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^OUVKRIE ST.. E. C. 4 



Less than two months after the completion of the text of this book 
the author has received copies of the two new English works on cytology: 
W. E. Agar's Cytology, With Special Reference to the Metazoan Nucleus and 
L. Doricaster's An Introduction to the Study of Cytology. Both deal 
almost exclusively with animal cytology, the first being valuable for 
its account of chromosome behavior in animals, and the second for its 
discussions of gametogenesis, fertilization, parthenogenesis, and sex- 
determination. These works, together with the botanical portions of 
the present volume, should make an acquaintance with the general field 
of cytology much more readily attainable. 


PREFACE . . . vii 



The discovery of the cell Preformation and epigenesis Early theories of 
cell-formation Early observations on the cell contents The foundation 
of the cell theory Elaboration of the cell theory The protoplasm doctrine 
The new conception of the cell Fertilization and embryogeny The be- 
ginning of the modern period in cytology Bibliography 1. 



Description of the cell The differentiation of colls Bihlioyntphy 2. 



Physical properties Protoplasm as a colloidal system Microdissection 
Chemical nature of protoplasm Varieties of protoplasm The plasma 
membrane Protoplasmic connections Vacuoles Protoplasm as the sub- 
stratum of life Micromeric theories Chemical theories Conclusion 
Bibliography 3. 


THE NUCLEUS .... 50 

Occurrence General characters Nucleoplasmic ratio Structure of nucleus 
Nuclei of bacteria and other protista The function of the nucleus 
Bibliography 4. 



The centrosome Occurrence and general characters Individuality 
Centrosomes in Algae Fungi Bryophytes Conclusion The blepharo- 
plast Occurrence In flagellates In thallophytes In byrophytes In 
ptcridophytes In gymnospcrms In animals Conclusion Bibliography 5. 



Plastids General nature and occurrence Leucoplasts Chromatophores 
Starch The pyrenoid Elaioplasts and oil bodies The eyespot The 
individuality of the plastid Chondriosomes General nature and occur- 
rence Physico-chemical nature Origin and multiplication Function 
Relation of chondriosomes to plastids Conclusion Bibliography 6. 



Metaplasm Extruded chrornatin The senescence of the cell Polarity 
Metabolic gradient- Bibliography 7. 






Somatic mitosis Preliminary sketch of mitosis Detailed description of 
the behavior of the chromosomes in somatic mitosis Chromomeres 
Summary The individuality of the chromosome The frequent persistence 
of visible chromosome limits in the resting rcticulum Prochromosomes 
Persistence of parental chromosome groups after fertilization Size and 
shape of chromosomes Chromosome number Discussion and Conclusions 

Bibliography 8. ^ x 



The achromatic figure In higher plants In animals Intranuclear 
figures Origin of the figure The mechanism of mitosis Cytokinesis 
In thallophytes In microsporocytes In animals Mechanism of furrowing 

The cell wall The primary wall layer Secondary and tertiary wall 
layers The physical nature of the cell wall The chemical nature of the 
cell wall The walls of spores Bibliography 9. 


OTHER MODES OF NUCLEAR DIVISION ................... 202 

Cyanophycea? Protozoa Other cases in plants A mitosis A mitosis and 
heredity Bibliography 10. 

THE REDUCTION OF THE CHROMOSOMES .................. 219 

Discovery The stage in the life cycle at which reduction occurs The 
meaning of reduction Interpretations based on WeismamVs theory 
Somatic and heterotypic mitoses compared Modes of chromosome reduc- 
tion Scheme A Scheme B Comparison of Schemes A and B Reduction 
with chromosome tetrads Numerical reduction without qualitative reduc- 
tion Synapsis, or chromosome conjugation Relationship of the synaptic 
mates The stage at which conjugation occurs The nature of the synaptic 
union Chromomeres Other opinions on the heterotypic prophase - 
Bibliography II. 

FERTILIZATION ............................. 273 

Fertilization Jn animals The gametes The fusion of the gametes 
Fertilization in protozoa The physiology of fertilization Fertilization 
in plants Algae Fungi Bryophytes and pteridophytes Gymnosperrns 
Angiosperms Chromosome behavior Endosperm Bibliography 12. 


* * Apogamy Apflspory Parthenogenesis in animals Bibliography 13. 

^ * -------- - - - ~- t^rO 



The law of genetic continuity The r61e of the nucleus The promorphology 
of the ovum Plastid inheritance Aleurone inheritance General con- 





Mendelism A typical case of Mcndelian inheritance The cytological 
basis of Mendelism Mutation Mutations accompanied by changes 
in chromosome number Bearing on the origin of species and varieties 
Mutations accompanied by no change in chromosome number Conclusion. 


HEX ! ? 354 

Experimental evidence for sex-determination Sex-chromosomes Hex- 
chromosomes and Mendelism Experimental alteration of the sex ratio 
Metabolic theories of sex General discussion. 


LINKAGE s : : 'i .^ 378 

A typical case of linkage Hex-linkage Non-disjunction Linkage groups 
The chiasmatype theory Application of the chiasmatype theory to the 
problem of linkage General discussion Other theories of linkage Value 
of chromosome theory of heredity. 



Darwin's hypothesis of pangcnesis DeVrieVs theory of intracellular 
pangcncsis Nageli's idioplasm theory Weisniann's theory Home modern 
aspects of Wcismannism Non-factorial theories X" chemical theory of 
heredity Conclusion Bibliography 14 (for Chapters X1V-XVIII). 

INDEX 427 




The history of cytology falls naturally into three periods, of which 
the first begins with the discovery of the cell by Robert Hooke in 1665. 
the second with the foundation of the Cell Theory by Schleiden and 
Schwann in 1838-9, and the third with the important researches of 
Strasburger, Hertwig, Biitschli, and others' between 1870 and 1880. In 
the present sketch attention will be confined almost entirely to the first 
two periods, the work of the third, or modern, period being dealt with in 
the other chapters of the book. 

