to
certain phenomena of heredity.

Cjrtology and Heredity. — As Wilson (1900) points out, the many
facts brought to light in the early days of cytology were of the greatest
significance in connection with the theory of evolution and the problem
of heredity, though for many years this was only vaguely perceived.
Darwin, aside from his hypothesis of pangenesis, scarcely mentioned
the theories of the cell, and not until many years later was the cell
investigated with reference to these matters. Researches on the origin
of the germ-cells, nuclear division, and fertilization, which brought
cytological research and the study of evolution and heredity into inti-
mate association, began shortly after 1870 with the works of Schneider,
Auerbach, Fol, Btitschli, 0. Hertwig, C. Bernard, van Beneden, Stras-
burger, and Flemming. These were followed by the noteworthy achieve-
ments of Boveri, Driesch, Herbst, Morgan, Loeb, and others. These
men laid the foundations for the work which has followed, and their
researches, greatly aided by the development of new refinements in
microtechnique,^ ushered in modern cytology.

A powerful stimulus to investigation w^as given when the zoologists
Hertwig, von Kolliker, and Weismann, and the botanist Strasburger,
concluded independently and almost simultaneously (1884-1885) that
the nucleus is the "vehicle of heredity," an idea which Haeckel had put
forward as a speculation in 1866. The announcement of this conception
led to an even more intensive study of the nucleus and of its role in hered-
ity, a study which is now in progress and which, more than any other
one thing, can be said to characterize the work of our modern period.

Special mention should be made of the theory developed by August
Weismann (1834-1914), because the modern nuclear theory of heredity,
although resting on a substantial foundation of observational and
experimental evidence, is largely an outgrowth of his speculations.
It may be noted that Weismann incorporated in his theory several points
of earlier theories, particularly those of Darwin, de Vries, and Nageli.^
His various hypotheses were set forth in his Das Keimplasma (1892)
and in more elaborated form in his Vortrdge iiher Deszendenztheorie (1902).

Weismann identified the supposedly distinct inheritance material, or
germ-plasm (idioplasm), about which there had been much speculation,
with the chromatic substance of the nucleus. His conception of its
constitution was essentially as follows. The ultimate living unit is the

6 For the history of staining, see Conn (1928a6, 1929, 1930a6, 1933), Conn et al.
(1929), Conn and Kornhauser (1928), Kornhauser (1930), and Conn and Cunningham
(1932).

' For fuller treatments of this subject, see Kellogg (1907), Delage and Goldsmith
(1913), Thomson (1899, 1913), ConkUn (1915), and the second edition of this book.

442 INTRODUCTION TO CYTOLOGY

biophore, a minute particle capable of growth and reproduction. The
many kinds of biophores in a given cell are the elements upon whose
presence the development of the cell's characters depends. The bio-
phores are grouped to form units of a higher order, known as determinants.
The determinant, since it is composed of the many kinds of biophores, has
the power of determining the development of a certain type of cell or
group of cells. In general, therefore, there are as many sorts of deter-
minants in the organism as there are types of cells, or "independently
variable parts."

The determinants are, in turn, grouped into ids. A single id contains
all the kinds of determinants and so stands for the sum of all the charac-
ters of the organism. The ids in a given species differ only slightly
among themselves, the differences corresponding to the variations
observed within the species: they are the "ancestral germ-plasms"
contributed by past generations. The ids are identified with the visible
chromatic granules in the nuclear reticulum or in the chromatic thread
during mitosis. In most cases the ids are grouped to form idants, or
chromosomes. The id, rather than the chromosome, is the unit of
primary importance. The several ids in a chromosome are arranged in a
linear series, as suggested for the hereditary "qualities " by Roux (1883).

Quoting Wilson (1900) again.

The end of fertilization is to produce new combinations of variations by the
mixture of different ids. Since, however, their number, like that of the chromo-
somes which they form, is doubled by the union of two germ-nuclei, an infinite
complexity of the chromatin would soon arise did not a periodic reduction occur.
Assuming, then, that the "ancestral germ-plasms" (ids) are arranged in a linear
series in the spireme thread or the chromosomes derived from it, Weismann
ventured the prediction (1887) that two kinds of mitosis would be found to occur.
The first of these is characterized by a longitudinal splitting of the thread, as
in ordinary cell-division, "by means of which all the ancestral germ-plasms are
equally distributed in each of the daughter-nuclei after hav ng been divided into
halves." This form of division, which he called equal division (^quat'ons-
theilung), was then a known fact. The second form, at that time a purely
theoretical postulate, he assumed to be of such a character that each daughter-
nucleus should receive only half the number of ancestral germ-plasms possessed
by the mother-nucleus. This he termed a reduction division (Reduktions-
theilung) and suggested that this might be effected either by a transverse
division of the chromosomes or by the elimination of entire chromosomes without
division. By either method the number of "ids" would be reduced; and Weis-
mann argued that such reducing divisions must be involved in the formation
of the polar bodies and in the parallel phenomena of spermatogenesis.

With the aid of this elaborate mechanism Weismann explained onto-
genetic development in the following manner. In the zygote from which
the individual is to develop, all the kinds of determinants are present:
those of the female parent were contained in the egg nucleus and those

HISTORICAL SKETCH 443

of the male parent were brought in by the nucleus of the spermatozoon.
During the long series of nuclear divisions beginning with that in the
zygote and ending with the completion of the mature organism, the
many kinds of determinants are sorted out through a progressive dis-
integration of the ids and are distributed in a definite and orderly manner
to the different parts of the body. Many somatic mitoses are therefore
regarded not as equational ("erbgleich'^) but in reality qualitative
("erbungleich"). When a given determinant finally reaches the proper
cell, i.e., when that cell is finally formed, the determinant splits up into
its constituent biophores, and these, through their action on the proto-
plasm, give to the cell its specific characters. The general character of a
cell is accordingly due to the type or types of determinant which it
receives.

Weismann accounted for the presence of a complete outfit of deter-
minants in the gametes and zygote, and hence for the phenomenon of
hereditary resemblance, by assuming that a certain portion of the
complete germ-plasm is carried along unchanged during ontogenesis and
is delivered intact to the germ-cells. He thus rejected Darwin's sugges-
tion that representative particles (gemmules) were transmitted from all
the body-cells to the germ-cells. It had been shown that in certain
animals the primitive germ-cells are set aside at once when development
begins, and Weismann pointed out that they are therefore differentiated
before any sorting out of the hereditary units could have taken place.
Hence the germ-cells are really produced by the germ-cells of the previous
generation and not by the individual's own soma (body) ; they are present
from the beginning of development with the full hereditary outfit, and
by a few equational divisions give rise to the gametocytes. In the case
of those animals and plants whose germ-cells appear later in the ontogeny,
Weismann held that, although a sorting out of the units occurs in the
majority of the cells during ontogenesis, those meristematic cells which
constitute the chain connecting the zygote with the germ-cells — the
germ-track (iiLem6a/in)— maintain the undiminished germ-plasm. Hence
in all cases there is a continuity of the germ-plasm, if not a continuity of
the germ-cells (unless meristematic cells also are germ-cells).

Weismann argued that since there is no contribution of hereditary
elements from the soma to the germ-cells, somatic changes being in no
way impressed upon the germ-cells from which the next generation is to
arise, there can be no inheritance of acquired somatic modifications.
In multicellular animals the only inherited variations are those origi-
nating in the germ-plasm of the germ-cells or germ-track as responses to
internal (nutritive, etc.) or external environmental stimuli and those due
to recombinations of hereditary units at the time of syngamy (amphi-
mixis). He admitted that the germ-plasm, though remarkably stable,
might be altered directly by the environment (parallel modification of

444 INTRODUCTION TO CYTOLOGY

germ and soma), or even by modifications in the surrounding soma; but
he denied that in the latter case the alteration would be of such a nature
as to cause the reappearance of the same somatic modifications in the
next generation. He accounted for the internally induced heritable
variations on the basis of his theory of germinal selection. He supposed
that the determinants, while multiplying in the germ-cells, are subject
to selection like all other organic units. Some determinants, being
better placed with respect to nutritive conditions, are favored thereby
and grow stronger and more influential, while others undergo changes in
the opposite direction. The parts of the organism receiving the deter-
minants which have had the advantage in the struggle become better
developed than those receiving the weaker determinants. As this process
continues from generation to generation, the new variation gradually
increases until it becomes pronounced enough to be laid hold of by
natural selection.

A review of the points brought out in earlier chapters will show that
modern genetics, although it has shown the inadequacy of certain ele-
ments in the hypotheses sketched above, owes many of its leading ideas to
Weismann. These ideas were put to the test in the brilliant experimental
researches on development carried out by Roux, Boveri, R. and O. Hert-
wig, and others, and later in the researches of modern students of cyto-
genetics. Weismann's view that heredity is conditioned primarily by the
genetic continuity of germ-plasm has its modern expression in the
statement that a specific type of nuclear composition, upon which the
development of characters largely depends, is maintained by growth and
division from generation to generation. That this composition or organ-
ization is preserved only in germ-cells sharply distinct from somatic
cells is, however, a conception which no longer squares with the results of
experiment. It now appears that the complex of nuclear genetic units
is complete in both vegetative and reproductive cells, the differentiation
of cell types not being due to any sorting out of the units during onto-
genesis. Our knowledge in this field is little more than fragmentary,
but it seems likely that differentiation is largely a response to the diverse
conditions inevitably arising in a growing mass, such conditions stim-
ulating different groups of genes to action at different stages and in
different regions. The results of such action are, in turn, a part of the
cause of what follows. The gene, moreover, is now regarded as a con-
stitutional factor somehow involved with others in the metabolic proc-
esses and thus influencing the development of many characters, rather
than something standing for the characters of a complete organism or a
structural part thereof as did Weismann's id and determinant.

The "germ-plasm," if this term is to be retained for the genes or
chromosomes, thus represents an integral part of a developing system
rather than an arbitrary determiner of development. For this reason

HISTORICAL SKETCH 445

many prefer to apply the term, if at all, to the entire protoplasmic system
capable of differentiation and reproduction (c/. p. 421). With regard
to the origin of heritable variations, geneticists are still in accord with
Weismann in attributing them chiefly to hybridization and alterations in
the inheritance units themselves. They are not, however, inclined to see
in any process like "germinal selection" the underlying cause of such
gene mutations. Weismann's prediction that there would be found a
reduction in the number of genetic units at gametogenesis (in animals)
by a special form of nuclear division has been fulfilled, though the precise
manner in which it is accomplished differs from that postulated
by him.

Notwithstanding the abandonment of Weismann's theory of onto-
genesis and the changes made in his theory of heredity, his influence on
both cytology and genetics can never be forgotten, chiefly because of his
emphasis on the need for careful studies of the nuclear mechanism at the
critical stages of the life history, and upon the idea that this mechanism
is in some way bound up with the phenomena of heredity. "It has been
Weismann's service to place the keystone between the work of the
evolutionists and that of the cjrtologists " (Wilson, 1900).

The Twentieth Century. — The year 1900 marks the beginning of a new
era in cytology, for reasons which may be stated in the words of Wilson
(1924):

This era of cell research coincides with the new era in genetics that opened
in 1900 with the rediscovery of the Mendelian phenomena of heredity by de
Vries, Correns, and Tschermak. This discovery was the outcome of purely genetic
experiments on hybrids; but almost at the moment of its announcement, by a
remarkable coincidence, cytologists had independently arrived at a point where
the cytological basis of the phenomena could be clearly recognized. Riickert
eight years earlier (1892) had briefly suggested a conjugation and disjunction of
corresponding paternal and maternal chromosomes in meiosis and an exchange
of material between them ("amphimixis of the chromosomes"), thus to a certain
extent foreshadowing the modern explanation of the Mendelian segregation
and of recombination by "crossing-over." Montgomery (1901), without knowl-
edge of Mendel's fundamental law of segregation, brought together almost all
of the essential data for its explanation, though he did not bring them into
specific relation with the genetic phenomena. He pointed out the constant size
differences of the chromosomes, emphasized the presence in the diploid groups
of paternal and maternal homologues in pairs, and accepted the conjugation
of these homologues in synapsis and their disjunction in the reduction division.
Boveri, in his remarkable paper on multipolar mitosis (1902), demonstrated
experimentally the determinative action of the chromosomes in development
and proved their qualitative differences in this respect. A possible connection
between the Mendelian disjunction and the reduction division was suggested
nearly at the same time by several observers, including Strasburger, Correns,
Guyer, and Cannon. It was, however, Sutton (1902, 1903) who first clearly set

446 INTRODUCTION TO CYTOLOGY

forth in all its significance the cytological explanation of the Mendelian phe-
nomena that is offered by the behavior of the chromosomes, and thus initiated
the remarkable movement in this direction that followed.

It was in such a manner that cytology was brought into an alliance
with genetics. As in other instances in the history of science, the frontier
of one field of research turned out to be the border of a neighboring field,
and the gratifying yield of significant results along the line of meeting
has been due in no small measure to the fact that those who formerly
worked independently on the two sides can now employ their combined
methods and speak the same language. The field of physics has con-
tributed a valuable tool in the form of X-radiation. By means of this
tool workers in modern cytogenetics are now able to obtain desired data
far more rapidly than would be possible without it, and they are entitled
to hope that they may some day exercise a fuller measure of control over
the course of evolution by some such means.

Closely associated with the movement outlined above has been
another line of investigation characteristic of the present century, namely,
the study of the morphology of the chromosomes and the comparison of
the chromosome complements of related organisms. Research in this
field was stimulated by the discovery of heteroploidy and observations on
chromosome behavior in hybrids early in the century (p. 339 et seq.), while
its problems were placed in a much clearer light by the work on the
morphology of individual chromosomes begun about 1910 by S. Nawas-
chin (1857-1930) and his associates. Such researches have already
yielded important evidence with regard to systematic relationships, par-
ticularly among plants, and they promise to contribute largely to the
solution of many outstanding problems of this nature. During
the years which lie ahead, one of the most fruitful regions in the
field of biology with its disappearing hues of subdivision should be
this cytotaxonomy.

Of special importance also is the modern renewal of the investigation
of protoplasm, its inclusions, its differentiations, and its reactions in the
living state. This type of study has been greatly promoted not only by
the development of methods of tissue culture and micromanipulation
but also by the conception of protoplasm as a colloidal system. Investi-
gations in this field are removing many misconceptions growing out of the
too exclusive use of fixed material and are yielding partial explanations
for a variety of puzzling cytological phenomena. Moreover, they are
bringing cytology into ever more intimate associations with physical
chemistry, physiology, and experimental medicine, just as the study of
chromosomes has allied it with genetics and systematics. To such fields
cytology has made invaluable contributions; in return it has received
incentives to deal more directly and experimentally with major problems

HISTORICAL SKETCH 447

as well as with objects. Every field concerned has thus gained a wider
appreciation of the significance of its own data. No tendency of the
present is more encouraging to the investigator and promising for the
future of biology than the development of such alliances, for they afford
our only strong hope that we shall come nearer to a solution of the
peculiar problems presented by living organisms.

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454 INTRODUCTION TO CYTOLOGY

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456 INTRODUCTION TO CYTOLOGY

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458 INTRODUCTION TO CYTOLOGY

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464 INTRODUCTION TO CYTOLOGY

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476 INTRODUCTION TO CYTOLOGY

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504 INTRODUCTION TO CYTOLOGY

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506 INTRODUCTION TO CYTOLOGY

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510 INTRODUCTION TO CYTOLOGY

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512 INTRODUCTION TO CYTOLOGY

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514 INTRODUCTION TO CYTOLOGY

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516 INTRODUCTION TO CYTOLOGY

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1880.

1882a.

18826.

1884a.

18846.

1888.

1889.

1892.

1893.

1894.

1895.

1897a.

18976.

1898.

1900a.

19006.

1900c.

1901a.

19016.

1904a.

19046.

1904c.

1905a.

1907a.

19076.

1907c.

1908.

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19106.

1910c.

1910f/.

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532

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INDEX

Numbers in bold-face indicate pages bearing illustrations.

Aase, 121, 342, 356, 360

Abderhalden, 100

Abegg, 99, 100

Aberrant mitosis, 184—188

Abies (fir), 95, 235

Abnormal mitosis, 184, 186

Abraxas (moth), 380

Abromavich, 398

Abulilon (angiosperm), 417

Acacia (angiosperm), 164

Acer (maple), 237

Acetabularia (green alga), 279

Achlya (fungus), 105, 229

Achromatic figure, 149-164, 440

Aconilum (angiosperm), 129

Acqua, 58

Acquired somatic modification, 443

Acrididae (see also Grasshopper), 130, 130

Acroblast, 78, 204, 216, 219, 220

Acrosome, 78, 204, 216, 219, 220, 221, 241

Actinophrys (protozoan), 277, 278

Actinosphcerium (protozoan), 194, 195, 277

Activation of egg, 247

Acton, 192

Addoms, 188

Adsorption, 38, 89

JUgilops (angiosperm), 128, 129, 366

^gilotricuni (angiosperm), 368

/Ethalium (slime mold), 26

Afzelius, 341, 345, 348, 405

Agar, chromidia, 195
chromosome, 116, 142
meiosis, 256, 272
nucleus, 48

sex-chromosome, 378, 380
syngamy, 239

Agathis (conifer), 23, 24, 207, 235

Agave (century plant), 103

Agglutination, 248

Aggregata (protozoan), 277

Aglaozonia (brown alga), 280

Agropyrum (angiosperm), 128

Aida, 378

Akkeringa, 381

Albach, 53

Alberti, 187

Albugo (fungus), 10, 200, 201, 229

Albumin, 84, 96

Alchemilla (angiosperm), 402, 404, 405

Aleurodiscus (fungus), 230, 386

Aleurone, 96, 98, 101, 103

Alexander, 144, 312

Alexieff, 82

Algae, apomixis, 402

cell wall, 177

gametogenesis, 196

heredity, 306

meiosis, 278-280

mitosis, 159, 191

plastids, 63, 64

sex, 386

sporogenesis, 196

syngamy, 226-228
Alkaloids, 96
Allelomorph, 289, 310
Allen, C. E., cell wall, 176

chromomeres, 142

cytokinesis, 171, 174

heredity in bryophyte, 307

meiosis, 250, 262, 266, 279, 283

recombination, 302

sex determination, 382, 384, 395

spermatogenesis, 201, 202, 203
Allen, R. F., 204, 231, 387
Allium (onion), canaliculi, 79

chondriosomes, 83

meiosis, 258, 267

parthenogenesis, 402, 404

root tip, 5, 79

somatic chromosomes, 124, 130, 132, 133, 134

tonoplast, 42
AUoheteroploidy, 340, 348, 369
Allomyces (fungus), 199, 281
AUopIasm, 45
Allosynapsis, 362
Alnus (angiosperm), 104
Aloe (angiosperm), 129, 130, 177, 271
Altenburg, 187, 311, 316, 325, 395
Alternation of generations, 122, 196, 279-281, 401
Altmann, 26, 82, 89, 434
Alvarado, 90
Alveolar spheres, 32
Alveolar theory of protoplasm, 434
Alveolation theory of chromosomes, 132, 140
Alverdes, 51

Alyssum (angiosperm), 357
Alytes (toad), 272
Amblycorypha (katydid), 382
Amblystegium (moss), 405
Ameiosis, 345
Ames, 387

Amici, 432, 436, 437
Amides, 96

Amitosis, 183-185, 439
Amoeba (protozoan), 39, 43, 58, 59
Amphiaster, 156

533

534

INTRODUCTION TO CYTOLOGY

Amphiastral figure, 153-159

Amphibia, 114

Amphidiploid hybrids, 367-371

Amphimixis, 401

AmphitSne, 256

Amphitornis (insect), 265

Amygdaius (angiosperm), 103

Amyloplast, 62, 65, 98

Amylose, 99

Anabcena (blue-green alga), 191, 192

Anaphase, meiotic, 267, 262

somatic, 106, 107, 109, 134, 135
Anastomoses, 54, 106, 136, 137
Anastral figures, 149-153
Ancel, 272

Anderson, D. B., 176-178
Anderson, E. G., 30, 266, 302, 306, 310, 353, 393,

415,416,419
Anderson, R. J., 30
Andersson-Kotto, 405, 415
Andrews, E. A., 18
Andrews, F. M., 18, 57, 58, 161
Androcyte, 202, 203
Androgenesis, 407, 412
Androgone, 202, 203
Androspore, 206
Andrus, 231

Anesthetizing agents, 186
Aneuploidy, 339, 341
Anisogenomatic, 340
Anitschkow, 83
Ankel, 401

Anomcpontis (diatom), 386 '

Antecedent genom, 419
Antennaria (angiosperm), 402, 403, 407
Antheridium, 197, 229, 230
Anthoceros (liverwort), meiosis, 283
plastid, 61, 63, 70
pyrenoid, 68, 69
syngamy, 233
zygospore, 201

Anthocyanin pigments, 96, 97

Anthoxanthurn (angiosperm), 133

Anthurium (angiosperm), 103

Antipodal cells, 183, 210, 211, 237

AntirThinum (angiosperm), 97, 342, 415

Aphis (aphid), 411, 413

Apical body, 71, 81, 202, 203, 204, 222

Apical cell, 12, 93

Apis (bee), 410

Aplanospores, 198

Aplocheilus (fish), 378, 393

Apogamy, 403

Apomixis, 401-413

Apospory, 404, 405

Apotettix (grasshopper), 410

Apposition, 177

Aquilegia (angiosperm), 367, 370

Arabis (angiosperm), 415

Araratian, 121, 124, 187, 321

Arbacia (sea urchin), 32, 40, 164, 221

Arber, 49, 183

Archegonium, 201, 206, 233

Archieracium (angiosperm), 402

Archoplasm, 44

Arctostaphylos (angiosperm), 103

Arcyria (myxomycete), 278

Ariscema (angiosperm), 396

Aristotle, 422

Arnold, 85, 87, 88, 379

Arrangement of chromosomes, 125

Arrhenatherum (angiosperm), 54, 111, 171

Artemia (crustacean), 343, 411, 413

Artemisia (angiosperm), 405

Arthur, 231, 283

Artichoke, 103

Artom, 343

Artschwager, 238

Ascaris (nematode), centrosome, 153

chromosomes, 132

fertilization, 240, 244

meiosis, 263, 272, 440

sex-chromosomes, 376, 377, 378

spermatozoon, 222
Ascidian, 182

Asdepias (angiosperm), 210, 236
Ascobolus (fungus), 281, 387
Ascogonium, 229
Ascomycetes, achromatic figure, 166, 157, 158

meiosis, 281

sex, 387

spore coat, 181

spore formation, 167, 173, 201, 230

syngamy, 229, 230
Asilus (insect), 272
Asparagin, 94, 96
Asparagus (angiosperm), 90
Aspidiotus (insect), 411
Aspidium (fern), 404, 405
Asplenium (fern), 405
Astaurow, 129
Astbury, 178, 179

Aster, 3, 111, 149, 155, 156, 157, 170, 244
Asterias (starfish), 154, 411
Astral rays, 157
Asynapsis, 273, 345, 359
Atamosco (lily), 402, 407
Atelomitic, 116
Athyrium (fern) 402, 405
Atkinson, 226, 281
Attachment constriction, 116
Aucuba (angiosperm), 329
Auerbach, 441

Autoheteroploidy, 340, 348, 350-358
Autosome, 376
Autosynapsis, 362
Auxin, 19
Auxocyte, 251
Auxospore, 228
Avdulow, 121, 128
Avena (oats), 343, 416
Avery, 124, 187, 188, 320, 356
Axial filament, 217, 219, 221
Axial gradient, 19
Axon, 13, 14
Azolla (water fern), 138

B

Baache-Wiig, 96

Babcock, 128, 139, 142, 260, 268, 286, 367

INDEX

535

Baccarini, 56

Bacillus, 89, 193

Back-cross test, 289, 295

Bacteria, 82, 89, 100, 177, 193, 194

Bacterium, 194

de Baehr, 411, 413

von Baer, 425

Bagchee, 156, 157, 158, 281

Bailey, E. W., 21, 436

Bailey, I. W., 40, 51, 94, 96, 97

Baird, 229

Balanced emulsions, 36

Balanophora (angiosperm), 346

Balbiani, 61, 141

Balfour, 439

Ballowitz, 222

Balls, 176, 178

Baltzer, 397, 412

Bancroft, 33, 169

Bangham, 342

Banta, 397

Baranetzky, 132

Baranov, 118

Barkley, 176

Baron, 188

Barry, 438

Bartlett, 336, 358, 396

de Bary, 23, 403, 433-436

Basal granules or corpuscles, 203, 205, 224

Basic number of chromosomes, 340, 347

Basichromatin, 54, 55

Basidiobolus (fungus), 281

Basidiomycetes, gametogenesis, 200

meiosis, 282

sex, 386

syngamy, 230
Basidiospores, 200
Basidium, 200, 230, 282
Bast, 184

Bataillon, 154, 248
Bateson, 286, 308, 351
Bauch, 282
Baumgartel, 192
Baur, 286, 392, 415, 416
Bayliss, 25, 33, 38, 40, 43
Beadle, 271, 273, 360, 371
Beams, 58, 78, 244
Beardsley, 233
Beauverie, 64
Bechhold, 33
Becker, 58, 172
Beckwith, 85
Bee, 410

Beer, 49, 66, 180, 181, 183
Beikirch, 31
Belajeff, 199, 204, 208
BSlaf, achromatic figure, 155, 161, 162, 163

cell-plate, 171, 172

chiasraa, 268

fixation, 7

flagella, 223

fragmentation, 316

furrowing, 169

meiosis, 256, 277

Mendelism and chromosomes, 286

BMaf, nucleus, 189

parthenogenesis, 411

reticulum, 54

sex, 397

somatic mitosis, 108, 109, 112

spindle attachment, 116

syngamy, 245
Bellamy, 381

Bellevalia (angiosperm), 128
Belling, chromomeres, 142

chromonema, 139

chromosome fragments, 320

chromosome morphology, 124

genes, 144

meiosis, 258, 267, 268, 270, 271, 273

meiosis and heteroploidy, 351, 352

monoploid Datura, 356, 406

non-disjunction, 345

reciprocal translocation, 327-329, 331, 335

reticulum, 54

spindle attachment, 116

temperature effect, 186

trisomic mutants, 298, 327, 343
Belzung, 100
Benda, 82, 87
van Beneden, achromatic figure, 159

centrosome, 153

cytology and heredity, 439, 441

individuality of chromosome, 141, 145

mitosis, 159, 440

protoplasmic structure, 434
Benetzkaja, 367
Benoist, 53
Bensaude, 230
Bensley, 79, 80, 84, 95
Berberidaceae, 129
Berberis (angiosperm), 18
Berg, 368
von Bergen, 73
Berghs, 256, 266
Bergner, 124, 327, 337
Bergon, 228
Bernal, 178
Bernard, 58, 441
Bernhardi, 426
Berridge, 235
Bersa, 186, 187

Bertholletia (Brazil nut), 101, 103
Besley, 354

Beta (angiosperm), 186, 238, 347
Beutner, 20, 38, 40, 42, 180
Beyer, 49
Bhatia, 88, 225
Bhattacharya, 78
Bichler, 187

Bicornes (angiosperms), 342
Biddulphia (diatom), 280
Binder. 139
Binnenkorper, 189
Binuclearity hypothesis, 194
Binz, 100

Bioblast, 82, 89, 434
Biogen, 46
Biophore, 442
Biourge, 180

536

INTRODUCTION TO CYTOLOGY

Bisceglie, 187

Bivalent chromosomes, 252, 351, 440

Black, 233

Blackburn, 347, 357, 305, 367, 390

Blackman, M. W., 272

Blackman V. H., 210, 230, 231, 235, 283

Blair, 283

Blakeslee, Datura chromosomes, 124

gene mutation, 310

heteroploidy, 343, 362, 358

monoploid sporophyte, 356

non-disjunction, 345

pollen tube growth, 293

primary mutants, 327

radium treatment, 188, 311

sex, 387, 388, 398

tetraploidy, 351

translocation, 323, 329, 335-337

triploidy, 354

trisomic mutants, 298
Blasia (liverwort), 201
Blastomere, 243, 438
Bleier, 149, 157, 161, 163, 164, 186, 342, 356, 366,

367
Blephariama (protozoan), 44
Blepharoplast, 198, 199, 201-208, 202, 205, 207,

223, 234
Blood, 14. 49, 73, 89
Blue-green algjE, 191-193
Blunt, 133
Bobilioff-Preisser, 58
Bock, 22
Boeck, 190
Boedijn, 334

BcBhmeria (angiosperm), 178
Boeke, 13
Bokorny, 79
Bold, 68
Bolleter, 201
Bone, 14
Bonnet, C, 424
Bonnet, J., 183, 196, 278
Bonnevie, 132, 133, 142, 266
Boos, 402
Border brim, 205
Bordered pit, 175
Borelli, 424
Borgenstam, 186
Boring, 378, 381
Borodin, 188
Borzl, 16
Bosaeus, 410
Bose, 20, 79
Botrychium (fern), 181
Bouin, 93

Bougainvillea (angiosperm), 3CS
Bouquet stage, 250
Bourquin, 65
Bouygues, 83, 90
Boveri, amitosis, 187

centrosome, 153

cytology and heredity, 439, 444

dispermy, 347

fertilization, 244

individuality of chromosome, 145, 146, 440

Boveri, nucleios size, 51

parthenogenesis, 412

role of chromosomes, 445

sex-chromosomes, 378, 381
Bowen, chondriosome, 86, 89, 90, 91

Golgi material, 73, 75, 70, 79, 80

heteroploidy, 340

leucoplasts, 62

plastids, 09, 70, 91

secretion, 75 ff.

spermatogenesis, 201, 203, 214

spermiogenesis, 215-223, 216, 217, 218, 219, 221

spindle, 164

syngamy, 241
Bowenia (cycad), 234, 235
Bower, 404
Bozler, 13
Brachet, 412, 420
Brachiomonas (green alga), 68
Brachymeiosis, 281

Brachystola (grasshopper), 122, 254, 272
Bragg, 178
Brambell, 74, 397
Brand, 165, 166
Brassica (angiosperm), 342, 346, 364, 365, 367,

370
Brauer, 376, 411
Braun, 433
Bremer, 369
Breslawetz, 236
Bresslau, 121
Bridges, crossing-over, 306

factorial hypothesis, 312

fragmentation, 320

gene theory, 144, 309, 312

homologous chromosomes, 123

linkage, 301

meiosis, 206

mutation, 310

non-disjunction, 345

sex, 394

translocation, 321

triploidy, 353
Brieger, 293, 340, 305
Brill, 179

Brink, 99, 100, 293, 308, 329, 332
Brochymena (insect), 218, 219
Brodie, 388
Brooks, F. T., 230
Brooks, W. E., 281
Brooks, W. K., 47, 158
Brown, A. P., 30
Brown, H. B., 230
Brown, R., 427
Brown, V., 223

Brown, W. H., 158, 192, 230, 237, 281
Brownian movement, 6, 31, 43, 53, 161
Bruchus (insect), 376
Briicke, 433
Bruns, 100
Brunswik, 386
Bryonia (angiosperm), 388
Bryophytes, cytoplasmic inheritance, 418

gametogenesis, 201-204

heredity in, 307

INDEX

537

Bryophytes, meiosis, 283

plastid, 63, 71, 80

sex-chromosomes, 382

sporogenesis, 204

syngamy, 233
Bryopsis (green alga), 8, 22
Bryum (moss), 405
Bucciardi, 187
Buchholz, J., 293, 311
Buchner, 194, 411
Bucholtz, 188
Buchtien, 204
Buck, 90
Bud sport, 311
Buder, 17, 278
Bufo (toad), 80
Buller, 230
Bunting, 190, 223
Burgeff, 229, 387
Burmannia (angiosperm), 404
Burnham, 100, 293, 322, 327, 329, 330
Burrows, 6

Bursa (angiosperm), 342
Biitschli, achromatic figure, 160, 440

blue-green algse, 192

cytology and heredity, 441

furrowing, 169

polar bodies, 438

protoplasm, 434
Buxton, 346, 367

Cabomba (angiosperm), 69, 85

Cajal, 73

Caldwell, 207

Calkins, 43, 160, 189, 223, 245, 246, 277

Callisia (angiosperm), 267

Callithamnion (red alga), 280

Callose, 167, 180

Calopogon (orchid), 236

Calycanthus (angiosperm), 402

Cambium, 12, 51, 94, 97

Camerarius, 436

Cameron, 29

Camp, 398

Campanula (angiosperm), 329, 351

Campbell, A. S., 223

Campbell, D. H., 204, 233, 437

Canaliculi, 79

Cancer problem, 187

Canis (dog), 376

Canna (angiosperm), 354

Cannabis (hemp), 343, 346, 390, 396, 397

Cannon, 125, 169, 445

Canti, 3, 188

Caoutchouc, 97

Capinpin, 352

Carbohydrate, 27, 96, 98-100, 99

Carbohydrate-protein ratio, 30

Carchasium (infusorian), 277

Carex (sedge), 341

Carleton, 50, 57

Carlson, 199

Carney, 434

Carothers, 115, 116, 123, 141, 205

Carotin, 64

Carpogonium, 228

Carrel, 6, 47

Carruthers, 158, 230, 281

Carter, G., 41

Carter, N., 63, 68, 191, 280

Cartilage, 14, 16, 171

Cartledge, 356

Cams, 438

Cassaigne, 96

Castetter, 167, 168

Castle, 286, 290, 311

Castrada (flatworm), 222

Cat, 378

Catalysis, 38

Catcheside, 271, 304, 334, 337, 352, 356

Catenation, 332

Catherinea (moss), 71

Cathode ray, 187

Cattaneo, 78

Cattle, 376

Caulerpa (green alga), 8, 10, 11, 190

Cavers, 82, 90

Cell, discovery, 2, 423
enucleated, 58
number, 9, 357
size, 23, 357

Cell-division, 110, 430

duration and periodicity. 111

Cell membrane of animals, 181

CeU-plate, 109, 110, 150, 171-174, 172

CeU sap, 2, 29, 96

Cell theory, 20 #., 428

Cell wall, 4, 12, 100, 165-168, 174-181

Cells and tissues, 1-24

Cellulose. 100, 176, ISO, 182
in animals, 182

Central spindle. 111, 155

Centrifuged cells, 31, 32, 57, 58, 84, 161

Centriole, 3, 153, 155, 215, 217, 221

Centroblepharoplast, 223

Centronema, 223

Centrosome, 3, 153, 154, 156, 169
in mitosis, 110
in syngamy, 244
Centrosphere, 3, 153
Centrurus (scorpion), 86
Cephalobrachial chromosomes, 116
Cephalotaxus (conifer), 95, 235
Ceratiomyxa (slime mold), 278
Ceratium (dinoflagellate), 190
Ceratopteris (fern), 138
Ceratozamia (cycad), 234, 440
Cerebratulus (worm), 154
Chcenia (protozoan), 51
ChcBTocampa (insect), 360
Chcetomorpha (green alga), 279
Chcetopterus (annelid worm), 23, 412
Chalaud, 70

Chamberlain, cell-plate, 173
cytokinesis, 167
heteroploidy, 342
life cycle, 196
oogenesis, 206

538

INTRODUCTION TO CYTOLOGY

Chamberlain, spermatogenesis, 207

syngamy, 234-236, 239
Chambers, achromatic figure, 157, 161, 164, 170

amitosis, 184

Brownian movement, 32

chondriosomes, 83, 85, 86

chromosome, 142

ectoplasm, 44

Golgi material, 74

hydrogen-ion concentration, 29

meiosis, 256

microdissection, 6, 142

nucleus, 52-54, 59

parthenogenesis, 411

plasma bridges, 18

plasma membrane, 39, 40

syngamy, 241, 242

tonoplast, 42

viscosity, 31
Champy, 50
Chang, 74
Chara (stonewort) and other Charales, 183, 199,

227, 279, 402
Chatton, 278
Chiarugi, 212, 402. 405

Chiasma, 257, 259, 260, 268. 269, 271, 337
Chicken, 381, 393
Chicliering, 215
Child, 19, 20, 51
Chilodon (infusorian), 277
Chiloscyphus (liverwort), 283
Chimera, 311, 343, 357, 367
Chipman, 356
Chironomus (insect), 61
Chitin, 177, 179, 182
Chittenden, 415, 419

Chlamydomonas (green alga), 68, 223, 277
Chloralized cells, 115, 185, 186
Chlorococcum (green alga), 68
Chlorophyll, 64, 67, 192

inheritance, 414-418
Chloroplast, 63 67, 68
Choaborus (insect), 378
Chodat, 256
Cholesterol, 27
von Cholnoky, 228, 280. 386
Chondrilla (angiosperm). 402
Chondriocont, 83
Chondriome. 83
Chondriomite. 83
Chondriosomal mantle. 151, 152
Chondriosome, 3, 82-92, 214
function, 87

relation to plastid, 90 ff.
r61e in secretion, 77
in spermatogenesis, 86
in spermiogenesis, 215, 218, 221
in sporogenesis, 85, 86
in syngamy, 244
Chorthippus (grasshopper), 7, 112, 162, 169, 256,

316
Christiansen, 190, 223, 232
Christman, 231
Chromatid, 252, 267, 264
Chromatin, 27, 52, 55

Chromatium (bacterium), 43
Chromatophore, 62
Chromidia, 194
Chromioles, 55, 141, 143
Chromocenter, 2, 56
Chromomere, 142-144, 312
in meiosis, 259, 260
in reticulum, 56
theory. 132, 141
Chromonema, 54, 105, 106, 114, 133, 134, 136,
139, 140, 142-144, 260, 264, 312, 335
theory, 132
Chromoplasts, 62 ff.
Chromosomal vesicle, 136
Chromosome cycle, 251, 291
Chromosomes, 105 ff.