Prior to the seventeenth century attempts to analyse the structure 
of organisms were necessarily unsatisfactory. Aristotle (384-322 B.C.) 
in his De Partibus Animalium distinguished the " homogeneous parts" 
and the " heterogeneous parts/' the former corresponding in general to 
what we classify as tissues (bone, fat, cartilage, flesh, blood, lymph, 
nerve, membrane, nails, hair, skin, vessels, tendon, etc.), and the latter 
being the larger members of the body (head, face, hands, feet, trunk, 
etc.). Theophrastus, the pupil and successor of Aristotle, taught in his 
Historia Plantarum that the plant body is composed of "sap," "veins," 
and "flesh." Aristotle's classification was developed further by Galeq 
(131-201 A.D.) and by his followers. Although we no longer regard the 
above components as elementary parts, but rather as tissues and organs, 
the ancients may be pardoned for not carrying the analysis further, for they 
did not possess the necessary instruments. Something was then known 
about the refraction of light, but it was not until many centuries later 
that suitable lenses were available. The first compound microscope was 
brought out in 1590 by J. and Z. Janssen, spectacle makers of Middle- 
burg, Holland; and during the first part of the seventeenth century 
other improved models were designed by other workers. These instru- 
ments in the hands of men possessed of scientific curiosity^ soon led to 
jrpvny significant discoveries. A new world was opened to the eye of 
science, and the compound microscope- has since remained an instru- 
ment of extraordinary value in biological research. 



The Discovery of the Cell. Cytology may be said to have begun with 
the discovery of the cell by Robert Hooke (1635-1703) in 1665. Hooke, 
who lived in London and has been described as a man of eccentric appear- 
ance and habits, showed a remarkably varied scientific activity. For a 
time he was a professor of geometry, and later became an architect. He 
performed many original experiments in mechanics and for a number of 
years was curator of experiments to the Royal Society. His interest in 
optics led him to examine all sorts of objects with the compound micro- 
scope. In charcoal and later in cork and other plant tissues he found 
small honeycomb-like cavities which he called "cells." He had no dis- 
tinct 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 Micrographia (1665), a 
large work illustrated with 83 plates. The chapter containing his re- 
marks on cells is entitled "Of the schcmatisme or texture of cork and 
the cells and pores of some other such frothy bodies." Quaint arid crude 
as it now appears to us, the Micrographia takes its place as the earliest 
cytological classic. 

Three other names even more prominent in the early history of micro- 
scopy are those of Malpighi, Grew, and Leeuwenhoek. Marcello Mal- 
pight (1628-1694), an Italian physiologist and professor of medicine at 
Bologna, Pisa and Messina, is best known for his important pioneer work 
in anatomy and embryology. Most of his observations on plants wore 
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. 
Malpighi made a distinct step in advance in studying tissues with the 
cell as a unit; a clear fore-shadowing 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, who was 
one of the first to use the microscope on the tissues of higher animals. 

Nehemiah Grew (1641-1712) was an English physician and botanist. 
He began a careful study of plant structure in 1664, and in 1670 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:" . . .theparen- 
chyma of the Barque," he said, "is much the same thing, as to its con- 
formation, which the froth of beer or eggs is, as a fluid, or a piece of fine 
Manchet, as a fixed body" (p. 64). 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 interwoven threads. He accordingly compared the structure 
of the plant with that of a basket, and with "fine bone-lace, when the 
women are working it upon the cushion " (p. 121). 

Antony 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. His work, in spite of the fact that 
it was carried on without any definite plan, brought to light a number 
of important facts, but in general his accomplishments do not bear 
favorable comparison with those of Grew and Malpighi. 

Preformation and Epigenesis. After the death of Leeuwenhoek 
there ensued a period during which the actual investigation of the cell 
and the structure of organisms remained practically at a standstill. At 
that time, however, certain speculations were indulged in which should 
be recorded here, not because they can be regarded as scientific cytology 
but because of the influence they exerted upon the formulation of many 
cytological problems in later years. These speculations resulted in the 
division of the biologists of the day into two schools, the main question 
at issue being the manner in which the embryo develops from the egg. 
The two theories formulated in answer to this question have been called 
the Preformation Theory and the Theory of Epigenesis. 

According to the Preformation Theory, the basis for which was laid 
in the seventeenth century works of Swammerdam, Malpighi, and 
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 Evolu- 
tion, a phrase 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. This theory 
of encasement (emboUemenf) was a logical deduction from the since 
abandoned premise that everything, including organisms for all time, 
had been formed by one original creation, and that no thing c&ttld there- 
fore be formed anew. The preforrnationists soon became separated into 
two groups: the spermists or animalculists, and the oyists. By the 
former the new individual was supposed to be encased Jn the sperma- 
tozoon, and figures were actually 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 of preformationists, and various 
interesting compromises were made. But all extreme forms of pre forma- 
tionism 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 Animaliunij 1651), 
and Caspar Friedrich Wolff (1733-1794;,JF/ie0na Generations, 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 there was room for the principle of true generation, or "the 
production of heterogeneity out of homogeneity." The Theoria Genera- 
tionis 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 
von Baer 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 or both of these views, but to seek out the 
germs of truth possessed by each, and to relate them to modern biological 
conceptions. "The two views missed the mark by over-shots in contrary 
directions," says Whitman. The one theory claimed too much preforma- 
tion: everything was preformed at the start. The other theory claimed 
too much postformation: everything was formed anew. 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 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 post-formation to be explained as the result of pre-formation, and 
how far as the result of external influences?" When it is borne in mind, 
therefore, that one of the outstanding problems of modern cytology is 
that of identifying the factors involved in the development of an organ- 
ized and highly differentiated individual from an organized but rela^v :)y 
undifferentiated egg cell, it is at once evident that our sketch of cyto- 
logical history would be incomplete without the above reference to the 
early Theories of Preformation and Epigenesis. 


Early Theories of Cell-formation; The researches of Hooke, 
Malpighi, and Grew in the seventeenth century had shown that " cells," 
or " globules/' are important structural elements in organisms. When 
attention was again directed to such matters in the eighteenth century 
there was very soon felt a need for a theory which would account for the 
origin of cells. We may briefly review some of the suggestions which were 

One of the earliest theories of cell-formation was that put forward by 
Wolff in the Theoria Generationis. According to Wolff, every organ is 
at first a clear, viscous fluid with no definite structural organization. 
In this fluid cavities (Blaschen; Zellen) arise and become cells, or, by 
elongation, vessels. These v may later be thickened 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 essen- 
tialis) inherent in the living mass. Three important points in Wolff's 
theory should be noted because of the relation they bear to subsequent 
conceptions of the role of cells: the spontaneous origin of the cell> the 
organization of parts by differentiation in a homogeneous living mass, 
and the passive role of the cell in this organizing process. This theory 
was adopted in 1801 by C. F. JVLirbelCl 776-1854), who further believed 
that the cells communicate through pores in their walls. 

K. Sprengel (1766-1833) stated that cells originate in the contents 
of other cells as granules or vesicles which absorb water and enlarge. 
SprengePs observations seem to have been very poorly made, for he 
evidently mistook starch grains for the " vesicles" which were supposed 
to grow into new cells. But Sprengcl's theory 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 thebry 
that granules in the latex are "cell germs" which later hatch in the inter- 
cellular spaces to form new cells. 

With a much clearer understanding of the nature of the problems 
involved a number of excellent observations were made by J. J. Bern- 
hardi 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 views, for they promised to lead in the right 

A number of years later Mirbel, inaworkonMarc/ianta'a(1831-l833), 
distinguished three modes of celUformation: (1) the formation of cells on 
the surface of other cells, (2) the formation of cells within older cells, and 
(3) 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 misinterpreta- 
tion of the process of cell-multiplication in growing gemmae. 


Hugo von Mohl (1805-1872), in spite of his many valuable observa- 
tions on the growth of algae, in 1835 agreed essentially with Mirbel. He 
made a step in advance, however, when he described carefully for the 
first time the division of a cell. We shall see further on that von MohlV 
later researches contributed largely to the upbuilding of an adequate 
theory of the cell. 

F. J. F. Meyen (1804-1840) held that there are three fundamental 
forms of elementary organs: cells, spiral tubes, and sap vessels. He 
noted the wide occurrence of cell-division but did not describe the process 
in detail. Meyen apparently made the first attempt to distinguish cell- 
division from the free cell-formation described by previous workers. It 
has been pointed out by Sachs that if this short step had been clearly 
taken earlier the peculiar theory of coil-formation later developed by 
Schleiden would have been impossible. Von Mohl also had made obser- 
vations ruling out Schleidcn's idea, but his excessive caution prevented 
him from making a decisive statement on the subject. H. J. Dutrochet 
(1776-1847) in 1837 described the body as being composed of solids and 
fluids, the former being aggregations of cells of a certain degree of firmness, 
and the latter, such as blood, being made up of cells freely floating. He 
believed that although the cell contents may be more or less solid, the 
highest degree of vitality is compatible only with the liquid condition. 
He further recognized muscle fibers as elongated cells. 

To all the above workers the important elementary unit was the 
"globule." It was customary to refer to this conception as the Globular 
Theory, in contradistinction to the curious and fanciful Fiber Theory 
put forth by Haller (1708-1777) many years before (1757), according to 
which the organism is made up of slender fibers cemented together 
by "organized concrete/' For some the term "globule" stood for the 
granules seen in the cell contents, whereas for others it meant the cell 
itself. As observations multiplied and ideas became more definite the 
Cell Theory of Schleiden and Schwann was more and more distinctly fore- 
shadowed. Before turning to the Cell Theory, however, we must notice 
briefly a few observations which had been made on the cell contents. 

Early Observations on the Cell Contents. Although the true nature 
and significance of the contents of cells were not recognized until many 
years later, a number of early investigators had seen protoplasm and had 
been impressed by certain of its activities. As early as 1772 Corti, and a 
few 3'ears later Fontana (1781) saw the rotation of the "sap" in the 
Characese and other plants. After being long forgotten these facts 
were rediscovered by L. C. Treviranus (1811) and G. B. Amici (1819), 
whereupon Horkel, an uncle of Schleiden, called attention to the earlier 
work of Corti. Protoplasmic circulation of the more complex type was 
discovered in the stamen hairs of Tradescantia by Robert Brown in 1831, 
and other workers, especially Meyen, soon added other cases. 


During the first third of the nineteenth century no name is of greater 
interest to cytologists than that of Robert Brown (1773-1858). Al- 
though he is famous chiefly for his great taxonomic monographs and his 
morphological work, he is known in cytology as the man who is usually 
given the credit for the discovery of the nucleus, which he announced 
in 1831. Although it was Brown who was impressed by the probable 
importance of the nucleus, and who concluded in 1833 that it is a normal 
cell element, certain other observers, notably Fontana, who described a 
nucleus in 1781, and Meyen, who saw it in Spirogyra in 1826, should 
share the honor for its discovery. The phenomenon which has since 
been known as "Brownian movement" was seen by Brown in 1827. 