aberrations, 185 ff., 359 ff.
alveolation, 132. 140
arm, 116

arrangement. 125
balance among, 325
basic number, 340, 347
complement, 121 ff.
constrictions. 115 ff.
continuity. 145

fragmentation, 117. 185, 314 ff., 349
in heredity, 284 ff.
heteromorphic, 265, 272
historical. 439
homologous pairs. 252. 272
human, 379
in hybrids, 359 ff.
individuality, 145

knob, 119, 123, 271, 298, 305, 318, 332, 333
in life cycle, 122, 261, 291, 383, 440
map, 299, 301, 323, 324
matrix, 106, 133-144
in Mendelian heredity, 291 ff.
morphology, 114-131, 349, 446
multivalent, 304, 356
non-homologous association, 276
nucleolus-forming region, 118-121
number, 121, 339 ff.
alterations, 344

and taxonomy, 126, 340 ff., 446
pairing in somatic cells, 123, 126, 272
satellites, 118 ff.
set, 121, 254, 325
sex, 297, 375-400
size and shape, 114 ff.
small, 138
splitting of, 105, 113, 133, 137, 145, 190. 265,

363. 440
splitting in meiosis, 252, 255, 258, 261, 265, 275
structure, 132-148
tetrads, 252 ff.
trivalent in synapsis, 274
A'-chromosome, 304, 376 ff.
F-chromosome, 304, 378 ff.
Chrysanthemum (angiosperm), 340, 345
Cienkowski, 433

Cilia, 43, 197, 203, 207, 208. 223. 229, 233
Ciliary mechanism, 224. 225
Ciliated cells, 184, 223, 224, 225
des Cilleuls, 184

INDEX

539

Cirdnella (fungiis), 165
Circotettix (grasshopper), 320, 329
Cirri, 43

Citrus (angiosperm), 405

Cladophora (green alga), alternation of genera-
tions, 279

body structure, 8, 23, 49

cytokinesis, 165, 166

eyespot, 67

mitosis, 190, 191

nuclei, number, 9

sex, 386
Clark, 178

Clarkia (angiosperm), 329
Clausen, J., 139, 142, 260, 268, 273, 342, 361,

415, 416
Clausen, R. E., 286, 345, 356, 365, 367, 407
Claussen, P., 158, 199, 230, 281
Cleavage of egg, 168-171, 242-244

furrowing, 165-171

historical, 438

and promorphology of ovum, 23

rate, 420
Cleland, meiosis, 280, 334

nucleolus, 58

CEnothera, 334, 336, 336

translocation, 336, 337
Clivia (angiosperm), 177
Closing membrane, 175
Closterium (desmid), 166, 279
Clowes, 36, 37, 41
Coagulation, 37, 53
Cobb, 336

Cocconeis (diatom), 228
Codium (green alga), 190, 279
Ccenocentrum, 200, 229
Coenocytes, 8, 10, 21-23, 48, 197
CcEnocytic embryo, 23, 24
Coenogametes, 10
Cohen, 29
Cohn, 433
Coker, 235
Cole, 424

Coleochwte (green alga), 227, 279
Colley, 283
Collins, G. N., 407
Collins, J. L., 124, 363
Colloidal state, 33 ff., 434
Colorblindness, 392
Commdina (angiosperm), 181
Complement of chromosomes, 121 ff., 340 ff.
Components (of colloids), 34
Conard, 184, 228
Conduction of stimuli, 18-20, 39
Conductivity of protoplasm, 180
Conidia, 167, 200
Conjugate division of nuclei, 229
Conjugation, in alg®, 228

in Paramoecium, 245
Conklin, amitosis, 183, 184

cellular differentiation, 9

cleavage, 23

cytoplasmic inheritance, 420

fertilization, 243

fibrils, 87

Conklin, individuality of chromosomes, 136, 146

mutation, 311

nucleoplasmic ratio, 51

parthenogenesis, 412

promorphology of ovum, 23

Weismannism, 441
Conn, 441

Connecting piece, 218
Connective tissue, 14, 15, 18
Conner, 415

Constrictions in chromosomes, 115, 116
Continuity of protoplasm, 16-18
Contractile vacuole. Amoeba, 39

Diplodinium, 10

discharge, 42

origin, 44

Spirogyra, 45, 228
Convallaria (angiosperm), 210
Cook, 190

Cooper, D., 329, 332, 388
Cooper, G., 199
Copeland, 410

Coprinus (mushroom), 230, 386
Corallina (red alga), 280
Corethron (diatom), 280
Cork, 176

Cornea, 76, 154, 187
Corner, 213
Correlation, 9, 15-20
Correns, cytoplasmic inheritance, 418

Mendelism, 289, 445

pollen characters, 308

recombination, 302

sex, 388, 390, 391, 396, 398

variegation, 415, 416

wall structure, 177
Corsinia (liverwort), 233
Corti, 432

Coscinodiscus (diatom), 228
Cotton fiber, 176, 178
Couch, 64, 197, 199, 387
Coulter, 167, 196, 227, 235, 236, 239
Cowdry, E. V., chondriosomes, 82, 83, 84, 87, 89,
90

chromidia, 195

Golgi material, 73-75, 78

respiration, 89
Cowdry, N. H., 82-84
Cox, 378
Crabb, 240
Craigie, 231, 386
Creighton, 121, 303, 306, 337
Crepidula (mollusk), 136, 184, 243
Crepis (angiosperm), chromomere, 142

chromosome complement, 124, 127, 349

chromosome duplication, 325

fragmentation, 320

heteroploidy, 343, 348

hybrid, 361. 362, 363, 367, 371, 372

kinetic bodies, 117

meiosis, 260

monoploid sporophyte, 356, 357

parthenogenesis, 402

somatic chromosomes, 124, 127, 130, 139

species and chromosomes, 127, 128

540

INTRODUCTION TO CYTOLOGY

Crepis (angiosperm), translocations, 314, 321
Crew, 37G, 397

Crossing-over, 266-272, 293-295, 298-306, 320,
323, 327, 337, 393

cytological evidence, 302-304

in triploid, 353

between two chromatids only, 306
Crown gall, 186
Cruciferae, 342

Cryptobranchus (amphibian), 76, 136, 243
Cryptomeria (conifer), 235
Cryptoplasm, 33
Crystallites, 178
Crystalloid, 101
Crystals, 101-103
Cucumis (angiosperm), 186
Cucurbita (angiosperm), 164
Cu6not, 375
Culex (mosquito), 344
Cumingia (mollusk), 32
Cunha, 90
Cunningham, 441
Cuscuta (angiosperm), 17
Cuticle, 176
Cutin, 176, 180

Cutteria- Aglaozonia (brown alga), 280
Cyanophycese, 191-193
Cyanophycin granules, 193
Cyanotis (angiosperm), 272
Cycad, 206, 234
Cycas (cycad), 234, 236
Cyclops (copepod), 136, 243
Cylindrocystis (green alga), 279
Cypripedium (orchid), 212
Cyrtanthus (angiosperm), 130
Cystolith, 103
Cystosira (brown alga), 407
Cytaster, 164, 248
Cytoblast, 430
Cytoblastema, 430
Cyto-idioplasm, 418
Cytokinesis, 85, 86, 105 i'.. Ill, 116, 162, 1G5-173

by furrowing, 109, 166, 165-171

in meiocyte, 263
Cytome, 83
Cytomicrosome, 82
Cytoplasm, cell constituent, 2

in heredity, 286

mantle, 235

in syngamy, 234, 236
Cytoplasmic heredity, 414-419
Cytosome, 2, 83, 91
Cytotaxonomy, 126, 340 ff., 446
Czaja, 386

Czapek, 25, 33, 93, 97, 100, 176
Czurda, 68, 190

D

Dahlgren, 210, 212, 226, 236, 239, 398

Dahlia (angiosperm), 351, 355

Da Fano, 74

Dale, 230

Daltonism, 392

DanchakofT, 195, 242

Dangeard, aleurone, 101

ascomycetes, 231

chondriosomes, 61, 69, 83, 90, 91

elements of protoplast, 104

ergastome, 102

nucleus, 53

syngamy, 229, 230

vacuole, 93-97

vital staining, 6
Dannehl, 172

Daphnia (copepod), 411, 413
Darbishire, 100
Dark, 351

Dark field, 3, 6, 43, 84
Darlington, amphidiploidy, 367

chiasma, 267, 268, 270, 271

chromosome complement, 129

disjunction, 323

fragments, 314, 319

gene theory, 312

meiosis, 256, 258, 275

QSnothera, 304, 334, 335, 337

reciprocal translocation, 329

synapsis in heteroploid, 274, 361, 352,
355
Darwin, 373, 441
Datura (angiosperm), aleurone, 103

chromosome complement, 124

heteroploidy, 343, 352, 359

monoploid sporophyte, 356

non-disjunction, 345

parthenogenesis, 402, 406

primary mutants, 327, 328

reciprocal translocation, 331, 332, 337

syngamy, 238

tetraploidy, 351

triploidy, 353, 354

trisome, 298
Davenport, 392
Davey, 396
Davis, B. M., achromatic figure, 151

algffi, 197, 278

cytokinesis, 165

heteroploidy, 345

meiosis, 283

monoploid sporophyte, 356

Oenothera, 334

oomycetes, 199

plastid, 70

protoplasmic connections, 16

syngamy, 229
Dawson, 44
Day, 43

Decaploidy, 339
Deconjugation, 272, 273
Decticus (insect), 142
Deficiency, 317, 325
Dehorne, 133
Deineka, 73, 76
Delage, 46, 441

Delaunay, 116, 124, 126, 128, 187
Ddesseria (red alga), 280
Deletion, 188, 274, 315, 317, 318
Delitsch, 230
Delphinium (angiosperm), 129

INDEX

541

Dembowski, 172

Demerec, 308, 310, 388, 398, 415, 416, 419

Dendrite, 13, 14

Deiidrucoelum (flatworm) , 258

Denhatn, 342

Dermatosome, 177

Desynapsis, 273, 345

Determinant, 442

Deutoplasm, 100

Development, 7

and cells, 20 /.

chromosome influence, 273

gene theory, 309

and heredity, 284 ff.

Weismann's theory of, 442
Developmental selection, 293
Devis6, 71, 86, 151, 152, 171
Dextrin, 99

Diakinesis, 257, 258, 260, 334
Diatoms, 228, 2S0, 386
Dictyokinesis, 75
Dictyosomes, 75, 216, 220
Dictyota (brown alga), 159, 227, 280
Didelpkys (opossum), 378, 379
Didymium (slime mold), 165, 172, 278
Dietel, 283

Differential polyploidy, 340
Differentiation, 9 /., 443, 444
Diffuse stage, 261
Digby, apomixis, 402, 403, 404

chromosome number and taxonomy, 126

hybrids, 367

nucleolus, 57, 58
Digestion, 89

Digitalis (angiosperm), 346, 361, 363, 367
Dikaryon, 230
Dikaryophase, 230, 232
Dileptus (protozoan), 245
Dinophilus (annelid worm), 399
Dioecism, 388, 398
Dioncea (angiosperm), 18
Diospyros (angiosperm), 17
Dioon (cycad), 50, 206, 207, 234
Diplocystis (protozoan), 277
Diplodinium (protozoan), 10
Diplodization, 230
Diplohaplont, 278
Diplonema, 257, 258, 259, 264
Diplont, 278
Diplosis, 226
Dippel, 177
Dipsacacese, 129
Diptera, 122, 125, 272

Disjunction, 250, 252, 255, 265, 272, 291, 322
Dislocation hypothesis, 347
Disney, 423
Dispermy, 347
Disperse phase, 33
Dispersions medium, 33
Dissosteira (grasshopper), 86, 256
Dixon, 256

Dobell, 10, 21, 193, 277, 429, 436
Dobzhansky, 123, 187, 297, 320-325, 322, 324,

329, 395, 399
Dodel, 100

Dodge, B. O., 231, 278, 282, 283, 387

Dodge, C. W., 196, 226, 231, 283

Doflein, 27, 189

Dogiel, 182

Dolley, 51

Dominance, 287

Doncaster, 239, 256, 272, 380, 382, 410, 411

Dore, 178, 179

Double crossing-over, 300

Double fertilization, 211, 236, 237, 238, 437

Double reduction, 230, 281

Doubt, 16

Douin, 382

Dowding, 387

Downing, 213

Dracinschi, 204, 205

Drayton, 387

Drew, 79, 184

Driesch, 441

Drosera (angiosperm), 339, 361

Drosopkila (fruit fly), bar eye, 304

black body, 294, 300

carnation eye, 304

chromonema, 139

chromosome complement, 122, 129, 344

chromosome map, 324

crossing-over, 302, 303, 353, 393

embryo, 24

fragmentation, 316, 318

gynandromorph, 382

inversion, 320

linkage, 294

linkage groups, 296-298

linkage map, 301

meiosis, 295

non-disjunction, 345

polyploidy, 275

reciprocal translocation, 329

recombination, 304

sex-chromosomes, 377, 378, 381

sex-linkage, 391, 392

synapsis, 272

syngamy, 243

translocation, 121, 317, 318, 321, 322, 323, 325

triploidy, 353

vestigial wings, 294, 300

X-ray treated, 187
Druner, 160, 162
Druse, 102, 103
Dublin, 272
Dubreuil, 88
Duck, 381

Duesberg, 73, 75, 82, 85, 87, 195, 379
Dufrenoy, 91, 98
Dujardin, 432
Dumas, 438
Dunn, 286
Dupler, 235
Duplex genes, 354

Duplex group of chromosomes, 292, 325
Duplication of genes, 319, 322
Duplicational polyploidy, 340
Dutrochet, 20, 426-428, 435
Dyad, 252, 262, 264

542

INTRODUCTION TO CYTOLOGY

E

Eames, 12, 24. 175, 206, 235

East, 355, 305, 407, 419

Eberdt, 100

Echinops (angiosperm), 210

Echinus (sea urchin), 57, 412

Ectocarpus (brown alga), 196, 226, 227, 280, 402

Ectoplasm, 39, 43

Ectoplast, 3, 39

Edman, 405

Edwards, 378

Eftimiu, 158

Egg, of animals, 213

of plants, 197, 206, 210, 211, 232
Egregia (brown alga), 280
Eichhorn, 29
Eisen, 55
Eisentraut, 136
Ekman, 286
Elceis (palm), 103
Elaioplast, 66, 102
Elasticity of protoplasm, 31, 37
Elastin, 182

Elatostema (angiosperm), 407
Electosome theory, 88
Electrical phenomena, 39, 52
Electrical theories of mitosis, 160
Elkner, 74

Elodea (angiosperm), 31, 44, 68, 388, 389
Emberger, 69, 83, 90
Embryo sac, 210, 212, 235, 237
Embryogeny, 211, 436-439
Emerson, R. A., 296, 298, 299, 300, 310, 312, 371,

398
Emerson, S. H., 271, 334-337, 356

Emmel, 49

Emulsifying agent, 35

Emulsion, 3S

Enchylema, 434

End piece, 221, 222

Enderlein, 193, 194

Endocrine secretions, 398

Endomixis, 246

Endoplasm, 39

Endosome, 189, 190

Endosperm, amitosis, 183
cytokineais, 171, 173
development of, 211, 212, 238
effect on embryo, 396
genetics of, 303, 355
plasmodesms, 17, 18
storage, 95, 96, 100, 101

Endospore, 180, 181

Engrafted tissue, 403, 404

Enneaploid, 339

Enriques, 277

Enteromorpha (green alga), 279

Entz, 223

Enucleated cells, 58

Enucleated egg fragments, 410, 412

Environment, 47

Enzyme, 28, 38, 89, 96, 235, 236

Ephedra (gymnosperm), 174, 235

Epigenesis. 424

Epilobium (angiosperm), 186, 308, 342, 419

Epithelium, 15, 18, 171, 224

Equational division, 113. 252, 263, 255, 265, 272

Erdmann, 245, 246

Erdtman, 180

Equisetum (pteridophyte), chondriosomes, 86, 91

spermatogenesis, 204, 205

spore coat, 181

stem, 103

syngamy, 233
Ergastic materials, 4, 46, 93
Ergastome, 102
Ergastoplasm, 44, 93
Ergosterol, 27
Erhard, 225
Ericales, 342

Erigeron (angiosperm), 402
von Erlanger, 169
Erlanson, 267, 365, 397
Ernst, 348, 401, 402, 408
Erysiphe (fungus), 96
Erythroblast, 73
Erythrocyte, 49
Erythroplastid, 49
Escoyez, 169, 201
Euastrum (green alga), 63
Euchromocenters, 56, 57

Euchlcena (angiosperm), 341, 342, 351, 360, 407
Euchlcena-Zea hybrids, 371
Eudorina (green alga), 22, 67, 68, 190, 198
Euglena (flagellate), 66, 67
Eupatorium (angiosperm), 402
Euploidy, 339, 340
Euplotes (protozoan), 19, 42, 49, 277
Euschistus (bug), 75, 86, 214, 219, 346
Evans, 379
Evolution, 441
Exine, 180, 181, 208
Exospore, 180, 181
Eyespot, 44, 66
Eyster, 61, 310, 416

Fi and Fi, 287

Factor (see also Gene), 287, 290

Factorial theory, 308-312

of sex, 397
Fairbrother, 186
Fairchild, 436

False hybrids, 405, 406, 411
Fankhauser, 154
Farmer, achromatic figure, 151

apogamy, 404

chromosomes and species, 126

meiosis, 283, 440

nucleolus, 58

parthenogenesis, 402, 403
Farnham, 124, 343, 352, 354
Farr, C. H., 167
Farr, W. K., 167, 178
Fats, 27, 88, 102
Fatuoid oats, 276
Faull, 158, 159, 230, 281
Faur6-Fremiet. 30, 51, 82. 84, 86, 93. 195

INDEX

543

Faussek, 51

Federley, 360, 369

Fein, 57

Fels, 57

Ferdinandsen, 416

Ferguson, A. J., 188

Ferguson, M., 206, 235, 239, 342

Fernandas, 342

Fertilization (see also Syngamy), animal, 239-249

cone, 240, 241

historical, 436-439

membrane, 241, 247

physiology of, 247

plants, 226-239
Fertilizin, 248
Fetter, 32
Feulgen, 52

Feulgen reaction, 52, 120, 192
Fiber-attachment point (see Spindle-attachment

region)
Fibrillar theory of protoplasm, 434
Ficus (rubber plant), 103
Fikry, 120
Fila, 82

Filament sheath, 219
Findlay, 82
Finn, 210, 236
Fischer, A., 55, 192
Fischer, E., 382
Fischer, M., 37
Fish, 378, 381, 393
Fisk, 123
Fission, 189

Fitting, 31, 67, 180, 181, 196
Fitzpatrick, 196, 226, 230, 283
Fixation, achromatic figure, 151, 152

of cell, 5, 7

cell-plate, 171

chromosomes, 114, 115, 139, 140, 142

Golgi material, 73

nucleus, 54

plastids, 69

and chondriosomes, 91
and Golgi material, 79-81

protoplasm, 37
Flagellates, 189, 190, 191, 223
Flagellum, 43, 44, 189, 223
Flavon and flavonol pigments, 97
Flax fibers, 176
Fleischer, 386
Flemming, amitosis, 184

cell-division, 439

chondriosomes, 82

chromosome division, 440

chromosomes in man, 379

meiosis, 250

net knots, 56

nucleolus, 58

nucleus, by division only, 432
in heredity, 441

protoplasm, 434
Floridean starch, 62, 65, 100
Florin, 283
Fluorescence, 68, 91
Focke, 406