The first period in the development of our subject is seen to have 
been one in which there was a tendency to indulge in speculation to an 
extent quite unwarranted by the facts at hand. As we have already 
pointed out, however, this speculation was of considerable importance to 
us, in that it had to do with questions which later became central prob- 
lems of cytology. Carefully made observations were meanwhile in- 
creasing in number and varieyt, and the time eventually became ripe 
for the formulation of a theory which would correlate these data and give 
a definite trend to cytological investigations. Such a theory was soon 

The Foundation of the Cell Theory. The year 1838 marks an epoch 
in the history of biology. In this and the following year Schleiden and 
Schwann founded the Pell' Theory, which, in view of its enormous in- 
fluence upon all branches of biological science, may be regarded as second 
in importance only to the Theory of Evolution. We have seen that cells 
had been observed by various workers during many years, and had been 
recognized as being constantly present in the bodies of living organisms, 
but it remained for Schleiden and especially Schwann to formulate a 
comprehensive theory embracing the known facts and affording a start- 
ing point for further researches. 

The Cell Theory stated primarily that the body is composed entirely of 
cells and their products , the cell being the unit of structure and function 
and the primary agent of organization. Subsidiary to* this was Schleiden's 
theory of cell-formation, which should not be confused with the main 
thesis just stated. 

Matthias Jakob Schleiden (1804-1881) is one of the most prominent 
and interesting characters in botanical history. He studied law at 
Heidelberg, medicine at Gottingen, and botany at Berlin, where he met 
Schwann and Robert Brown. The association of these men undoubtedly 
meant much to the future of botany and zoology. Eventually Schleiden 
became Professor of Botany at Jena, where he remained for 23 years. 
Schleiden was famous not merely because of his own work, but chiefly as 
the result of the tremendous impetus which he gave to investigation. 


He sought to place botany on a scientific footing equal to that of physics 
and chemistry, and insisted upon accurate observation and developmental 
studies as the basis of morphology. Sachs says: " Endowed with some- 
what too great love of combat, and armed with a pen regardless of the 
wounds it inflicted, ready to strike at any moment, and very prone to 
exaggeration, Schleiden was just the man needed in the state in which 
botany then was." 

Theodor Schwann (1810-1882) was associated as a student with 
Johannes Miiller, the great physiologist, first at Wiirzburg and later at 
Berlin. It was in the latter place that he put forth his statement of the 
Cell Theory. Immediately afterward he went to Louvain, where he was 
a professor for nine years, and later transferred to Li&ge. In disposition 
he contrasted strongly with Schleiden, being described as " gentle and 
pacific. " 

It is said that Schleiden, while dining with Schwann, discussed with 
him some of his ideas regarding cells in plants, which he had been studying 
in his laboratory. Schwann had been making similar observations on 
animals, and after the meal the two went to Schwann's laboratory, whre 
they came to the conclusion that cells are fundamentally alike in both 
kingdoms. Schleiden's treatise on the subject, Beitrdge zur Phylogenesis, 
appeared in 1838 and dealt mainly with the origin of cells. Robert Brown 
had recently discovered the nucleus, and about it Schleiden built up his 
theory of "free cell-formation, " which was essentially as follows: In the 
general cell contents or mother liquor (" cytoblastcma ") there are formed, 
by a process of condensation, certain small granules (later called "nu- 
cleoli" 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. 7 ' This vesicle in each case enlarges and forms a new cell, 
and, since it arisee upon the surface of the cytoblast (nucleus), "the 
cytoblast can never lie free in the interior of the cell, but is always en- 
closed [i.e., imbedded] in the cell wall . . . " Schleiden thus regarded 
new cell-formation as endogenous ("cells within cells") rather than the 
result of cell-division. With respect to the main proposition of the Cell 
Theory he says in the opening paragraphs: "... 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 in- 
dividual cells must form the first, absolutely indispensable fundamental 
basis, both as regards vegetable physiology and comparative physiology 
in general; . . . " 

Schleiden shared the results of his observations, including his errors, 


with Schwann, who was the one to formulate the Cell Theory in a com- 
prehensive manner. Schwann announced the theory in concise form in 
1838, and in 1839 published a very full account under the title "Mikro- 
skopische Untersuchungen uber die Uebereinstimmung in der Struktur und 
dem Wachsthum der Thieve und Pflanzen." He says: "The elementary 
parts of all tissues are formed of cells in an analogous, though very diver- 
sified manner, so that it may be asserted that there is one universal prin- 
ciple of development for the elementary parts of organisms^ however different, 
and that this principle is the formation of cells. )} And further: "The 
development of the proposition that there exists one general principle 
for the formation of all organic productions, and that this principle is 
tho formation of cells, as well as the conclusions which may be drawn from 
this proposition, may be comprised under the term Celt Theory . . . " 
" . . .all organized bodies are composed of essentially similar parts, 
namely, of cells . . . " 

Elaboration of the Cell Theory. The Cell Theory at once became 
established as one of the main foundation stones of biological research, 
but it underwent considerable modification as investigations proceeded. 
The main thesis, that the body is composed of cells and their products, 
remained, but other ideas associated with this in the minds of Schleiden 
and Schwann, particularly that concerning free cell-formation, were 
superseded. Soon after the formulation of the Cell Theory its elabora- 
tion was begun by linger, von Mohl, and Nageli, who based their con- 
clusions on observations of a very high order. FranzUnger (1800-1870), 
in two works appearing in 1844 on vegetable growing points and the 
growth of internodes, argued for the origin of cells by division. Von 
Mohl^ in two treatises (1835, 1844), maintained tKatlTierc~are two metl> 
ods of cell-formation : by division aiic^ by the formation of cells within 
cells. He thought the "primordial utricle " (protoplast) must be ab- 
s"orbed to make way for the two new ones, or, less probably, the old one 
must divide into two. Like Schleiden, he thought the nucleus must be 
incorporated in the cell wall, but later (1846) concluded that it lies in 
the primordial utricle. It was in his paper of 184j^ that von Mohl in- 
troduced the term "fitf^^jala^^ * n its present sense. 

Carl von Nacgli (1807-1891) in 1844 produced an exhaustive treatise 
on the nucleus, cell-formation, and gfi.wib In algae and the micro- 
sporocytes of angiosperms he ejfearly showed that cells multiply by 
.division, and Schleiden was forced to admit that this might be "aj&eeoiid 
kjnji of cell-forjnation." The continuation of Naegli's researches in 
1846^oinpte1^y'0"ver l EhrGw Schleiden's conception of free cell-formation, 
establishing the significant fact that 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 
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 was 
only a special case of the former. Nageli's conclusions were supported 
by new evidence furnished by other investigators, who further demon- 
strated 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 was now clear 
i\\&i\cells arise only from preexisting cells } )Si conception which had been 
emphasized by Remak (1841) and which Virchow (1855) expressed in the 
dictum " omnis cellula e cellula." 

Opinions concerning the origin of the nucleus and its role in cell- 
division varied greatly among these workers, reliable observations being 
as yet insufficient to allow the formulation of any definite conclusion. 
In 1841 Henle believed with Schleiden and Schwann that the nucleus was 
formed by trie aggregation of " elementary granules/' and that it was not 
constantly present. Goodsir looked upon the nucleus as the reproduc- 
tive organ of the cell. Von Kolliker in 1845 asserted that nuclear divi- 
sion precedes the division of the cell, and 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, arid cell mem- 
brane were supposed to divide in turn by simple constriction. Just such 
a process, though evidently very exceptional, has been observed at a 
more recent date by Conklin (1903). In describing a case of nuclear 
division Wilhelm Hofmeister (1824-1877) stated that the membrane of 
the nucleus dissolved, the nuclear material then separating into two 
masses around which new membranes were formed (1848, 1849). It was 
generally believed, however, that the origin of nuclei by division was 
of rare occurrence, and that ordinarily the nucleus dissolved just before 
cell-division, two new ones forming de novo in the daughter cells. Von 
Mohl (1851), who in the main agreed with Hofmeister, wrote as follows: 
"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 produc- 
tion 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. Naegli thinks that the process is 
quite similar to that in cell-division, the membrane of the nucleus form- 
ing a partition, and the two portions separating in the form of two dis- 
tinct cells. " 

It was not until many years later, in connection with researches upon 
fertilization and embryogeny, that the behavior of the nucleus in cell- 
division became known in detail, and its probable significance pointed 
out. 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" (1882). (See footnote, p. 143.) 


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. To its discoverers the 
cell meant nothing more -than the 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. Even those who had been impressed by the phe- 
nomenon of protoplasmic streaming were not aware of the significance of 
the substance before their eyes. 

Felix Dujardin (1801-1860) in 1835 described the "sarcode" of the 
lower animals as a substance having the properties of life. Von Mohl 
had seen a similar substance in plant cells, and in 1846, as noted above, 
he called it "Schlcim," or "Protoplasma," the latter term having been 
used shortly before by Purkinjc in a somewhat different sense. Niigeli 
and A, Pa yen (1795-1871) in 1846 recognized the importance of proto- 
plasm as the vehicle of the vital activity of the cell; and Alexander Bniun 
(1805-1877) in 1850 pointed out that swarm spores, which are cells, con- 
sist 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, hut which 
is imprisoned, and only becomes free in the animal; or, to strip off the metaphor 
which obscures simple thought, the energy of organic vitality which is manifested 
in movement is especially exhibited by a nitrogenous contractile substance, 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 jSchultge was especially 
important in that it firmly established in 1861 the Protoplasm Doctrine J 
namely, that the units of organization are masses of protoplasm, and that 
this substance is essentially similar in all living organisms. The cell, 
according to Schultze, is "a mass of protoplasm containing a nucleus, 
both nucleus and protoplasm arising through the division of the corres- 
ponding elements of a preexisting cell." The cell wall, upon which the 


early workers had focussed their attention, turned out to be of secondary 
importance. The ell was thus seen to be primarily the organized 
protoplasmic rna$s, to which Hanstein in 1880 applied the convenient 
term protoplast. 

Extensive studies on the physical nature of protoplasm were soon 
undertaken by Kiihne (1864), Cienkowski (1863), and'de Bary (1859, 
1864); and there later followed the well-known structural theories of 
Klein, Flemming, Altman, and Btitschli. (See Chapter III.) 

Von Mohl as early as 1837 held that the plastid is a protoplasmic 
body. The classic researches of Nageli (1858, 1863) on plastids and 
starch grains laid the foundation for our knowledge of these bodies, which 
was greatly extended in later years by Meyer (1881, 1883, etc.) and 
Schirnper (1880, etc.). (Sec Chapter VI.) 

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, in which he has learned to 
include himself. 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 Huxley in his well-known 
essay, The Physical Basis of Life (1868). 

The New Conception of the Cell. The conception of the cell had now 
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 
and multiplication of cells had been overthrown. Future researches 
were to show more clearly the importance of the cell 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 Schlei- 
den and Schwann the multicellular 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, 
notwithstanding its severe criticism by Sachs, de Bary, and many other 
later writers who pointed out that, owing to the high degree of physio- 
logical 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 as such the exercise 


of its functions must be governed to a considerable extent by the organ- 
.ism as a whole (Wager). Such divergence of opinion led to much dis- 
cussion over the^fuestion of organic individuality, which remains as 
one of the important problems of modern biology. 