Fceniculum (angiosperm), 103

Fol, 160, 438-441

Fold-back, 276

Fontana, 432

Forenbacher, 85, 90

Fortuin, 112

Fossil pollen, 180

Fowl, 381, 393

Foyn, 190, 279

Fragaria (angiosperm), 367, 391, 406

Fragmentation of chromosomes, 188, 314-326, 349

Francini, 402, 405

Frandsen, 367

Frank, 188

Franze, 66, 67

Fraser, 158, 230, 281

Free, 41

Free cell-formation, 173, 174, 201, 430

Fr6my, 176

Freundlich, 31, 33

Frew, 164

Frey, 178, 230

Friedrichs, 69, 85, 90

Fries, W., 413

Friesner, 112, 342

Fritillaria (angiosperm), 237, 238, 267

Fritsch, 278

Frog, 23, 169, 239, 242, 410, 438

Frolowa, 129, 344, 378

Frommann, 434

Frost, 193, 320, 343, 356

Fry, 155

Fucoxanthin, 64

Fucus (brown alga), achromatic figure, 139

egg, 36

eyespot, 66

gametes, 196, 199

meiosis, 280

parthenogenesis, 247, 402

syngamy, 227, 437
Fujimoto, 415
Fukuda, 186
Fukushima, 346, 356
Fuligo (slime mold), 26, 28, 165
Fulton, 64

Funaria (moss), 65, 233, 307, 343, 371. 418
Fundulus (fish), 136
Fungi, cell wall, 177

gametogenesis, 199

meiosis, 281-283

mitosis, 156-158

sex, 386-388

sporogenesis, 199

syngamy, 229-232
Furrowing (cytokinesis), 109, 166

Gdbor, 188

Gartner, 436

Gagea (angiosperm), 186, 273, 347

Gager, 188, 196, 311

Gaines, 356, 366

Gairdner, 329, 351

544

INTRODUCTION TO CYTOLOGY

Gaiser, 103, 121

GaJactinia (fungus), 281

Galan, 393

Galanthus (angiosperm), 133, 209, 210

Galeopsis (angiosperm), 372

Gallardo, 160

Galls, 186

Galtonin (angiosperm), 117-119, 133, 139

Gametangia, 229

Gametes, 226, 227, 287

Gametic meiosis, 279

Gametic number, 122

Gametogenesis, 196-223

Gametophyte, 122, 208, 211, 251, 306-308, 343,

382-386, 401 ff.
Gamophase, 122
Ganglion cell, 73
Garber, 233
Gardiner, M., 58
Gardiner, W., 16, 18, 19, 98
Gardner, 192
Gargeanne, 102
Gamier, 93

Gasteria (angiosperm), 129, 130, 139, 260, 264, 265
Gastrodia (orchid), 402
Gatenby, 74, 78, 79, 88, 215, 218, 220
Gates, catenation, 332

chromosomes and taxonomy, 126, 334
cytokinesis, 167, 168
heredity, 286

heteroploidy, 339, 345, 347, 348
monoploid sporophyte, 356
mutation, 311
nuclear membrane, 136
nucleoplasmic ratio, 52
plastids, 61
translocation, 337
<5auba, 176
Gaudissart, 87

Gaumann, 196, 226, 231, 283
Gay, 144, 311
Geerts, 334, 346
Gegenbaur, 438
Geitler, 68, 190, 228, 280, 386
Gel, 34

Gelatin, 34, 182
Gelei, 258, 271, 274
Gellhorn, 40
Gemini, 252
Gene string, 144
Gene theory, 144 #., 308-312
Generative cell, 208, 209
Generative nucleus, 209
Genes, 144, 287, 290
in chromonema, 144
in crosses, 287, 290
in development, 273, 398
mutations, 310
nature of, 311, 312
role in origin of species, 373
Genetic continuity, 439
Genie balance, 309, 394
Genom, 121, 325, 340, 419
Genomeres, 416
Genotype, 290

Gentiana (angiosperm), 168
Geotriton (salamander), 87, 220
Geranium (angiosperm), 308
Gerassimow, 50, 58
Gerhard, 334
Germ cell, 213, 441, 444
Germ-plasm, 441, 442, 444
Germ pore, 180, 208
Germ-track, 443
Germinal selection, 444
Germinal vesicle, 213
Gerould, 426
Gerris (insect), 216, 220
Gershoy, 342
Ghimpu, 164, 342
Giard, 438
Gibbs, 176
Gibson, 396
Gicklhorn, 6, 53
Giglio-Tos, 243
Gill cells, 225
Gilson, 176

Ginkgo (gymnosperm), 71, 207, 234
Girdle wall, 166
Giroud, 82, 84
Gland cell, 75, 84, 154, 183
Glaser, 249
Gleisberg, 176
Globoid, 101
Globulin, 101

Gloeocapsa (blue-green alga), 192
Glaeotrtchia (blue-green alga), 192
Glucose residue units, 178, 179
Glucoside, 96
Glutamin, 96
Glutathione, 89
Glycine (angiosperm), 164, 415
Glycogen, 27, 62, 100, 193
Goblet cell, 76, 78
Godetia (angiosperm), 329
Godlewski, 15, 412
Goebel, 236

Goldschmidt, chromidia, 194
gynandromorph, 381
Mendelism, 286
parthenogenesis, 410
sex-determination, 382, 394, 397, 398
temperature and mutation, 311
Goldsmith, 441
Goldstein, 50, 51
Golgi, 73

Golgi material, 3, 73-81
fixation, 73
remnant, 220
role in secretion, 75-78
in spermiogenesis, 214-217, 219
zone, 77
Gones, 251

Gonium (green alga), 22, 67
Gonomery, 235, 243
Gonotokont, 251
Goodspeed, 187, 188, 273, 311, 320, 345, 356, 365,

367
Goodwin, 334, 337, 356
Gordon. 381, 393

INDEX

545

Goroschankin, 16, 206

Gortner, 25, 27-29, 33, 41, 64, 93, 97, 176

Gossipium (angiosperm), 342

Gowen, 144, 295, 310, 311, 394

Grafe, 25, 52, 176

Grafting, 17, 186, 344

Graham, 233

Gramineae, 121

Granata, 268

Granular theory of protoplasm, 434

Grasshopper, 86, 114, 126, 130, 136, 139, 141,

220, 254, 256, 258, 265, 304, 320, 329, 410
Grave, 67, 224, 225
Gray, cell form, 9

cleavage, 170

colloids, 33

fertilization, 247

flagella, cilia, 43, 223, 225

nucleolus, 57

plasma membrane, 40, 41
Greenwood, 378
Gr^goire, chromocenters, 57

chromomeres, 142

chromosomes, 136, 140

meiosis, 256, 266

nuclear reticulum, 55, 56
Gregory, 277, 351, 357, 415, 416
Grew, 423

Griffithsia (red alga), 280
Gris, 101

Gross, 53, 279, 343, 411
Grosser, 379
Growth, 7

Growth period in oocyte, 147, 213, 261
Gruber, 51
Grunberg, 397

Gryllotalpa (mole cricket), 86, 87
Guignard, 66, 199, 204, 210, 236, 437, 440
Guilliermond, ascomycetes, 158

canaliculi, 79

chondriosomes, 80, 82-85, 83, 89, 91, 102

Cyanophycece, 192

elaioplast, 66

elements of protoplast, 104

meiosis, 282

nucleolus, 57

plastids, 69, 71, 80, 90

reticulum, 54

syngamy, 226, 230

vacuole, 93, 96, 101
Guinea pig, 220, 222, 376
Gulick, 376
Gums, 97, 100
Gurchot, 169
Gurwitsch, 87, 188, 436
Gutherz, 379
Gutstein, 52
Guttenberg, 188
Guy6not, 295
Guyer, 19, 379, 3S1, 445
Gwynne-Vaughan, 158, 230, 281, 387
Gymnadenia (angiosperm), 256
Gymnasperms, 206, 234
Gynandromorph, 344, 381, 382

Gynogenesis, 406, 411
Gynospore, 206

H

Haas, 64, 93

Haase-Bessell, 120, 361, 363
Haberlandt, apogamy, 404

apomixis, 409

nucleus, 50, 58

parthenogenesis, 402

plasmodesms, 16

plastid, 61

syngamy, 236

wounds, 19
Hnhrobracon (insect), 382, 395
Haeckel, 285, 441
Haecker, 146, 185, 243, 440
Hcemanthus (angiosperm), 133, 135
Haemoglobin, 30
Hamatococcus (green alga), 44
Hagedoorn, 311
Hagerup, 342
Hagiwara, 296
Hair, 179

HSkansson, 329, 334, 335, 341-343, 352
Haldane, 351, 352, 355
Hall, 66, 73, 74, 81, 189. 190, 223
Hamm, 437
Hammarlund, 329
Hammarsten, 25-27
Hance, 320, 381
Hand, 28

Hanna, 230-232, 386
Hannig, 181
Hanson, 187, 188, 311
Hansteen-Cranner, 52, 177
Hanstein, 2, 45, 46, 93, 433
Haplodiplonts, 356

Haploid (see also Monoploid), 122, 339, 410
Haplont, 278, 306
Haplosis, 250, 263, 440
Harder, 196, 387, 419
Hardy, 52, 55
Harlow, 176
Harman, 123
Harms, 213
Harnisch, 121
Harper, algae, 193, 414

cell constitution, 4

centrosome, 158

cleavage furrow, 165

meiosis, 282

mitosis, 158, 190

plastids, 66, 72, 90

protoplasm, 31

syngamy, 230
Harrison, J. W. H., 347, 365, 367, 413
Harrison, R. G., 6
Harrison, W., 99
Hartig, 101
Hartmann, A., 187
Hartmann, M., apomixis, 401

heredity, 286

546

INTRODUCTION TO CYTOLOGY

Hartmann, M., karyosome, 189
raeiosis in algse, 279
mitosis, 190

motile apparatus, 198, 223, 224
on Protista, 376
pyrenoid, 68

sex in lower plants, 226, 387
syngamy in Protozoa, 245
Hartmann, O., 61
Hartog, 160
Harvey, E. N., 188
Harvey, L., 88, 121, 425
Hatschek, 33

Haupt, 191, 192, 201, 233, 280
Haustoria, 206, 207
Haworthia (angiosperm), 129, 130
Hayes, 355
Hazen, 68

Headed chromosome, 116
Heartwood, 177
Heberer, 136

Hedayetullah, 133, 137, 334
Hegler, 192
Hegner, 51, 213

Heidenhain, achromatic figure, 153
animal cells, 13
cell theory, 20
chondriosomes, 87
cilia, 43, 223
connective tissue, 16
intercellular substance, 182
living cells, 3
metaplasm, 45
mitosis, mechanism, 160
nuclear structure, 55
organismal theory, 24, 436
protoplasmic structure, 46
Heidinger, 197
Heilborn, 126, 341
Heilbronn, 31

Heilbrunn, 25, 31, 32, 40, 164, 170, 188, 242, 248
Heimans, 125, 210. 236

Heitz, chromosome morphology, 116, 118, 129
function of nucleus, 58
heteroploidy, 342, 343, 395
heteropyknosis, 146, 386
meiosis, 283
nucleolus, 57, 120, 121
plastids, 69

sex-chromosomes, 384, 386, 390
Heitzmann, 436
HdU (snail) , 80, 272
Hellebores;, 128
Helleborus (angiosperm), 86
Helvdla (fungus), 281
Helvestine, 184, 225
Helwig, 115, 320, 329
Hemerocallis (angiosperm), 209, 210, 354
Hemicellulose, 100, 176
Henckel, 65, 100
Henderson, 28
Henking, 376, 411, 440
Henle, 431
Henneguy, 225
Heptaploid, 339

Herbst, 441
Heredity, algae, 306

cytology and, 284 #., 441
defined, 285
fungi, 387
heteroploids, 350 ff.
Mendelian, 284 /.
nucleus in, 285
physical basis of, 286 ff.
Weismann's theory of, 441
Bering, 20
Herla, 146
Herlant, 247, 248
Hermann, 160, 397
Herrick, 222

Hertwig, G., 245, 410, 412
Hertwig, O., heredity, 444
meiosis, 263

nucleus in heredity, 285, 439, 441
organismal theory, 436
parthenogenesis, 411, 412
syngamy, 438
Hertwig, P., 401, 410, 412
Hertwig, R., 51, 58, 194, 277
van Herwerden, 27, 51, 194, 195, 220
Herzfeld, 206, 234
Herzog, 178, 179

Heterobrachial chromosomes, 116
Heteromorphio pairs of chromosomes, 265, 271,

303, 388
Heteronema (flagellate), 190
Heterophytic angiosperms, 388
Heteroploidy, 339 ff.

and sex, 394
Heteropyknosis, 56, 146, 386
Heterospory, 206
Heterothallism, 232, 387
Heterotypic mitosis, 250
Heterozygous, 290
Heuser, 440
Hexaploidy, 339
Hexose, 27, 30
Heys, 188, 213, 311
Hibbard, 78
Hick, 16
Hicks, 341

Hicoria (angiosperm), 238
Hieracium (angiosperm), 346, 347, 364, 405, 406,

407, 415
Higgins, 190, 279, 280
Hill, H. E., 298, 354
Hill, S. E., 342
Hill, T. G., 14, 16, 64, 93
Hiller, 29
Hilum, 98
Hiras6, 207, 234
Hirata, 346

Hirschler, 78, 194, 195, 215
Histon, 27

History of cytology, 422-447
Hoar, 329
Hober, 40
Hobson, 242
Hoefer, 196
Hoeppener, 337

INDEX

547

Hof. 12

Hoffman, 342

Hofler, 39

Hofmeister, 23, 430-439, 431

Hogben, 272, 411

Holden, 282

Hollaender, 188

Hollingshead, 124, 128, 343, 356, 357, 361, 367,

372
Holman, 196

Holmgren, I., 348, 402, 408
Holt, 344

Homarus (lobster), 222
Hom&, 98

Homoeotypic mitosis, 250
Homology of chromosomes, 252, 272
Homoploid, 339
Homospory, 206
Homozygous, 290
Hooke, 2, 423
Hoppe, 163, 410
Hoppe-Seyler, 26
Hopwood, 187, 317
Hormones, 19
Home, 190
Horning, 85, 89, 90
Horse, 376
Hosono, 121

Hosta (angiosperm), 139, 416, 417
Hoven, 87, 88
Howard, 51, 97, 187
Huates, 133

Huettner, 24, 155, 243, 295, 382
Hughes-Schrader, 410
Humaria (fungus), 281
Hume, 16

Humulus (angiosperm), 390, 396, 402, 415
Hurst, 340, 364, 365
Huskins, 133, 139, 258, 261, 267, 275, 341, 343,

366, 367
Hutchinson, 235
Huth, 163
Huxley, J. S., 22
Huxley, T. H., 45, 249, 435
Hyacinthus (angiosperm), aberrant mitosis, 186

achromatic figure, 150

cell-plate, 171

chondriosomes, 91

heteroploidy, 345

meiosis, 258, 267, 274, 304
in heteroploids, 351-354

plastids, 62
Hyaloplasm, 31, 32
Hyalotheca (green alga), 63
Hybridization, 361 ff., 408
Hybrids, 287, 348, 359-374

amphidiploid, 367-371

false, 405, 406, 411

permanent, 338

structural, 336

twin, 338
Hydatina (rotifer), 399
Hydnobolites (fungus), 281
Hydnotrya (ascomycete), 181
Hydra (coelenterate), 9. 213

Hydrodictyon (green alga), 63, 165, 414
Hydrogen-ion concentration, 5, 29, 84, 91, 97, 139
Hyperdiploidy, 322, 323
Hypericum (angiosperm), 329, 416
Hyperploidy, 339
Hypoploidy, 339

Icerya (insect), 410

Ichijima, 367

Ichikawa, 187

Id, 442

Idiochromatin, 194

Idiogram, 128

Idioplasm, 441

Idiosome, 216, 219

Ikari, 68

Ikeda, 78

Ikeno, 201, 202, 207, 208, 234

Illick, 334

Imai, 296

Impatiens (angiosperm), 117

Inactivation, 188, 317

Inariyama, 139

Independence of factor pairs, 290

Individuality, of chromosome, 145 ff.

of plastid, 70 ff.

of vacuole, 94 ff.
Ingvar, 20
Inheritance, 284 ff.
Insectivorous plants, 98
Insertion of spindle fibers, 116 ff.
Intercellular substance, 4, 182
Interkinesis, 263, 264
Interlocked tetrads, 271
Interphase, 109, 134
Intersex, 394, 398
Intine, 180, 208
Intussusception, 178
Inulin, 103
Inversion of chromosomes, 188, 276, 315, 318,

319, 320
Ipomcea (angiosperm), ISO
Iriki, 378

Iris (angiosperm), 79, 133, 171, 173
Irvine, 178

Ishikawa, 68, 210, 236, 347
Isobrachial chromosomes, 116
Isoelectric point, 29
Isogamy, 227
Isogenomatic, 340
Isomerism, 30
Ives, 311

Jackson, 231, 283
Jacobs, 40, 73, 77
Jacobsson-Stiasny, 239
Jahn, 66, 190, 278
Jakushkina, 342
Jameson, 277
Jancke, 178, 179
Janet. 278

548

INTRODUCTION TO CYTOLOGY

Janssen, 423

Janssens, cell-plate, 169

chiasmatypy, 266, 270

chromosomes, 132, 141

meiosis, 258, 272

recombination, 302, 304
Jansson, 186
Janus green, 84, 89, 90
Jaretsky, 88, 111, 342, 343, 357
Jasswoin, 77
Jeffrey, 103, 348
Jelly, 34
Jenkins, 366

Jennings, 47, 191, 245, 246. 277, 312
Johansen, 342
Johanssen, 286
Johnson, D. S., 212
Johnson, H. H., 155, 215, 218, 220
Johnson, L. N., 66
Jollos, 311

Jones, D. F., 286, 293, 398
Jones, S. G., 230
Jonsson, 16
Jordan, 225

J0rgensen, C, 186, 344, 356, 367, 406
Jorgensen, I., 64

Jorgensen, M., 57, 58, 156, 194, 195
Joyet-Lavergne, 89, 398
Juel, 282, 402

Juglans (walnut, butternut), 101
Jungers, 16, 17, 161, 171, 173
J uniperus (juniper), 235
Jiissen, 405