But in spite of all these changes we should not forget the great service 
rendered by Schleiden and Schwann in the formulation of the CellTheory. 
Huxley (1853)"estimated the value of their contribution in the following 

" Doubtless the truer a theory isthe more appropriate the colligating; 
conception the better will it serve its mnemonic purpose, but its absolute 
truth is neither necessary to its usefulness, nor indeed in any way cognizable by 
the human faculties. Now it appears to us that Schwann and Schleiden have 
performed precisely this service to the biological sciences. At a time when the 
researches of innumerable guideless investigators, called into existence by the 
tempting facilities offered by the improvement of microscopes, threatened to 
swamp science in minutiae, and to render the noble calling of the physiologist 
identical with that of the 'putter-up' of preparations, they stepped forward with 
the cell theory as a colligation of the facts. To the investigator, they afforded 
a clear basis and a starting point for his inquiries; for the student, they grouped 
immense masses of details in a clear and perspicuous manner. Let us not be 
ungrateful for what they brought. If not absolutely true, it was the truest 
thing that had been done in biology for half a century." 

Fertilization and Embryogeny. In Plants. Although it was known 
to the ancients that there is in plants something analogous to the sexual 
reproduction seen in animals, 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. Definite 
proof that the stamens are (to speak somewhat loosely) the male organs 
was furnished in the well-known experiments of R. J. Camerarius (1691). 
But in spite of the excellent work of J. G. Koelreuter (1761), C. K. 
Sprengel (1793), and K. F. Gacrtner (1849), all of whom proved the 
correctness of this conclusion, the idea of sexuality in plants was vigor- 
ously combatted 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 stigma 
down 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 
supposed to enter the ovule and enlarge 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, Schleiden (1842, 1844) using the most vigorous 
language in support of his position. After Hofmeister (1849) had fol- 


lowed the process with his 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, but that a 
fertilizing substance diffused through its wall. 

It was in the algse that the union of the sperm cell with the egg cell 
(the act of fertilization) was first seen in the case of plants. In 1853 
Thuret saw spermatozoids attach themselves to the egg of Fucua, 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 Pringshcim (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 (1879), 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. 

That the same process occurs in fertilization in the higher plants 
was demonstrated by Strasburger, who in 1884 described the union of the 
egg nucleus with a nucleus brought in by the pollen tube. In 1898 and 
1899 S. Nawaschin and L. Guignard completed the story by describing 
the phenomenon of double fertilization, whereby the second male nucleus 
contributed by the pollen tube unites with the two polar nuclei to form 
the primary endosperm nucleus. The subsequent work of Strasburger 
and others on the gymnosperrns arid angiospcrms greatly cleared up the 
whole matter of fertilization and embryogeny in these plants. This 
work belongs to the modern period of cytology. 

In Animals. It is probable that the spermatozoon was first seen in 
1677 by Ludwig Hamm, a pupil of Leeuwenhoek. The credit for the 
discovery, however, is 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 
into the egg, but it was thought at that time and for many years after- 
ward that they were parasitic animalcules in the spermatic liquid; hence 
the name " spermatozoa." 

Although L/ Spallanzani (1786) is usually said to have shown by his 
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 spermatozoon 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 considering 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 Cams 
(1824). Butschli (1875) showed them to be formed as the result of 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 (b. 1849) announced the important discovery that the two 
nuclei seen fusing in the fertilized egg are furnished by the egg and the 
spermatozoon by the two parents. The role of the nucleus in fertiliza- 
tion was thus demonstrated 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 fertilization in both kingdoms consists in the union of 
two cells (gametes), one from each parent (in dioecious forms), and that 
the central feature of the process is the union of the two gamete nuclei, the 
new individual therefore deriving half of its nuclear substance from each 

Although the cleavage of the fertilized animal egg to form 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 known to be 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, 
and by a number of later writers, including A. von Kolliker, who traced 
in detail the long series of changes by which the multiplying embryonic 
cells become differentiated into the various tissues and organs. Ernbry- 
ogeny was thus shown to be a process of cell-division and differentiation, 
the fertilized egg cell initiating a series of divisions giving rise to all the 
cells of the body, and to the germ cells. The life cycle was now recognized 
as a cell cycle; and since the egg is the direct descendant of the egg of the 
previous generation it became evident, as Virchow pointed out in 1858, 
that there has been an uninterrupted series of cell-divisions from the 
beginnings of life on the earth in the remote past down to the organisms 
in existence today. The statement of this conception is known as the 
Law of Genetic Continuity. In the words of Lpcy (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 


biology.' 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. '* 

The Beginning of the Modern Period in Cytology. As Wilson (1900, 
p. 6) points out, the great significance of the many facts brought to light 
in the early days of cytology lies in the relation which they bear to the 
Theory of Evolution and to the problems of heredity, though for many 
years this was only vaguely realized. 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 fertiliza- 
tion, which brought the Cell Theory and the Theory of Evolution into 
intimate association, began shortly after 1870 with the works of Schneider 
(1873), Auerbach (1874), Fol (1875, etc.), Biitschli (1875, etc.), O. Hertwig 
(1875, etc.), van Beneden (1875, etc.), Strasburger (1875, etc.), Flemming 
(1879, etc.), and Boveri (1887, etc.). 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 was given when the 
zoologists Hertwig, von Kolliker and Weismann, and the botanist Stras- 
burger, 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 
heredity, 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. 

Bibliography 1 

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the cell: 
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GEGENBAUR, K. 1861. Ueber den Ban und die Entwicklung der Wirbelthiere. 

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WOLFF, C. F 1759. Theoria Generationis. 



In a survey of the evolution of biological science it is noticeable that, 
while (^verging )iftes of inquiry have broadened the field of view, the 
attention of investigators, speaking generally, has been directed in turn 
to successively smaller constituent parts of the organism. F*or many 
years plants and animals were studied chiefly as wholes. But very 
early there were made many scattered observations on the various or- 
gans and tissues composing the body, and from these relatively crude 
beginnings morphology and histology later arose. Again, 

protoplasmic mass which we know as the cell came to be recognized as 
the unit of structure and of function, it was evident that the problems 
it presents should be investigated to a certain extent by themselves, and 
such investigation is the task of modern cytology. 

Within the field of cytology itself the focus of fottpntion. has gradu- 
ally shortened. While many workers occupied themselves with a study 
of the general behavior of the cell nucleus, others devoted their efforts 
entirely to an investigation of its important constituent elements, the 
chromosomes. Furthermore, cytologists at present are much interested 
in knowing whether or not any smaller units, corresponding to the 
" genes" of the geneticist, can be directly demonstrated, and whether 
or not the chromatic granules or " chromomeres " are of significance in 
this respect. 

In the course of all such studies there are encountered questions 
which must be referred ultimately to the chemical molecules and atoms 
and their interactions within the cell, so that biochemistry may in a 
measure be looked upon as a department of cytology, just as it is to be 
regarded in other respects as a subdivision of chemistry. The subject of 
cytology thus occupies an important position in the system of natural 
sciences. It stands with cherni^ry and physics on the one hand and the 
complex phenomena peculiar to living organisms on the other; and the 
steady mutual approach of the physico-chemical and biological fields 
is due in large measure to the results of morphological and physiological 
studies on the cell. 

For the term cell we are indebted to Robert Hooke and the other 
microscopists of the seventeenth century, who applied it to the small 
cavities in the honeycomb-like structiire which they discovered in plant 
tissues. Today^Thentefm denotes primarily the protoplasmic "cell 
contents/' which, strangely enough, the early workers regarded as an 




unimportant fluid product. The term protoplast, proposed by Hanstein 
(1880), is more appropriate and is coming into more general use, but long 
usage n and brevity have probably insured the permanence of the older 

Fia. 1. Diagram of the cell, showing its principal constituent parts. 
A % centrosphere, with centrosome and aster. B, nucleolus or plasmosome. C, nuclear 
membrane. Z>, nucleus, filled with karyolymph. E, nuclear reticulum, composed of 
linin and chromatin. F, plastid. (?, metaplasmic inclusion. H, chondriosomes. /, 
vacuole. J, tonoplast or vacuolar membrane. K, cytoplasm. L, ectoplast. 

^Description of the Cell. The morphology of the cell will here be 
sketched only in its barest outlines, by way of introduction to the detailed 
descriptions presented in the subsequent chapters. 

The two most constant components of the cell (Fig. 1) are th.e 
cytoplasm, in which the other cell organs are imbedded, and the 



s, which at least in many respects is the most important of these 
organs. 1 

The cytoplasm, a more or less transparent, viscous, granular fluid, 
may, with its inclusions, occupy the whole volume of the cell. This is 
generally true of animal cells and the younger cells of plants. If the 
cell is vacuolate, as is usually the case in the mature plant cell, the 
cytoplasm may constitute only a thin layer lining the wall, the central 
vacuole with its cell sap often far exceeding it in volume (Fig. 2, C). 

FIG. 2. 

A-C, diagram of a plant cell in three stages of development: the vacuoles increase in 
volume and the protoplasm becomes limited to the parietal region. D, cell of stamen hair 
of -TradeHcantia, showing streaming movements in the cytoplasmic strands. E, paren- 
chyma cell from cortex of Polygonella, showing nucleus, plastids, and scanty cytoplasm. 

In many cases the cytoplasm forms a system of anastomosing strands that 
often show active streaming (Fig. 2, D). Externally the cytoplasm is 
limited by a layer of different consistency, the plasma membrane, or 
ectoplast. Where it comes in contact with the enclosed vacuole it is also 
limited by a membrane, the vacuole ^ membrane^ Q^j8^lQ&t. 

The nydeM is bounded by a m&skffr wsmhrane. and contains an 
extremely clear fluid, the yuc^T sn -p { n y, ^ /ir wlVM&fr In the karyo- 
lymph is imbedded the nuclear reticulum, composed usually of linin, an 
achromatic supporting material, and chromatin, the " nuclear substance 
par excellence." One or more true nudeolL or plasmosomes. are commonlv 

, . ,, , , *+*tSS**rs" , -* LTfemuaiitjiMiu ^ ry * . , . f 

present m the nucleus, and may ior may not be closely associated with 
the reticulum. There are often present also (foomatin nucleoli^rjcqryo- 
somes^ which represent accumulations of chromatin at certain points on) 
the reticulum, and should not be confused with the true nucleoli. * ' 

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


There are usually plastids of one or more kinds in the cytoplasm, 
the most conspicuous irt plant cells being the green chloroplasts. 

A centrogome. is present in the majority of animal cells and in those of 
certain lower plants. It may occupy the center of a visibly differentiated 
region, the centrosphere ^j^acJ,JQw sphere, and at the time of cell- 
division is the focus of a conspicuous system of radiating astral ro^s, 
collectively known as the astet, 

Chondriosomes have now been demonstrated in the cells of nearly all 
plant and animal groups. These are minute bodies having the form of 
granules, rods, or threads, and apparently constitute a group of materials 
having various functions. 

Metaplasmic inclusions are accumulations of food materials and 
differentiatiorr M pr6ducts that arc relatively passive. These non-proto- 
plasmic bodies may exist in the form of droplets or crystals, and those 
which are not transitory or reserve food materials apparently play a very 
minor rdle in the life of the cell. 

Strictly speaking, the c^4oZi-as at present understood is not a part 
of the cell proper, or protoplast, but is rather regarded by many as a 
secretion of the latter. In many cells, particularly those of animals and 
the motile cells of algae and flagellates, it may be absent. 