Just, 169, 188, 239, 242, 243, 247, 249, 347
Juul, 187

K

Kabsch, 100, 176

Kachidze, 129

Kagawa, 129, 342, 346, 366, 367

Kahle, 411

Kangaroo, 139

Karling, 279

Karpechenko, 273, 342, 364, 367, 368, 370, 371

Karper, 415

Karpova, 74

Karsten, 112, 196, 228, 279, 280

Kartaschowa, 129

Karyogamy, 231

Karyokinesis, 105 ff., 439

Karyolymph, 2, 53, 135, 136, 149

Karyolysis, 187

Karyomeres, 136, 146

Karyoplasm, 2

Karyoplasmic ratio, 51

Karyosome, 56, 164, 189, 190, 223

Karyotin, 2, 55

Karyotype, 126

Kassmann, 69, 85, 90

Katayama, 366

Kater, 68, 78, 88, 183, 190, 223

Katsuki, 382

Kauffmann, H.. 279

Kaufmann, B. P., 133, 136, 137, 139, 140, 256

Kawakami, 121
Keene, 229
Keimbahn, 443
Kellicott, 112
Kellogg, 46, 441
Kemp, 185, 187, 379
Kempton, 407
Kendall, 186
Keratin, 177, 182
Kerr, 29
Keuten, 189
Kidney, 77
Kienitz-Gerloff, 16
Kiernan, 289
Kiesel, 25, 26
Kieser, 426
Kihara, asynapsis, 273

chromosome complement, 121, 129

grains, 366

heteroploidy, 340, 342, 395

human chromosomes, 379

(Enothera. 334

sex-chromosomes, 388, 390, 391, 395
Kildahl, 235
Kindred, 225
Kinetic bodies, 116, 117
Kinetic constriction, 116
Kinetochore, 116
Kinetonucleus, 224
Kinetosomes, 203
King, R. L., 78, 115, 378
King, S. D., 73, 78
Kingery, 84
Kingsbury, 82, 88
Kinney, 58
Kinoplasm, 44, 165
Kinoplasmic plates, 203
Kirby, 90
Kirchensteins, 193
Kisliak-Statkewitsch, 188
Kisser, 53, 184
Kite, 6, 39, 52-54
Kiyohara, 69, 80
Klebahn, 227, 228, 280
Klebs, 58, 66, 165, 386
Klein, 159, 434
Klingstedt, 53

Kniep, 230-232, 281, 282, 386, 387
Knight, 278, 280
Knob on chromosome, 119, 123, 143, 271, 298,

303, 318, 332
Koch, 58
Koelreuter, 436
Koerperich, 136, 140, 149, 164
Kofoid. 10, 183, 190, 191, 195, 223, 245
Kohl, 16, 192
Kojima, 112
Kolatchev, 74
von Kolliker, 431, 438, 441
Koltzoff, 221, 222
Komuro, 187
Kondo, 415
Konopacki, 88, 164
Koos, 186, 344, 356
Kopsch, 73. 74

INDEX

549

Kornhauser, 266, 441

Korotneff, 86

Korschelt, 51

Koshuchow, 186

Kossel, 26, 30, 58

Kostanecki, 240, 411

Kostoff, 186. 407

Kostrioukoff, 210

Kowalevsky, 440

Kowalski, 14

Koyama, 385

Krabbe, 177

Kramer, 100

Kranzlin, 190, 278

Kretschmer, 190, 193

Kropp, 89

Kruch, 437

Kruger, 412

Krupko, 90

Kuckuck, 63

Kuczynski, 224

Kuhla, 16

Kuhn, A., 411

Kuhn, E., 56, 57, 118, 340, 343, 391, 406

Kulkarni, 334, 356

Kulp, 30

Kunieda, 280

Kupelwieser, 412

Kupper, 419

Kurssanow, 72, 279

Kusano, 402

Kiister, 6, 53, 62, 66, 98, 415

Kuwada, chromomeres, 142

chromonemata, 139, 140

chromosome arrangement, 125

hybrids, 360

nucleolus, 57

restitution nucleus, 340

spermatogenesis, 207

syngamy, 234, 236

Zea chromosomes, 123
Kylin, apomixis, 402

eyespot, 66

Floridean starch, 65, 100

gametes, 199

meiosis, 278, 280

Laboulbenia (fungus), 281

Laburu, 79

Lachnea (fungus), 281

Lagging chromosomes, 345, 355, 361-363, 364

Laguesse, 87

Laibach, 57

Lamarck, 426

Lammerts, 367, 407 .

Lampe, 99, 100

Lampsilis (mollusk), 224, 225

Lams, 244

Lancefield, 296, 378

Land, 174, 210, 235

Landis, 49

Lang, 405

Langlet, 129, 340, 342, 343, 346

Larix (conifer), 86, 151, 162, 171, 236

Larval characters, 419

Lastrwa (fern), 403, 405

Latex, 97

Lathyrus (angiosperm) , 308

Latter, 58

Laughlin, 111

Lauterborn, 228

La Valette St. George, 438

Lawrence, 351, 355

Lawson, 206, 234, 235

Lawton, 405

League, 295

Lebedeff, 368

Lebistes (fish), 378, 381, 393

Lecanium (insect), 411

Lecithin, 27

Lee, A. B., 73, 251

Lee, B., 176

Lee, S., 192

Leeman, 102

van Leeuwenhoek, 424, 437

LeguminossB, 121, 129

Lehfeldt, 230

Lehmann, 334, 338, 419

Leighty, 367

Leliveld, 334

Lenhoss6k, 14, 225

Lenoir, 58, 256

Lenzites (fungus), 388

Lepeschkin, 26, 33, 40

Lepidosiren (fish), 272

Lepisma (nematode), 220

Leptolegnia (fungus), 200

Leptonema (brown alga), 63

Leptonema, 256, 257

Lesley, J. W., 320

Lesley, M. M., 274, 320, 343, 346, 352, 356

Lethal factors, 293, 336, 338

Leucoplast, 62, 64, 65, 69, 90

Levan, 124, 267

Levi, 87

Levine, 187, 188, 282

Lewis, C. E., 201

Lewis, G. N., 311

Lewis, I. F., 280

Lewis, M. R., 187

Lewis, M. and W., achromatic figure, 161

chondriosomes, 84, 85, 87

neurofibrils, 13

nuclear fragmentation, 184

nucleus, 53

tissue cultures, 6, 111
Lewitsky, amphidiploidy, 367

chondriosomes, 82, 84, 86, 90

chromosomes, 114-116, 121, 124
and taxonomy, 126, 128, 129

irradiation, 187

plastids, 69, 71, 90

translocation, 321
Leydig, 434

Libocedrus (conifer), 235
Life cycles, 383
Ligniera (myxomycete), 190
Lignin, 100, 176

550

INTRODUCTION TO CYTOLOGY

Liliacesp, 342
Lilienfeld, 26, 366
Lilium (lily), canaliculi, 79
chondriosomes, 71, 83
chromonema, 139, 142
homoploidy, 342
megaspore nuclei, 212
meiosis, 256, 258, 267
nucleus, 50

syngamy, 236, 237, 238
Lillie, F. R., fertilization, 239, 240, 242, 247-249,
438
sex-determination, 397, 308
spermatozoon, 222
Lillie, R. S., activation of egg, 247, 248
chromosome arrangement, 125
differentiation, 11
electrical phenomena, 52, 160
oxidation, 59
plasma membrane, 40
polarity, 20

protoplasmic structure, 31, 37, 38
specificity of protoplasm, 30
Limosphere, 71, 81, 202-204
Limosphere remnant, 203, 204
Lind, 279

Lindegren, 194, 282, 387
Lindenbein, 279
Lindfors, 282
Lindsay, 388
Lindstrom, 186, 344, 356
Linin, 65

Link, G. K. K., 415
Link, H. F., 426
Linkage, 293-296, 298-306
groups, 296
map, 299, 301
Linmn (angiosperm), 419
Lipide, 140
Lipide theory, 40

de Litardiere, alveolation theory, 140
chromomeres, 142
heteroploidy, 343, 346
matrix, 136
mitosis, 138
nucleolus, 68
reticulum, 54, 55
Liu, 74
Liver, 77, 88
Liverworts, 382
Lizard, 376
Ljungdahl, 347, 363

Lloyd, 41, 43-45, 63, 64, 68, 103, 192, 228
Lockwood, 187
Locy, 439

Loeb, J., 59, 247, 441
Loeb, L., 6
Loefer, 190
Logan, 436
Lohnis, 90, 193

Longley, 100, 123, 308, 341, 358, 360, 407
Loos, 188
Lophius (fish), 16
Lorbeer, 283, 382, 384, 395
Lotsy. 251, 335

Loui, 90, 91

Lowe, 63

Lowschin, 84, 85, 90

Loyez, 88

Lubimenko, 64

Lubosch, 58

Lucas, 139, 223, 225

Ludford, 57, 58, 74, 77, 187

Ludtke, 101

Lund, 20

Lundegirdh, chondriosomes, 82, 90

chromomeres, 142

chromosomes, 140

cilia, 43, 223

colloids, 33

karyotin, 55

plasma membrane, 40

plasmodesms, 16

protoplasm, 25, 31

reticulum, 54, 55

vacuoles, 93
Lupinus (angiosperm), 71
Luther, 222
Lutkov, 361
Lutman, 166, 231
Lutz, 320, 334, 339, 346
Lychnis (angiosperm), 390, 392
Lycogala (myxomycete), 26
Lycopersicum (angiosperm), 186, 274, 343, 346,

356
Lycopodium (pteridophyte), 204
Lygodium (fern), 229, 233
Lynch, 58, 59

Lyngbya (blue-green alga), 192
Lynn, 398
Lyon, 31, 180, 181
Lyophilic, 34
Lyophobic, 34

M

Ma, R., 69

Ma, W., 74

Macallum, 58

MacArthur, 310

MacDaniels, 12, 175

MacDougal, 27

MacDougall, 49, 277

Macfarlane, 18

MacGillivray, 100, 293, 308

Mackel, 402

Macormick, 229

Macronucleus, 10, 49, 194, 245, 246

Macrosomes, 32

Mactra (mollusk), 411

Madge, 210, 236

Maeda, 124, 139, 207, 267, 270

Magistris, 52

Magnets, 125

Magnolia (angiosperm), 168

Magrou, 188

Maige, 51

Maire, 158, 281, 282

Maize (see Zea)

Makino, 121

INDEX

551

Male cells and nuclei, 208, 209, 210, 234, 235-237

Malone, 376
Malpighi, 423, 424
Malsen, 399
Malte, 55
Mameli, 177
Mammals, 376, 378
Man, centrosome, 154

chromosomes, 379

colorblindness, 392
Mangelsdorf, 293
Mangenot, canaliculi, 79

chondriosomes, 82, 83, 90, 91

eyespot, 66

Floridean starch, 100

nucleolus, 57

oil, 102

plasmodesms, 16

plastids, 65

vacuoles, 97, 98
Mangin, 176
Mann, 71, 124, 356, 363
Manoilov, 398
Mantidffi, 378
Mantle of cytoplasm, 235
Manton, 342, 405
Marchal, 386, 405
Marchand, 15

Marchantia (liverwort), 201, 202, 427
Marcus, 51, 194
Mar^chal, 142, 256, 266
Margolena, 52
Mark, E. L., 87, 410, 438
Mark, H., 178
Marsden-Jones, 367
Marshak, 124
Marsilia (water fern), apomixis, 402, 403, 407

spermatogenesis, 205

spermatozoid, 199

spore coat, 181
Marsupials, 378
Martens, cell-plate, 171

chromonema, 139

chromosomes, 119

fixation, 7, 54

matrix, 136

micromanipulation, 6

nucleolus, 58

somatic mitosis, 111

spindle, 161, 163
Martins-Mano, 55, 142
Marwick, 178
Maschka, 101
Masdevallia (orchid), 18
Mason, 129
Massee, 16
Mast, 43, 67
Masui, 376

Maternal inheritance, 415 ff.
Mather, 436
Mathews, A. C, 200
Mathews, A. H., 20, 25, 243
Mathias, 280

Matrix, 106, 119, 133, 134-137, 140, 143, 144, 260
Matsumoto, 13

Matsuura, 286

Matthiola (angiosperm), 267, 320, 343, 356

Maturation divisions, 214, 239, 250

Maupas, 245

Maurer, 17

Mavor, 187, 302, 393

May, 89

Mayer, 89

Mayer, Rathery, and Schaeffer, 89

Maziarski, 58

McAllister, 68, 166, 212

McClendon, 169

McClintock, anastomoses, 120, 135

asynapsis, 273

chromosome matrix, 120

chromosome morphology, 115, 118, 119, 123,
298

crossing-over, 303, 305, 337

deletion, 318, 319

fragmentation, 317

heteroploidy, 343, 346, 347

inversion, 318, 319

linkage groups, 298

meiosis, 259, 261, 265, 270, 302

non-homologous association, 276

nucleolus, US, 119, 120

reciprocal translocation, 329, 330, 332, 333

synapsis, 274

triploidy, 352, 353, 354
McClung, chiasma, 268

chromosome individuality, 115, 141

chromosomes and taxonomy, 123, 126, 129,
130, 342

linkage and chromosomes, 297

meiosis, 256, 265

reticulum, 55

sex-chromosomes, 376
McCubbin, 230
McDonald, 10, 223
McKay, 240
McPhee, 397
Mead, 154

Mecostethus (insect), 129, 258, 265, 342
Meek, 126

Megaspore, 180, 206, 210, 211
Megasporocyte, 210
Mehta, 58
Meiocyte, 251, 282
Meiosis, 250-283

alga?, 278

and apomixis, 407

gametic, 279

historical, 440

in hybrids, 360 ff.

in living cells, 256

and Mendelian segregation, 291-293

in monoploid sporophyte, 356

outline of, 252, 253

in plant groups, 278 ff.

in polyploids, 350 ff.

in Protozoa, 277

summarized, 255

theory of, 275
Melandrium (angiosperm), 236, 388, 389, 390,
392, 397, 415

552

INTRODUCTION TO CYTOLOGY

Melburn, 366

Melilotus (angiosperm), 168
Melin, 283
Mellon, 194
Membranellse, 43
Mendelism, 284-313
in algse, 306

and chromosomes, 284 ff., 445
rediscovery, 445
Menoidium (flagellate), 190, 223
Mercerization, 179
Mercurialis (angiosperm), 388
Meristem, 11, 12, 94, 96
Merogony, 407, 412
Merokinesis, 146

Mesembryanthemum (angiosperm), 415
Mesoderm, 17
Mesospore, 180
Metabolic gradient, 19

Metabolic nucleus, 105, 106. 134, 136, 147
Metabolic rate, 398
Metabolism and genes, 309

and sex, 398
Metachromatic corpuscles, 101
Metachromatin, 97, 101, 193
Metachrome, 95

Metaphase, 106, 107, 108, 134, 137
Metaplasm, 45 ff., 93
Metapodius (insect), 379
Metaxylem, 175
Metcalf, 191
Metopsilus (insect), 360
Metz, chromosome morphology, 123

chromosomes and species, 129

haploidy, 410

linkage, 296

meiosis, 272, 295

monocentric mitosis, 163

sex-chromosomes, 378

somatic pairing, 126

spermatogenesis, 215
Metzner, 43

Meurman, 329, 335, 341, 366, 389, 390
Meves, centrioles in sperm and oocyte, 166, 217,
218

chondriosomes, 82, 83, 90

chondriosomes and fertilization, 244

differentiation theory, 87

parthenogenesis, 410

spermatozoid, 199

spermatozoon, 222
Meyen, 430
Meyer, A., bacteria, 193

chondriosomes, 82, 85, 88

colloidal state, 33

elements of protoplast, 104

ergastic substances, 30, 93, 94, 96, 101

intercellular substance, 182

nucleolus, 57, 58

pigment, 97

plasmodesms, 16

plastid, 61, 63, 65, 67, 70, 90, 91

protoplasm, 25 ff., 31, 45, 46

starch, 98-100
Meyer, K., 233

Meyer, K. H., 178

Meyers, 100

Miastor (fly), 411

MiceUa;, 33, 99, 162, 177-179

Michaelis, 186, 342, 419

Microcentrum, 153

Micromanipulation, 6, 52, 53, 142, 161, 184, 446

Micromeric theories of protoplasm, 46

Micronucleus, 10, 49, 194, 245, 246

Microscope, 423

Microsome, 92, 178

Microspore, 206, 208, 209

of diatoms, 228
Microspore quartet, 167

Microsporocyte, achromatic figure, 151, 162
cytokinesis, 167
meiosis, 209, 364
Microsporogenesis, 85
Mid-body, 155, 158, 169
Middle lamella, 171, 174
Middle piece, 217, 218, 221, 222, 240
Miescher, 26, 30
Millardet, 406
Miller, 436

Milovidov, 82, 84, 89, 90, 190
Mimosa (angiosperm), 18
Minchin, 43, 44, 189, 223, 277, 278
Minenkov, 398
Minot, 51
Minouchi, 378
Minoura, 397

Mirabilis (angiosperm), 289, 415, 416
Mirande, 82, 103
Mirbel, 426, 427
Mitchell, 178
Mitochondria (see also Chondriosomes), 82

Mitogenetic rays, 188

Mitokinetism, 160

Mitome and paramitome, 434

Mitosis, aberrant, 184-188, 186
duration and periodicity. 111, 112
historical, 439
mechanism of, 159-164
monocentric, 163
premeiotic, 272
in Protozoa, 189
semiheterotypic, 346
somatic, 105-113, 110, 112

Mitosome (Gatenby), 218

Miyake, 57, 199, 200, 201, 207, 235

Mnimn (moss), 405

Mobius, 61, 64, 97

Mockeridge, 192

Modilewski. 212, 407

Moenkhaus, 146

Moffett, 351

von Mohl, 94, 177, 430, 432

Mohr, 188

Moissejewa, 188

de Mol, 186, 187, 342, 345, 357

Moldenhawer, 426

Molge (amphibian), 76

Molisch, 17. 93, 176, 177

Mols, 376

Monkey, 378, 379

INDEX

553

Monoblepharis (fungus), 199, 229
Monocentric mitosis, 163
Monoploid, 121

Monoploid plants, Mendelism, 306
Monoploid sporophytes, 356, 402
Monotropa (angiosperm), 59, 237, 238
Montgomery, chondriosomes, 86

chromosome individuality, 445

meiosis, 266, 272

nucleolus, 57

sex-chromosomes, 376, 379
Moore, A. C, 151, 283
Moore, B., 25
Moore, E. L., 246
Moore, J. A., 116
Moore, J. E. S., 379
Moreau, 85, 90, 165, 229
Morelle, 77, 85
Morgan, C. L., 47
Morgan, L. V., 306, 381
Morgan, T. H., activation, 249

chromosome complement, 344

chromosome set, 123

crossing-over, 266

cytasters, 164, 248

cytoplasmic inheritance, 420

factorial hypothesis, 309

fragmentation, 320

gene theory, 312

genes, 144

lethal factors, 293

hnkage, 294, 296, 301, 392

Mendelism, 286, 373

mutations, 311

parthenogenesis, 410-412

sex-chromosomes, 378, 393

sex determination, 381, 382

syngamy, 243, 245
Morinaga, 342, 356, 365
MorofF, 194
Morphallaxis, 9
Morrill, 376
Morris, 146

MoTus (mulberry), 390, 396
Mosaic endosperm, 239
Moses, 129, 163, 410
Mosses, cytoplasmic inheritance, 418

heredity in, 307

heteroploid, 357

hybrids, 371, 418
Moths, 368, 398
Motile structures, 14
Motte, 69, 70, 90, 196, 201, 283
Mottier, achromatic figure, 159

aleurone, 101

centrosomes, 169

chromomeres, 142

cytokinesis, 173

male cells, 210

meiosis, 262, 280

nucleolus, 57

plastids, 69, 90, 91

sex, 386
Mougeotia (green alga), 68, 190
de Moulin, 13

Mounce, 230

Mouse, 378

Mucilage, 100, 102

Mucor (fungus), 8, 10, 50, 200, 201

Muhldorf, 201, 203

MuUer, H. A. C, 124, 142

Muller, H. J., lethal factors, 293

linkage, 296

mutation, 310, 311

reciprocal translocation, 329

sex-chromosomes, 393, 395

somatic pairing, 123

tetraploid ratios, 352

translocation, 316, 318, 322-325

X-radiation, 187, 302, 311, 316
Muller, O., 228
Mulsow, 376

Multiple allelomorphs, 310
Multivalent chromosomes, 304, 355
Mundie, 190, 197, 279
Muntzing, 340, 343, 372, 396, 407
Murbeck, 402, 404, 405
Murgantia (insect), 219
Murphy, 199
Murray, 74
Murrill, 235

Musa (angiosperm), 345
Muscari (angiosperm), 128
Muscle, 14, 18
Mutation, 188, 310, 338
Myers, 280
Myofibril, 15, 87, 88
Myoneme, 44

Myriatica (angiosperm), 103
Mytilus (mollusk), 225, 412
Myxomycete, chondriosomes, 86

cytokinesis, 165

glycogen, 100

meiosis, 278

mitosis, 190

protoplasm, 26, 32, 39

surface-volume ratio, 8

N

Nachtsheim, 410

Nadson, 186, 187

Nagai, 386

Nagao, 352

von Nageli, cell-division, 430, 431

cell wall, 177

idioplasm theory, 441

importance of protoplasm, 433

starch grain, 99, 100

vacuole, 94
Najas (angiosperm), 117, 124
Nakahara, 58, 183
Nakanishi, 194
Nangia, 74, 78

Narcissus (angiosperm), 133, 139, 352, 354, 357
Nassonow, 76, 77, 90
Nasturtium (angiosperm), 64
Nath, 58, 73, 74, 78, 82, 88, 215
Nathansohn, 166, 185
Naville, 295

554

INTRODUCTION TO CYTOLOGY

Nawaschin, M., amphidiploidy, 367

chromosome morphology, 115, 121, 124, 127,
128

dislocation hypothesis, 347

fragmentation, 320, 349

heteroploidy, 343, 349

hybrids, 301, 372

translocation, 314, 321, 325

X-radiation, 187
Nawaschin, S., chromosome morphology, 114—
119, 128, 446

fertihzation, 236, 238, 437

male nuclei, 210

Sorodiscus, 190
Nebel, 133, 137, 139, 256, 260, 261, 265, 329, 335
Nebenkern, 88, 90, 216, 218, 219
Nebennucleoli, 56
Neck canal cells, 201
Nelumbo (angiosperm), 167
Nemalion (red alga), 280
Nematodes, 376
Nematus (saw-fly), 411
Nfmec, altered chromosomes, 186

chloralized cells, 185

dispermy, 347

mitosis, 191

nucleolus, 57

nucleus, 52, 53, 55

spindle, 161, 164

spore wall, 181
Nephrodium (fern), 86, 233, 403, 404
Nereis (annelid worm), 221, 222, 238, 240,

242-244, 247
Nerve cells, 13, 14, 83
von Neuenstein, 48
Neurofibrils, 13, 87
Neuromotor apparatus, 10, 19
Neurospora (fungus), 282, 387
Neuroterus (gall-fly), 411
Newport, 438
Newton, D., 386
Newton, W. C. F., 258, 267, 268, 274, 346,

351, 352, 355, 367
Nichols, G. E., 206, 235
Nichols, S., 31
Nicholson, 89
Nicolosi-Roncati, 71, 82
Nicotiana (angiosperm), amphidiploidy, 367

androgenesis, 407

chimera, 343

chromosome morphology, 124

cytokinesis, 167

cytoplasmic heredity, 419

digluta, 367

fragmentation, 320

haploidy, 356, 402

non-disjunction, 345

pollen characters, 308

tabacum, 365, 368

temperature effect, 186

X-radiation, 273
Nienburg, 230
Nieschulz, 223
Nigella (angiosperm), 129
Nigritella (angiosperm), 405

Nikolaewa, 342

Nishimura, 199

Nishiyama, 293, 343, 366

Nissl substance, 13

Nitella (stonewort), 97, 279

Nitophyllum (red alga), 280

Nitzschia (diatom), 386

Noack, 69, 90, 417

Nodules of legumes, 90

Noll, 22

NoUer, 224

Non-conjugation, 273

Non-disjunction, 338, 344, 345, 393

Non-division, 345, 346

Non-homologous association of chromosomes,

276, 316
Nonidez, 272

Non-Mendelian inheritance, 415 ff.
Nor6n, 235

Nostoc (blue-green alga), 192
Nothnagel, 153, 236, 237, 238
Nowikoff, 194
Nucellar embryo, 404, 405
Nuclear budding, 183
Nuclear fragmentation, 183
Nuclear membrane, 2, 136
Nuclear reticulum, 63, 105, 134, 136
Nucleic acid, 26, 27, 29
Nuclein, 26, 27
Nucleolo-centrosome, 189
Nucleolus, 2-59 ff., 118-121, 119, 164
Nucleome, 49
Nucleoplasm, 2
Nucleoplasmic ratio, 8, 51
Nucleo-proteins, 26, 140
Nucleus, 48-60

of bacteria, 193, 194

cell constituent, 2

chemical nature, 52

discovery, 427

division, 105 ff.

evolution of, 193

fusion and heteroploidy, 346

in heredity, 285, 441

metabolic or resting stage, 59

migration of, 403, 404

origin by division, 432

oxidation, 59

in Protista, 189 ff.

restitution, 346

size and chromosome number, 51

structure, 53 ff.

synthesis, 58 ff.
NuUiplex, 354
Nurse cells, 213
Nussbaum, 74, 194, 195
Nymphaa (water lily), 83

Oakley, 187, 317

Obersteiner, 14

Ochna (angiosperm), 402, 405

Octoploidy, 339

CEcanthus (cricket), 218

INDEX

555

CEdogonium (green alga), blepharoplast, 198

gametes, 196, 199

meiosis, 279

mitosis, 190

pyrenoids, 63

syngamy, 227, 437

zoospores, 19S
CEhlkers, 279, 334, 337
(Enothera (angiosperm), 334-338

abnormal mitosis, 186

apomixis, 409

cytogenetic composition, 336

fragmentation of chromosomes, 320

gigas mutant, 339

heteroploidy, 339, 343, 346, 347

meiosis, 273, 334

monoploid sporophyte, 356

non-disjunction, 345

parthenogenesis, 402

pollen characters, 210, 308

recombination, 304

Renner complexes, 336, 336

semisterility, 332

structural hybridity, 336

syngamy, 236, 238

tetraploid, 357

triploid, 352, 358

twin hybrids, 338

variegation, 416
Oes, 55
Ogata, 56

Oguma, 121, 378, 379, 381
Ohashi, 190
Oil, 102

body, 102

droplet division, 169
Okabe, 280
Oleosome, 66
Olitsky, 89
Olive, 190, 192, 278
Oliver, 18, 311
Olpidiopsis (fungus), 165
Olson, 187, 311

Oltmanns, 11, 64, 165, 196, 197, 226, 227, 278
One-plane theory of chiasma, 268, 269, 271
One-sided inheritance, 391
Ono, 340, 342, 390, 395
Onoclea (fern), 199, 233
Onslow, 25, 64, 93, 97, 100
Ontogenesis (see Development)
Oocytes or ovocytes, 213, 238
Oogenesis, in animals, 213, 214

in plants, 196, 197, 200, 201, 206, 210, 211
Oogonia or ovogonia, 213
Oogonium (of plants), 197
Oomycetes, 199, 229, 281
Opercularia (infusoria), 277
Ophiocephatus (fish), 78
Opisthacanthus (scorpion), 86
Opossum, 378, 379
Orchidaceffi, 342
Orchis (orchid), 62
Organelle, 10
Organic acids, 96
Organismal theory, 20 ff., 435

Orman, 85

Ornithogalum (angiosperm), 66

Orobanche (angiosperm), 210

Oryza (angiosperm), 308, 350, 415

Osawa, 402, 405

Oscillatoria (blue-green alga), 192

Osmiophilic platelets, 71, 81

Osmosis, 42

Osmunda (fern), 93, 405

Ostenfeld, 402, 408

Osterhout, 40, 59

Ostwald, 33

Otidea (fungus), 281

van Overeem, 358

Overton, E., 16, 40, 66, 440

Overton, J. B., chromocenters, 57

life cycle, 196

meiosis, 256, 266

parthenogenesis, 247, 402

somatic mitosis, 140
Ovule, 210, 211
Ovum, 213
Owens, 80
Oxidase, 220
Oxidation, and chondriosomes, 88, 89

and nucleus, 59

in respiration, 04
Oxychromatin, 54, 55
Oxyria (angiosperm), 405
Oxyrrhis (flagellate), 189, 190, 223
Oxytrichia (inf usorian) , 277
Ozawa, 82

Pace, 212, 236, 402, 407
Pachynema, 267, 268
Packard, 186, 412
Padina (brown alga), 280
Painter, deletion, 317, 318

sex-chromosomes, 376, 378, 379, 393, 395

somatic pairing, 123

translocation, 322, 323, 324

X-radiation, 187
Palla, 58
Palladin, 25, 64

Pallavicinia (liverwort), 283, 440
Palm, 167
Palmer, 64
Paltauf, 6, 53
Palitdina (gastropod), 74
Panceolus (fungus), 230
Pancreas, 77, 88
Pandorina (green alga), 22
Pangenesis hypothesis, 441
Papaver (angiosperm), 308, 347, 363
Pappenheimer, 73

Parachromosomio substance, 136, 149, 164
Paracopidosomopsis (insect), 410
Paradesmose, 189, 223
Paradinium (flagellate), 278
Paragenoplast, 149, 164
Paramitome, 434

Paramoecium (inf usorian), 32, 42, 49, 245, 246
Paramylum, 66

556

INTRODUCTION TO CYTOLOGY

Parasynapsis, 337
Parat, 76-80, 220
ParateUix (grasshopper), 126, 410
Parenchyma, 12
Parker, 13
Parmenter, 410
Parnell, 308
Parthenogamy, 411
Parthenogenesis, in animals, 409
artificial, 247
and heteroploidy, 413
and hybridity, 408
and meiosis, 407
in plants, 401
and sex, 410
Parthenote, 409
Pascher, 89, 192, 277
Pathological tissue, 98, 184
Pathology and genetics, 415
Paton, 235
Patten, 187

Patterson, J. T., 187, 311, 381, 395, 410
Patterson, P. M., 199
Pauli, 187
Paulmier, 376
Pavillard, 228
Payen, 176, 433
Payne, 78, 86, 215, 378
Pea, Mendelism, 287-289, 296
Peacock, 413
Pearson, 382
Pectin, 100, 176
Pediastrum (green alga), 414
Pedicdlina (flatworm), 272
Pediculopsis (insect), 136
Pedicvlus (insect), 272
Pekarek, 187

Pelargonium (angiosperm), 62, 415
PeUew, 329, 331, 367, 419

PeUia (liverwort), chromosome morphology, 129
heteroploidy, 343, 395
heteropyknosis, 146
meiosis, 283

sex-chromosomes, 384, 386, 395
spermatozoid, 203
syngamy, 233
Pencillium (fungus), 96
Pensa, 69, 72, 91
Pentaploidy, 339, 409
Pentose and pentosan, 27, 30, 62
Peperomia (angiosperm), 212, 23T
Peptization, 34

Peranenui (flagellate), 190, 223
Percival, 342, 366
Percnosome, 202

Perforatorium, 78, 216, 220, 240, 241
Periderm, 176
Perinium, 180, 181
Periplasm, 200
Periplasmodium, 181
Periplast, 43
Perisperm, 101
Perispore, 181
Perivitelline space, 242
Permanent hybrid, 338

Permeability, 37, 40

Perroncito, 74

Perry, 133

P^terfi, 6, 242

Peterschilka, 68, 190

Petersen, J. B., 43, 44, 223

Petit, 193

Petrunkewitseh, 410

Petruschewsky, 192

Petunia (angiosperm), 239, 352

Peziza (fungus), 281

Pfeffer, 40, 94, 101, 102, 185

PfeifTer, 29

Pfitzner, 141

pH, 5, 29, 84, 91, 97, 139

Phacus (flagellate), 44

Phffioplast, 102

Phajus (orchid), 66, 238

Phaneroplasm, 33

Pharbitia (angiosperm), 296

Phascum (moss), 405

Phase reversal, 36, 41

Phaseolus (angiosperm), 66, 237

Phases in colloids, 34

Phelps, 58

Phenotype, 290

Philadelphus (angiosperm), 342

Philipp, 186

Phillips, 192

Philp, 267, 286

Phloem fiber, 12

PhoUota (fungus), 419

Phormidium (blue-green alga), 192

Phospholipide, 27, 84

Photosynthesis, 64, 65
Phragrnatobia (moth), 380

Phragmidium (fungus), 231

Phragmites (angiosperm), 357

Phragmoplast, 150, 173

Phrynotettix (grasshopper), 118, 136, 141, 265

Phycocyanin, 64, 192

Phycoerythrin, 64, 192

Phycomyces (fungus), 165, 166, 172, 387

Phycomycetes, 199, 229, 281

Phycophffiin, 64

Phyllocladus (gymnosperm) , 235

Phylloglossttm (pteridophyte), 204

Phyllopneuste (bird), 222

Phylloxera (aphid), 411

Physa (snail), 240

Physcomitrella (moss), 371

Physcomitrium (moss), 307, 418

Physical basis of heredity, 286, 421

Physiological gradient, 19

Physostegia (angiosperm), 174

Phytodecta (beetle), 310, 393

Phytosterol, 103

Picard, 165, 256

Pickett, 178

Piech, 174, 210

Pieris (butterfly), 50

Piersol, 14

Pig, chromosomes, 376

Pigeon, 381

Pigments, 96, 97, 192

INDEX

557

Pilayella (brown alga), 63, 280

Piloholus (fungus), 165

Pilularia (pteridophyte) , 233, 437

Pincus, 378

Pinney, 136, 141, 412

Pinnotheres (crustacean), 222

Pinus (gymnosperm) , 57, 207, 208, 235, 342

Pisciola (leech), 156

Pisum (pea), aleurone, 101

chondriosomes, 83, 90

chromosome complement, 124

hybrids, 360

leucoplast, 62

Mendel's work 287-289, 296

reciprocal translocation, 329, 331

root hairs, 60
Pits, 175

Plantago (angiosperm) , 357
Plantefol, 90

Plasma membrane, 2, 39, 172
Plasma theory, 436
Plasmodermal blepharoplast, 67, 198
Plasmodesms, 16, 17, 22
Plasmodial theory, 436
Plasmodial tissues, 10, 22
Plasmodiophora (myomycete), 190, 278
Plasmodium, 171
Plasmogamy, 231
Plasmolemma, 39
Plasmon, 418, 419
Plasmosome, 2, 57
Plastid, 3, 61-72, 80, 279

and chondriosomes, 90-92

development, 417

and Golgi material, 80, 81

individuality, 70 ff.

origin, 69 ff.

primordia, 69, 70, 101

in syngamy, 233, 234

in zygospore, 279
Plastidome, 61
Plastomere, 199
Plastonema, 70
Plastosome, 70
Platypcecilus (fish), 381, 393
Plethodon (amphibian), 215, 217
Pleurage (fungus), 387
Plough, 295, 302, 311
Plowe, 39, 40, 42
Plumbagdla (angiosperm), 212
Plus and minus strains, 231, 232
Poddubnaja, 210

FodophyUum (angiosperm), 133, 134, 139
Pogonatum (angiosperm), 385
Poirault, 16
Polar bodies. 213, 263
Polar caps, 149, 160
Polar-fusion nucleus, 238
Polar nuclei, 210, 211, 237
Polarity, 20, 75, 180, 185
Polarized light, 84, 98, 99, 178
Pole field, 108
Polianthes (angiosperm), 66
Policard, 84, 91
Politis, 66

Politzer, 187
Poljansky, 192
Pollack, 29
Pollen, characters, 308

grain, 174

tube, 208, 209, 235, 237, 293, 436, 437

wall, 180
Pollination, 237
Pollister, 78, 155, 215, 216, 220
Polocyte, 213
Polyembryony, 382, 405
Polygonum (angiosperm), 342
Polyploidy (see also Heteroploidy) , 125, 130, 339

in animals, 396

and apomixis, 408

in gametophyte, 343, 357, 395

and heredity, 350 ff.

and meiosis, 274

and size, 356, 357
Polypodium (fern), 138
Polysiphonia (red alga), centrospheres, 169

furrowing, 165

gametes, 196, 197

meiosis, 280

sex, 386

syngamy, 227, 229

zoospores, 198
Polyspory, 361, 362
Polystichuni (fern), 404, 405
Polytoma (green alga), 62, 223
Polytrichum (moss), 70, 71, 80, 202, 203, 283
Poole, 367
Popa, 221

Popoff, 51, 186, 194, 247, 277
Popovici, 102

Populus (angiosperm), 389, 390, 397
Porphyra (red alga), 68
Portier, 89

Postmeiotic division, 265
Postreduction, 254
Potentilla (angiosperm), 340, 407
Powell, 190, 223
Powers, 121, 342
Prdt, 192
Pratje, 25
Preformation, 424
Preissia (liverwort), 233
Prell, 401

Premeiotic mitosis, 272
Prenant, 93, 160
Prereduction, 254
Preston, 178
Prevost and Dumas, 438
Priestley, 176
Primary constriction, 116
Primary mutant, 327
Primordial utricle, 430
Primula (angiosperm), chiasma, 270

gametes, 210

heteroploidy, 351, 352, 357

hybrids, 367

meiosis, 267, 274

variegation, 415, 416
Principal piece, 221, 222
Pringsheim, 437

558

INTRODUCTION TO CYTOLOGY

Prionidus (bug), 377, 378
Prochromosomes, 57
Promitosis, 192
Promorphology of ovum, 419
Pronucleus, 242, 263
Prophase, meiotie, 256

second meiotie, 264

somatic, 105, 106, 134, 137
Proplastid, 69, 91, 417
Protamine, 27
Protein, 100 ff.
Protenor (bug), 376, 377
Prothallial cell or nucleus, 207
Protista, ectoplast, 39, 43 ff.

mitosis, 191

nucleus, 48, 189

organismal theory, 22

sex, 376
Protoplasm, 25-47

chemical nature of, 25—31

colloidal nature of, 36-39

continuity, 16, 17, 18

doctrine, 432

early observations, 433

physical nature, 31-33

streaming, 31, 160, 161, 169, 185, 186

structural theories, 433-435

term, 433
Protoplast, 2, 433

outline of structure, 103-104
Protoxylem, 175
Protozoa, amitosis, 184, 191

cell theory, 429

chondriosomes, 89

differentiation, 10

ergastic substance, 101

flagellar apparatus, 223

Golgi material, 74, 81

meiosis, 277

nucleus, 59, 189

relation to Metazoa, 21

syngamy, 245
Prowazek, 190, 278
Prozymogen, 77

Prunus (angiosperm), 341, 351, 365
Prywer, 347

Pseudoamitosis, 185, 187
Pseudoblepharoplast, 217, 221
Pseudochondriosomes, 91
Pseudogamy, 406
Pseudomixis, 404
Pseudomonas (bacterium), 194
Pseudonucleoli, 56
Pseudopodium, 32, 43
Pseudoreduction, 252
Psilotum (pteridophyte), 432
Pteridophytes, 204, 233, 386
Pteris (fern), 12, 138, 403, 405
Puccinia (fungus), 231, 380, 387
Punnett, 286, 308
Purkinje, 433
Purkinje cells, 73

Pustularia (fungus), 83, 166, 167, 164, 281
Py, 71
Pycniospore, 231

Pygcera (butterfly), 368
Pyknosis, 187

Pylaiella (brown alga), 63, 280
Pyrenoid, 64, 68, 198
Pyronema (fungus), 281
Pyrrhocoris (insect), 376
Pyrus (angiosperm), 351
Pythium (fungus), 200, 229

Q

Quadripartition, 167

Quadripolar spindle, 151

Quadrivalent chromosomes, 350, 361

Quadrula (mollusk), 225

Quartets, 250

Quercus (angiosperm), 238, 342

Quisumbing, 10, 17

R

Rabbit. 184, 378

Rabl, 145, 438, 440

Raciborski, 66

Radiations, 186, 189, 273, 316, 388

Radium, 188, 311, 412

Radlkofer, 437

Rahn, 188

Ramie, 178

Ramsden, 40

Ramslow, 230

Randolph, heat treatment, 345

heteroploidy, 342, 343, 346, 351, 366, 358

hybrids, 360

irradiation, 187

plastid, 69, 72, 417

Zea chromosomes, 123, 316, 317
Random assortment of chromosomes, 254, 291—

293
RanunculacesB, 342

Raphanobrassica (angiosperm), 367, 368, 370, 371
Raphanus (angiosperm), 364, 367, 370
Raphides, 102, 103
Rappeport, 379
Rat. 378
Ratcliffe. 190
vom Rath. 184, 440
Rathery, 89
Rau, 74, 272
Rauber, 436
Rawitscher, 231

Reboulia (liverwort). 201, 233, 283
Recedent genom, 419
Receptive spot, 196, 197, 234
Recessive, 287
Reciprocal crosses, 418

Reciprocal translocation, 315, 322, 327-338
Recombination of factors, 294-304
Redfield, 266, 306, 353
Reduction, 89

of chromosomes (see also Meiosis). 250-283
Reed. G., 30, 57, 58, 59
Rees. C. W., 10, 223
Refringent body, 222
Regaud. 82, 84, 89

INDEX

559

Reichenow, 27, 189, 194
Reichert, 30, 100
Reinke, 26, 63
Reiss, 75
Reiter, 188
Rejuvenescence, 246
Remak, 431, 432
Renaut, 76

Renner, alternation of generations, 278
apomixis, 401
false hybrid, 406
(Enothera, 334, 336, 337
pollen characters, 308
reciprocal hybrid, 419
variegation, 416
Renner complex, 335, 336
Renyi, 18

Repulsion in mitosis, 163
Resin, 97

Respiration, 64, 65, 88
Restitution nucleus, 346, 404
Reticular theory of protoplasm, 434
Reticularia (myxomycete), 26
Reticulum of nucleus, 2, 53, 106
Reuter, 105, 136, 144, 146, 162, 256
Reznikoff, 29

Rhabditis (nematode), 169, 411
Rheum (angiosperm), 103
Rhizoclonimn (green alga), 191
Rhizoplast, 189, 223
Rhizopus (fungus), 83, 165, 166
Rhoades, M. M., 300, 306, 322, 332, 351, 419
Rhoades, V., 238
Rhodites (gall-fly), 272, 411
Rhodochorton (red alga), 63
Rhoeo (angiosperm), 256, 329, 335
Rhopalodia (diatom), 228
Rhumbler, 58
Ribes (gooseberry), 346
Riccardia (liverwort), 199, 203, 232, 233
Riccia (liverwort), 233
Rich, 428

Richards, A., 136, 146
Richards, O., 188
Richardson, C, 391
Richardson, E., 329
Ricinus (castor bean), 96, 96, 101, 103
Rickett, 196, 233
Riddle, 397, 398
Riella (liverwort), 437
Rigg, 93
Rings, due to deletion, 316, 317

due to reciprocal translocation, 328 ff.
Rita (fish), 78
Ritter, G., 185
Ritter, G. J., 176, 185
Ritter, W. E., 21, 436
Rivett, 102

Rivularia (blue-green alga), 192
Robbins, W. J., 196
Robbins, W. W., 196
Roberts, 436
Robertson, A., 235
Robertson, T. B., 25, 33, 40

Robertson, W. R. B., chromomeres, 141

chromosome arrangement, 126

chromosome morphology, 123, 130

meiosis, 256, 266, 268

parthenogenesis, 409-411
Robinia (angiosperm), 94
Robyns, 102, 149, 150, 161, 171
Rodewald, 26
Rogers, 229, 233
Rohde, classification of cell elements, 45

cytokinesis, 171, 173

intercellular substance, 182

nucleolus, 58

organismal theory, 24, 436
Rokizky, 311
Romanova, 189
Root hairs, 50
Rosa (angiosperm), apomixis, 405, 409

chiasma, 267, 268

chromosome sets, 365

heteroploidy, 340, 347, 354

hybrids, 362-364

meiosis, 267

Wilsoni, 367
Rosen, 56
Rosenberg, apomixis, 401-408, 406

chromocenters, 57

chromosome morphology, 124

chromosomes in hybrids, 339, 361

heteroploidy, 346-348

hybrids, 364

meiosis, 256
Rosenbusch, 224
Rosenvinge, 16
Roskin, 189
Rossenbeck, 52
Rossmann, 188
Roth, 342
Rothert, 63, 165
Roux, 141, 442, 444
Rubus (angiosperm), 358, 371
Ruckert, 146, 243, 440
Rudenko, 210
Rudolph, 90
Rudolphi, 426
Ruhland, 40, 71, 91

Rumex (angiosperm), 129, 342, 389, 390, 395
Rumjantzew, 84, 195
Russell, 21, 47, 436
Russow, 16
Rusts, 283
Rutgers, 212
Ruttle, 343, 345, 356
Ruys, 105, 256
Rybin, 186, 367, 368
Rytz, 165

S

Sabellaria (annelid), 30
Saccharum (angiosperm), 369
Sachs, 23, 46, 50, 430, 435, 436
Saez, 129, 130, 378
Sagitta (round worm), 272
Saguchi, 57, 58, 77, 184, 224, 225

560

INTRODUCTION TO CYTOLOGY

Sainmont, 206, 378

Sakamura, abnormal mitosis, 185, 186
chromonema, 139, 140
chromosome morphology, 115
chromosome size, 115
chromosomes in Triticum, 342
homologous chromosomes, 124, 273
Salamandra (amphibian), 133, 166, 187
Salix (willow), 390, 396
Salter, 100

Salvia (angiosperm), 88
Sambucus (angiosperm), 210
Samuelsson, 239
Sanchez, 79
Sanday, 235
Sande-Bakhuyzen, 98
Sands, 161

Sansome, E., 329, 331
Sansome, F., 286, 344
Santos, 389
Sap6hin, 70, 90, 203
Sappin-Trouffy, 282

Saprolegriia (fungus), 96, 165, 184, 200, 229, 402
Sargant, 212

Sargassum (brown alga), 247, 280
Sass, 230, 386
Satellites, 118, 119, 124, 127, 128, 130, 314, 349,

361, 367
Satina, 388, 398
Saunders, 308
Sax, chiasma, 268, 270, 271
chromonema, 139
heteroploidy, 342, 345
hybrids, 363, 366
male nuclei, 210
meiosis, 260, 267, 268
reciprocal translocation, 329, 335
syngamy, 237

Saxifraga (angiosperm), 367

Scarth, 32, 44, 53, 54, 165, 176

Scenedesmus (green alga), 68

Schacht, 437

Schacke, 283, 382

Schaede, 53, 163

Schaeffer, 31, 39, 40, 89

Schaffner, 201, 383, 396

Schaudinn, 194, 277, 278

Schaxel, 84, 194

Scheben, 222

Scheremetzewa, 295

Scherrer, 63, 70, 85, 90

Schilling, 66

Schimper, 61, 65, 68, 70, 99, 100

Schizophyllum (fungus), 230

Schlater, 436

Schleicher, 439

Schleiden, 20, 428, 437

Schleip, 188, 266, 411

Schlosser, 402

Schmidt, E., 57, 82

Schmidt, J., 378

Schmidt, P., 228, 280

Schmidt, W. J., 222

Schmitt, 224, 225

Schmitz, 63, 68, 100, 437, 438

Schnarf, 212, 226, 237, 239
Schneider, A., 439, 441
Schneider, H., 266
Schneider, K., 133
Schoeffel, 188
Schottlander, 204

Schrader, achromatic figure, 162, 163
apomixis, 410, 411, 413
sex, 376, 395
Schratz, 357, 398
Schreiner, 256, 266
Schiiepp, 11

Schultz, E., 51, 158, 187, 281, 395
Schultze, M., 433
Schultze, W., 69
Schulz, 342
Schulze, 176
SchiirhofT, amitosis, 183
apomixis, 402, 405
embryo sac, 212
male cells, 210
meiosis, 256
mitosis, 105
nucleolus, 58
plastids, 61
syngamy, 226, 236
Schussnig, 190, 279, 386
Schwann, 20, 428, 435, 438
Schwarz, 188
Schwarze, 165
Schweigger-Seidel, 438
Schweizer, 386, 405
Schwemmle, 273, 334, 342, 419
Sciara (fly), 163
Scillefe, 129, 186
Scinaia (red alga), 280
Scirpus (angiosperm), 174, 210, 341
Sclerotina (fungus), 387
Scolopendra (centipede), 272
Scolopendrium (fern), 402, 405
Scopolia (angiosperm), 60
Scorpion, 86
Scott, 79
Seal, 378
Sears, 180, 402
Sebaceous gland, 77

Secale (angiosperm), 143, 237, 260, 267, 366
Second contraction, 260
Secondary association of bivalents, 351
Secondary constriction, 116, 118
Secondary mutant, 327, 328
Secondary wall layer, 12, 175, 176
Secretion, 14, 98

chondriosomes in, 77, 88
Golgi material in, 75-78
and nucleolus, 58
Sedgwick, 21, 206, 436
Seeds, storage, 101, 102
Segmental interchange, 327-338
Segregation, 287

Seifriz, cryptoplasm and phaneroplasm, 45
emulsion, 36
hyaloplasm, 33
micromanipulation, 6
nucleus, 52

INDEX

561

Seifriz, protoplasm, 31, 32, 37, 39

X-ray analysis, 178, 179
Seiler, 268, 3S0, 397, 411

Sdaginella (pteridophyte) , 61, 69, 180, 181, 204
Selini, 119

Semiheterotypic mitosis, 346
Semipermeability, 37, 40, 41
Semisterile plants, 329-334
Senecio (angiosperm), 341, 345, 415
Senescence, 246

Senjaninova, 70, 71, 86, 90, 118, 342
Senjaninova-Korczagina, 128, 129
Senn, 61

Sepia (mollusk), 222
Serebrovsky, 315, 320
Sertoli cells, 215

Set of chromosomes, 121, 254, 325
Sethi, 233
Sex, chemical reactions, 226, 398

chromosomes, 297, 375-400

genes, 394

and heteroploidy, 394

historical, 436

intergrades, 394

in life cycles, 383

-limited characters, 391

linkage, 297, 391-393

metabolic theory, 398

modification, 396-399

and parthenogenesis, 410
Shafler, 88
Sharp, L. W., blepharoplast, 208

chromosomes, form and structure, 116, 124,
133, 136

cytokinesis, 174

life cycles, 383

mitosis, 133, 134, 137, 140, 142

reticulum, 55

organism-environment, 47, 312

sex, 388, 398

spermatogenesis, 199, 201, 203, 204, 206
Sharp. R. G., 10, 223
Shaw, 178, 204, 233
Shchavinskaia, 367
Shearer, 18
Sheep, 376
Sheffield, 334
Sheppard, 58
Shibata, 238

Shigenaga, 52, 57, 120, 140
Shimamura, 57, 206, 234
Shimotomai, 186, 340, 342, 386, 390, 395
Shinke, 52, 57, 120, 139, 140
Shiwago, 381

Showalter, 203, 232, 233, 343, 383, 395
Shull, A. F., 410
Shull, G. H.. 390, 392, 415
Siebert, 188
Sierp, 196
Sieve tube, 12, 13
Silene (angiosperm), 357, 390
Silk, 179

Simocephalus (crustacean), 411
Simplex, 354
Simplex group of chromosomes, 292

Simultaneous division, 167

Sinapis (angiosperm) , 50

de Sin6ty, 376

Sinigaglia, 73

Sinnott, 23, 286, 358

Sinoto, 164, 334, 357, 388, 390. 396

Sirks, 286, 419

Sisa, 121

Sjovall, 220

Skalinska, 367

Skupienski, 190, 278

SUme, 96, 100

Small, 29

de Smet, 124

Smilacina (angiosperm), 212

Smith, B. G., 136, 146, 243

Smith, D., 88

Smith, E. L., 100, 102

Smith, F. E., 184

Smith, F. H., 133, 139

Smith, G. M., 68, 196, 226, 278

Smith, I., 206

Smith, S. G., 139, 341

Sm61ska, 206, 235

Soderberg, 167

Sokolow, 87, 215, 223

Sol, 34

Solarium (angiosperm), 186, 273, 352, 356-358,

367, 406
Solenobia (moth), 411
Solvation, 34
Somatic mitosis, 105-113, 106, 112, 133-139

duration and periodicity. 111

outline, 105-109
Somatic mutation, 310, 345

Somatic pairing of chromosomes, 123, 126, 272
Sorghum (angiosperm), 341, 342, 415
SoTodiscus (myxomycete), 190
Sorokin, 116, 118
Space lattice, 178
Spallanzani, 438
SpaHina (angiosperm), 367
Spathipkyllum (angiosperm), 405
Special wall, 167, 168
Specificity of organisms, 30
Spek, 31, 169, 171
Speltoid wheats, 276
Spemann, 23, 412
Spencer, Herbert, 47
Spencer, Hope, 246
Spermatia, 197, 227, 231
Spermatid, 201, 216
Spermatocyte, 214, 215
Spermatogenesis, in animals, 81, 214-223

in plants. 70, 196-211, 202, 206
Spermatogonia, 214

Spermatozoids, 197, 199, 202, 227, 232, 239
Spermatozoon. 26. 215, 221, 222, 240, 241, 437
Spermiogenesis, 215-217
Sphacelaria (brown alga). 111, 159
Sphoerocarpos (liverwort), 233, 266, 283, 307, 382.

384, 395
Sphaeroplea (green alga), 227, 279
Sphagnum (moss). 201, 283
Spier, 176

562

INTRODUCTION TO CYTOLOGY

Spierer objective, 33

Spinacia (angiosperm), 343, 346

Spindle, 106, 107, 149, 162, 161, 162, 259, 274

of cytokinesis, 171, 173
Spindle-attachment region, 106-109, 115-119,
123, 148, 332

altered position, 320

effect on crossing-over, 302

fragments without, 317

in translocations, 321
Spindle fiber, 150
Spindle substance, 149, 151, 152
Spirillum (bacterium), 43
Spirogyra (green alga), conjugation, 228

cytokinesis. 111, 166

gametes, 43, 45, 196

hybrids, 308

kinoplasm, 44

meiosis, 279

mitosis, 190

nucleus, early observations, 437

plastid, 63, 64, 72, 279

pyrenoid, 68

syngamy, 228, 437

tonoplast, 42

vacuoles, 228

zygospores, 279
Spirostomum (protozoan), 50, 61
Spirulina (blue-green alga), 192
Spitzer, 59

Splitting of chromosomes, in meiosis, 252, 255,
258, 261, 265, 275

somatic, 105, 113, 133, 137, 145, 190
Spoehr, 27
Spongioplasm, 434
Spongospora (myxomycete), 190
Sponsler, 99, 100, 178, 179
Spore coat, 180, 181
Sporidia, 231
Sporocyte, 204
Sporodinia (fungus), 165

Sporogenesis, 70, 196-198, 200, 204, 206, 209-211
Sporophyte, 122, 204, 383 ff., 401 ff.
Sporophytic budding, 404
Sprengel, C. K., 436
Sprengel, K., 426
Stabilizer, 35

Stadler, 187, 188, 311, 316, 317, 356
Stains, 5, 7, 84, 139, 142
Stakman, 232
St&lfelt, 112, 171
Stalk cell, 207
Stemmkorper, 162, 163
Stancati, 382
Stangeria (cycad), 234
Starch, 66, 80, 97, 98, 99
Starfish, 240, 241
Stark, 139
Starks, 378
Steere, 352

Steil, 199, 203, 403, 404
Stein, 51, 188
Stellaria (angiosperm), 415
Stenar, 107, 212, 239
Stenobothrus (grasshopper), 7, 162

Stentor (protozoan), 50

Sterility, 352, 354, 356, 358, 359 ff., 387, 419

Stern, 68, 286, 301, 302, 303, 304, 321, 393

Stethophyma (grasshopper), 258, 304

Stevens, F. L., 199

Stevens, N. M., 272, 378, 381

Steward, 40

Stieve, 55

Stigeoclonium (green alga), 23

Stigma (eyespot), 66

Stiles, 40, 64

Stizolobium (angiosperm), 331

Stoel, 188

Stole, 58

Stoll, 64, 68

Stolte, 49

Stolze, 121

Stomates in polyploid Zea, 358

Stomps, 142, 345, 412, 416

Stone, 395

Stopes, 206

Storch, 410

Stork, 402

Stoughton, 194

Stout, 396

Stow, 186, 273

Strangeways, 3, 111, 187, 317

Strasburger, apomixis, 401, 402, 407

blepharoplast, 198

cell-division, 439

cell wall, 173, 174, 177, 178

chondriosomes, 82

chromocenters, 57

chromomeres, 142

chromosome number, 126

cytokinesis, 171, 173

eyespot, 67

kinoplasm, 44

meiosis, 262, 440

Mendelism and chromosomes, 445

mitosis, 190

nuclei, origin of, 432

nucleolus, 58

nucleoplasm, 2

nucleoplasmic ratio, 51

nucleus in heredity, 285, 441

protoplasmic continuity, 16

recombination, 302

sex determination, 375, 382, 388

starch, 65

syngamy, 437

tetrad chromosome, 262

tetraploidy, 345

vacuoles, 94
Streaming, 31, 185, 186

in cell-division, 160, 161, 169
Street, 179
Strepsinema, 259
Stroma, 67, 68

Strongylocentrotus (sea urchin), 242
Structural hybrids, 336
Strugger, 53
Studnieka, 15, 182
Sturgeon, 222
Sturtevant, crossing-over, 299, 302, 320

INDEX

563

Sturtevant, linkage groups, 296, 301
QSnothera, 335, 336

reciprocal translocation, 329

sex determination, 395
Stypocaulon (brown alga), 169, 280
Suberin, 176
Successive division, 167
Suessenguth, 71, 167
Sugars, 100
Sugimoto, 139
Sumner, 28
Superlinkage, 338
Supersexes, 394
Surface tension, 169
Surirella (diatom), 280
Sutton, 122, 272, 445
Svedberg, 33
Svedelius, 122, 278, 280
Svenson, 302
Svensson, 239
Sverdrup, 351
Swammerdam, 424
Swarm spores, 197
Sweschnikowa, 124, 129, 343
Swezy, 10, 190, 223, 379
Swingle, D. B., 165, 166
Swingle, W. T., 159, 173
Symbiosis, 89

Symphoricarpos (angiosperm), 44
Symplasm, 90
Synapsis, 252, 256, 257, 272-277

and apomixis, 407

and deletion, 319

in heteroploids, 350, 351, 352

in hybrids, 359 ff.

after inversions, 319, 320

in polyploid hybrids, 361 ff.

after reciprocal translocation, 331, 332, 333

in tetraploid, 350

in triploid, 352
Synchytrium (fungus), 50, 165, 199, 229
Syncytium, 15, 24, 171
Synergids, 210, 211, 237
Syngamy, in alg», 226

in animals, 239-249, 263

in fungi, 229

historical, 436-439

physiology of, 247

in plants, 197, 200, 211, 22fr-239
Synizesis, 256
Sypkens, 55
Syringa (angiosperm), 186

Tackholm, apomixis, 405, 408, 409

cytokinesis, 167

heteroploidy, 340, 348

hybrids, 362-364
Tahara, 197, 247, 340, 345, 402
Takamine, 124, 188
Takeda, 415
Talceporia (moth), 380
Tammes, 64
Tanaka, 420

Tandy, 158, 281, 282

Tangl, 16, 18

Tannin, 96, 97

Tannreuther, 190

Tansley, 278

Tanzer, 51

Tapetal Plasmodium, 181

Tapetum, 79, 83, 181, 183, 308

Taraxacum (angiosperm), 402, 403, 415

Tassement polaire, 135

Taxodium (gymnosperm), 208, 235

Taxus (gymnosperm), 235

Taylor, C. V., 6, 10, 19, 31, 49, 53, 223

Taylor, G., 188

Taylor, J. W., 367

Taylor, W. R., 114, 124, 129, 130, 139, 142, 260,

264, 265
Telezynski, 54, 133, 135
Teliospore, 231
Telomitic, 116
Telophase, meiotic, 262

somatic, 106, 108, 134, 135
Teosinte {see Euchlmna)
Telosynapsis, 337

Temperature effects, activation, 248
chromosome behavior, 273
crossing-over, 302
mutation, 311, 345
rate of mitosis. 111, 186
translocation, 317, 321
Tennent, 146, 195, 412
Tephrosia (moth), 413
Terao, 415
Terletzki, 16
Terminalization, 268-271
Terni, 85, 86, 87, 220
Tertiary mutants, 329
Tertiary wall layer, 175, 176
Tetrad chromosome, 252, 258, 262, 263, 271
Tetradesmus (green alga), 68
Tetranychus (mite), 410

Tetraploidy, 339, 342, 347, 350, 365 ff., 395
Tetrasomic plants, 350
Tetrasomic ratios, 352
Tetraspores, 280

Thalictrum (angiosperm), 340, 343, 391, 396
Tharaldsen, 154, 244
Thatcher, 25, 64, 93
Theophrastus, 422
Thom, 204
Thomas, 177, 308
Thompson, D'A. W., 19, 23
Thompson, W. P., 342, 366, 396
Thomsen, 410, 411
Thomson, 47, 399, 441
Thuja (gymnosperm), 235
Thuret, 437
Tiffany, 177

Timberlake, 165, 171, 174
Timof^eff-Ressovsky, 311
Tischler, achromatic figure, 153
amitosis, 183
apomixis, 401
cambial initial, 51
chromomeres, 142

564

INTRODUCTION TO CYTOLOGY

Tischler, chromosome number, 121, 126, 342

exine, 180, 181

heteroploidy, 345, 357, 358

meiosis, 256

mitosis, 105, 111, 159

nuclear crystals, 101

nuclear function, 58

nuclear membrane, 136

nucleolus, 57

nucleoplasmic ratio, 52

nucleus, 48-50

protoplasm, 25

restitution nucleus, 346

syngamy, 226, 236
Tissue cultures, 6, 85, 187
Tissue theory, 436
Tissues, 1-24

Tolypothrix (blue-green alga), 192
Tomowo, 352
Tonoplast, 2, 42, 94
Torreya (gymnosperm), 235
Torus, 175
Torvik, 395
Townsend, 58
Toyama, 420
Tozer, 57

Tracheid, 12, 13, 175
Trachelomonas (protozoan), 67
Tractile fibers, 150, 151, 162
Tradescantia (angiosperm), achromatic figure, 162

amitosis, 184

cell-plate, 171, 172

chromosomes, 132, 133, 139, 143, 163

fragmentation, 314, 319

kinoplasm, 44

meiosis, 256, 260, 261, 265, 267, 270, 431, 432,
440

micromanipulation, 6, 64

protoplasm, 31, 434

reciprocal translocation, 329

somatic mitosis. 111, 139
Trankowsky, 116, 117, 209, 210
Transeau, 308
Translocation, 121, 188, 306, 314-326

reciprocal, 316, 322, 327-338
Trennungstelle, 116
Treub, 174
Treviranus, 426, 432
Trialeurodes (fly), 410
Trichia (myxomycete), 278
Trichites, 99
Trichocyst, 44
Trichogyne, 228, 231
Trichomonas (flagellate), 223
Trichoniscus (crustacean), 413
Trichosanthes (gourd), 176
Triebel, 88
Trier, 25, 93
Trifolie®, 342
Trillium (angiosperm), 117, 134, 139, 236, 238,

258, 261
Trimerotropis (grasshopper), 254, 265
Triple fusion, 237, 238
Triplex, 354
Triploidy, 339, 345, 346, 352

Tripsacum (angiosperm), 407

Trisome, 297, 327

Trisomic plants, 352

Trisomic ratios, 297, 354

Triticum (wheat), abnormal mitosis, 186

chromosomes in hybrids, 129, 363

heteroploidy, 342, 343, 345, 356

parthenogenesis, 402

restitution nucleus, 346

syngamy, 237

vacuole, 102
Triticum X ^gilops,^6Q, 367, 368
Triticum X Secale, 367, 368
Triton (amphibian), 222
Trivalent chromosome, 274, 361, 363
Tron, 128
Trondle, 72, 279
Trophochromatin, 194
Trophonucleus, 224
Trophoplasm, 44
Trow, 199
Trypan blue, 76
Trypanosoma (flagellate), 44
Trypanosomes, 224
Tschechow, 129, 342
Tschenzoff, 190
Tschermak, 366, 367, 445
Tschernoyarow, 124
Tschirch, 101, 103
T'Serclaes, 190, 191
Tsinen, 417

Tsuga (gymnosperm), 235
Tswett, 68
Tuan, 139

Tube cell or nucleus, 208, 209, 237
Tulasne, 437
Tulipa (angiosperm), 186, 268, 267, 274, 361, 352,

354, 355, 367
Tumor, 187
Tupper, 358
Tupper-Carey, 176
Turesson, 408
Turgor, 42
Turkey, 381
Turner, 277
Turrill, 367
Tuschnjakova, 390
Tuthill, 188
Tuttle, 279
Twin hybrids, 338
Twins, 382
Twiss, 85, 382

Two-plane theory of chiasma, 268, 269, 271
Tyloses, 17
Tyndall phenomenon, 33

U

Uda, 420

Ulothrix (green alga), 68, 196, 198, 226, 227, 279

Ultramicroscopic structure, 177

Ultra-violet light, 139, 188

Uha (green alga), 68, 190, 279

Umbellifera;, 342

Undulating membrane, 44, 223

INDEX

565

Unger, 430

Unna, 26, 57

Urease, 28

Urechis (echinoderm), 163

Uredinese, 283

Uroglena (yellow-green alga), 44

Uroleptus (infusorian), 277

Uromyces (fungus), 231

Ustilago (fungus), 231, 386

Vvularia (angiosperm), 186, 273, 320, 345

Vacuole, 2, 93-96, 210

contractile, 42, 228

in cytokinesis, 165, 168, 171

ergastic contents, 96-98, 101, 102

membrane, 42 ff.

origin of, 94
Vacuome, 94, 193
Valkanover, 334

Valeriana (angiosperm), 342, 389, 390
Valleau, 391

Vallisneria (angiosperm), 210, 236
Valonia (green alga), 97, 178
Van Camp, 58
Van Cleave, 9
Vandel, 413

Vandendries, 283, 386, 388
Van der Stricht, 244
Van Durme, 88
Vanessa (butterfly), 50, 61
Van Regemorter, 185
Van't Hoff's law, 112
Van Teighem, 95
Variegation, 317, 415
Vaucheria (green alga), body structure, 8, 10, 23

gametes, 196

gametic meiosis, 279

mitosis, 190

parthenogenesis, 402

sex, 386

syngamy, 197, 227

zoospore, 198
Vaupel, 378
Vavilov, 342

Vegetative propagation, 354
Vejdovsky, 132, 133, 142, 266
Velten, 434
Verson's cells, 215
Verworn, 46
Vesperugo (bat), 222
Vessel, 12
Vicia (angiosperm), abnormal mitosis, 186, 187

cell-plate, 171

chondriosomes, 91

chromosome complement, 115, 118, 124, 128,
129

cytoplasmic heredity, 419

heteroploidy, 343

leucoplast, 62

meiosis, 267

nucleolus, 120, 121

plastids, 69

somatic mitosis, 133, 134

Vinca (angiosperm), 210

Vincetoxicum (angiosperm), 210

Vines, 401

Viola (angiosperm), 210, 236, 273, 342, 361, 415,

416
Virchow, 431, 439
Viscosity, 31, 169, 186, 248, 249
Viscum (angiosperm), 17
Visscher, 245
Vital dyes, 6
Vitamin D, 27

Vitelline membrane, 214, 240, 241
Voinov, 78, 86, 87, 215
Volkonsky, 62
Volutin, 27, 193

Volvocales (green alg£e), 16, 68, 279
Vouk, 101
de Vries, (Enothera species, 336, 338

recombination, 302

rediscovery of Mendelism, 445

theory of heredity, 441

tonoplast, 42

vacuoles, 79, 94

W

Tf -chromosome, 379, 380
Wager, 67, 66, 67, 199, 226
Wagner, 71, 85, 188
Wakayama, 57, 206, 282
Wakker, 66, 101
Waldeyer, 440
Walker, 57, 283
Wall thickening, 50
Wallin, 89, 90
Walter, H., 25
Walter, H. E., 286
Walton, 378
Waltzing mice, 317
Wdmoscher, 193
Wanderplasm, 197
Wanscher, 342
Warburg, 38, 89
Wassilief, 194
Watkins, 342, 366, 396
Wax, 102
Weatherby, 43
Webber, 199, 207, 234
Weber, 31, 32, 40, 61
Weier, (Enothera, 334, 337

plastids, 68-71

and Golgi material, 80, 81

spermatogenesis, 201, 203
Weigl, 74, 220
Weinstein, 302, 306, 311
Weismann, 141, 441-445
Wells, 25, 26
Wels, 186

Welsford, 210, 230, 236, 237, 281
Wendel, 50

Weniger, 236, 237, 238
Wenrich, amitosis, 190

chiasma, 268

chromomeres, 136, 141

flagella, 223, 224

566

INTRODUCTION TO CYTOLOGY

Wenrich, meiosis, 265, 266

nucleolus, 118

nucleus, 49

vacuoles, 42
Went, 19, 95, 97
Wermel, 52, 120, 195
Werner, 381
West, 196, 278
von Wettstein, apomixis, 402

cell size, 357

cell wall, 176

cytoplasmic heredity, 418, 419

gametophytic characters, 307, 355

heteroploidy, 340, 343, 405

polyploid moss hybrids, 371, 405, 408

sex in algffi, 386
Wetzel, 71, 91
Wherry, 59
White, 289
Whiting, A. R., 395
Whiting, P., 311. 382, 395
Whitman, 21, 425, 436, 438. 439
Whitney, 399. 410
Whong, 18
Wieman. 379
Wierzyski, 240
Wiesner, 93, 176, 177, 178
Wigoder, 187

Wikstrannia (angiosperm) . 345, 402, 407
Wilcox, 387
Wildeman, 111
Wille, 16
WiUems, 272
Williams, J. L., 227, 280
Williams, M., 186, 188, 190, 197, 279
Williamson, 158, 230, 281, 387
Willstatter, 64, 68
Wilson, E. B., amitosis. 183

aster. 154

cell-division, historical, 439

centrosome, 153. 155

chondriosomes. 86, 88

chromatin, 55

chromidia, 195

chromosomes, and heredity, 286, 291, 292
somatic, 121. 125

cytology and genetics, 445

cytoplasmic heredity, 420

epigenesis, 425

flagellum, 223

individuality of chromosomes, 145

karyosome, 189

meiosis, 256, 265, 268, 272

mitosis, 159, 160, 164

nucleoplasmic ratio, 51

organismal theory, 22

parthenogenesis, 412

protoplasm, 31, 32, 93

sex-chromosomes, 376, 379

spermatogenesis, 213, 215

syngamy, 239-245, 248

Weismannism, 442
Wilson, H. v., 6
Wilson, M., 201, 203

Winge, alloheteroploidy, 369

amphidiploidy, 367

apomixis, 408

chromosome number, 124

factor combinations, 292

galls and tumors, 186, 187

heteroploidy, 343, 347, 348

Hnkage, 391, 392

myxomycete. 190

sex-chromosomes, 378, 381, 389, 390, 393

variegation. 415. 416
de Winiwater. 58, 256, 266, 378, 379
Winkleman, 188, 311
Winkler, apomixis, 100, 401, 402, 407

altered chromosomes, 186

heredity, 286

heteroploidy, 340, 358

grafting, 344

nuclear phases, 122

nucleoplasmic ratio, 51
van Wisselingh, 58, 176, 177
Witschi, 376, 397, 398
Wodehouse, 180
Wodsedalek, 376
Wolff, 425
Wolfson, 382
WoUenweber, 66
Wood, F. M., 177, 179
Wood fiber, 12, 13
Woodburn, 201, 233
Woodger. 78. 88. 220
Woodruff, 49. 246
Woodward, 249
Woodwardia (fern), 405
Wortmann, 16
Woskressensky, 295
Wound hormone, 409
Wounding, 185, 186
W6ycicki, crystals, 101

cytokinesis, 167, 168

elaioplast, 66

gonomery, 236

gymnosperm egg. 206

meiosis in fungus, 281

plastids, 71

pollen tube, 42, 210
Wu, 51, 58
Wuist. 386
Wurdack. 177
Wygaerts. 55, 140, 142
Wylie, 210. 236
Wyman, 87

X-chromosome, 304, 376 ff.
X-ray analysis, of cell wall, 178

of chromosome, 317 ff.

of starch granules. 99
X-ray effects, on chromosomes, 186, 187, 273

on crossing-over, 302

and inversion, 320

on mutation, 311

and translocation, 317, 318, 321
Xanthophyll, 64

INDEX

567

y-chromosome, 304, 378 /.
Yamagiwa, 187

Yamaha, 5, 27, 120, 164, 165, 185
Yamamoto, 121, 129, 390, 395
Yamanouchi, achromatic figure, 159, 165

apogamy, 403

chondriosomes, 86

eyespot, 66

meiosis, 280

spermatogenesis, 204

syngamy, 227, 228, 229, 233
Yampolsky, 388, 396
Yasui, 416, 417
Yatsu, 154, 412
Yazawa, 201
Yeast, 96, 167
Yocum, 10, 223
Yolk, 78, 88, 100, 213
Young, R. A., 32, 188
Yuasa, 204, 205

Z

2-chromosome, 379, 380

Zacharias, 25, 56, 57

Zade, 342

Zamia (cycad), 199, 234

Zanardinia (brown alga), 66, 280

Zattler, 386, 408

Zea (maize), abnormal mitosis, 186, 187

chiasma, 271

chromomeres, 142, 143, 259, 274, 276

chromosome set, 298

chromosomes, 115, 118, 119, 121, 123, 135, 140,
259, 274, 276

crossing-over, 302, 303, 305

cytoplasmic heredity, 419

endosperm, 355

heteroploidy, 342, 343, 345, 346

inversion and deletion, 318, 319, 320

liguleless leaves, 299

linkage, 296, 300

linkage groups, 296, 297, 298

linkage map, 299

matrix, 120, 136

meiosis, 259, 261, 265, 273, 274, 276

Zea (maize), monoploid sporophyte, 356

non-disjunction, 345

non-homologous association, 276

nucleolus, 119, 120

plastid development, 69

pollen characters, 30, 308

root tip, 5

reciprocal translocation, 327, 329-334, 330, 832

silkless ears, 299

spindle, 164

stomates in polyploids, 358

syngamy, 237, 238

temperature effects, 317, 345

tetraploidy, 345

translocation, 316, 317, 321, 322

triploidy, 346, 347, 352, 354

trisomic inheritance, 297, 354

variegation, 415-417

Zea-Euchlwna hybrid, 360, 371
Zebrina (angiosperm), 261, 329
Zeleny, 412
Ziegenspeck, 172, 177
Zimmermann, A., 25, 66, 154
Zimmermann, W., 31, 68, 111, 159, 279
Zirkle, chondriosome, 90, 91

chromosome, 133

early hybridizers, 436

fixation, S

nucleolus, 68, 118, 120

permeability, 40

plastids, 67, 68, 69

spindle, 164

vacuole, 79, 93, 94, 96, 97
Zonaria (brown alga), 280
Zoospores, 197, 198, 199
Zuelzer, 186
Zulueta, 310, 393
Zweibaum, 74

Zygnema (green alga), 61, 65, 72, 279
Zygomycetes, 200
Zygonema, 256, 257, 258
Zygophase, 122

Zygospore, 198, 228, 229, 279, 307
Zygote, 122, 249
Zygotic meiosis, 278
Zygotic number, 122
Zymogen, 88