The foregoing is a bare sketch of the general structure of a "typical" 
cell. 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 v ^immic_ system, in a constantly changing state of molecular 
flux, its constitution at any given moment being dependent upon ante- 
cedent^states and upon environmental conditions. As stated by Moore 
(1912), "the living cell may be regarded, from the physico-chemical 
point of view, as a peculiar energy transformer, through which a continu- 
ally varying flux of energy ceaselessly goes on, and the whole life of the 
cell is an expression of variations and alterations in rates of flow of 
energy, and of swings in the balance between various forms of energy." 
In the words of Harper (1919), the cell is a colloidal system in which the 
various processes have become progressively localized in certain regions, 
with the resulting formation of organs, which, with the increasing con- 
stancy of the processes involved, have come to possess a permanence 
and individuality of their own. In view of the spatial relationship and 
definite physiological integration of the various components of the cell, 
we are to look upon the cell not as a mercf mixture of complex substances, 
but as a definitely organized system, y 

The Differentiation of Cells. It is a striking fact that in spite of 
many minor variations the fundamental structure of the cell is essentially 
similar in nearly all living organisms, and in all the kinds of tissues 
which go to make up the body of any one of them. As Harper (1919) 
remarks, "evolution as we know it has not consisted in the production 


of new types of protoplasmic structure or cellular organization, but in 
the development of constantly greater specialization and division of 
labor between larger and larger groups of cells. " One obvious reason for 
the fundamental similarity of the cells of widely different tissues is found 
in the fact that all of them are derived by progressive modification from 
relatively undifferentiated " embryonic " or " meristematic " cells during 
the course of the ontogeny. In a young vascular plant, for example, 
definite regions (memcems) consisting of such cells are present in the 
root tip and stem tip, and, at a later stage of development in many 
cases, in the cambium also. As a general rule these meristematic cells 
are without large vacuoles or other conspicuous products of differentiation, 
and are separated by no intercellular spaces. They undergo successive 
divisions very rapidly (hence the use of root tips for the study of mitosis); 
and while some of the products of division become greatly modified in 
structure in connection with their specialization in function, others 
retain their embryonic or meristematic character and continue to produce 
new cells from which new tissues are built up throughout the life of the 

In the bryophytes and pteridophytes the meristematic activity of the 
apex (root tip or stem tip, or apical region of thallus) usually centers in 
a single " apical cell " of definite shape, which cuts 
off segments (daughter cells) from its various faces 
with great geometrical regularity. In the Mar- 
chantiales and Anthoceros the apical cell is cuncate 
(wedge-shaped) and forms segments from four of 
its faces; in the anacrogynous Jungermanniales 
it is sometimes cuneate but more often dolabrate 
(ax-shaped) and produces segments from its two 
lateral faces; and in the acrogynous Jungermanniales 
and mosses it has the form of a triangular pyramid, 
cutting off segments from its three lateral faces. 
This last type is found also in the pteridophytes: _, ^^ .. ,. . 

J ^ . , FIG. 3. -Longitudinal 

in the stem tip it produces segments from its three section of the root tip of 
lateral faces, whereas in the root tip, in addition Omunda, showing the 

' . > f . triangular pyramidal 

to these three series of segments, it cuts off from its apical c 5 eii. x 144. 
distally directed face a fourth series, which becomes 
the tissue of the root cap (Fig. 3). In the higher vascular plants there 
is no single cell characteristically different from the others of the apical 
meristematic group. 

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; strictly speaking, 
such characters are histological rather than cytological. Thus we have, 
besides meristematic and little modified parenchymatous cells (Fig. 2, 



E), a number of other types, such as tracheids, vessels, wood fibers, 
selcrenchyma fibers, and sieve tubes (Fig. 4), all of which are characterized 
by the peculiar ways in which their walls become modified through sec- 
ondary and tertiary thickenings, and by the form and arrangement as- 
sumed by the pits. (See p. 191.) The protoplasts may finally disappear 
completely from wood cells, leaving a tissue or framework composed of 
lifeless cell walls. 

FIG. 4. Differentiated cells from vascular plants. 

A t 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 t face view of sieve plate shown in section in E. 

All of this variety of form and structure is conditioned by varied 
functional activity on the part of different protoplasts: in the process of 
cell differentiation morphological and physiological changes stand in the 
closest relationship. All functional differences are accompanied by 
chemical or physical differences of some sort in the protoplasm, but it 
is mainly in the non-protoplasmic inclusions and secretions (including 
the wall) rather than in any conspicuous structural changes in the 
protoplast 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 differentiation (see p. 133), 
protoplasts performing widely different functions may appear much alike. 

Structural differentiation in connection with division of labor is very 
striking in animal cells, which are destitute of such walls as plant cells 
possess. The muscle cell shows many fine longitudinal fibrillse which 
have to do with the cell's power of contractility. In certain muscles 
these fibrillas are so segmented that the whole cell, or muscle fiber, has a 
transversely striped appearance (Fig. 5, F). The nerve cell (Fig. 5, 



FIG. 5. Nerve and muscle cells of animals. 

A, diagram of a typical neuron: a, axis cylinder process or axon, ending in arborescent 
system; d, dendrites. (After Obersteiner and Hill.) B, cell from human spinal cord, 
X 75. (After Obersteiner and Hill.) C, nerve cell from the eye. (After Lenhosstk.) D. 
Nerve cell from the 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.) 

FIG. 6. 

A, connective tissue from the jelly fish, showing branching cells and elastic fibers 
imbedded in gelatinous matrix. (After Lang.) B, cells of hyaline cartilage imbedded 
in their secretion. (7, blood cell from chick embryo. 



A-D) typically possesses a single unbranched prolongation (axori) and 
one or more others (dendrites) which often become very elaborately 
branched, especially in the ganglion cells of the spinal cord and brain. 
The cytoplasm of the nerve cell contains fine fibrils, and also granules 
of chromatic "Nissl substance.'' Cells specialized in connection with 
motility such as spermatozoa (Fig. 103) and the cells of certain epithelial 
tissues (Fig. 36), show complex structural modifications not only in the 
fliigelhe, cilia, and cirri which they bear (p. 45), but also in the other 
coll organs with which the activities of these motile structures are closely 

FIG. 7. Paramccciiim caudal um. Semidiagrammatic figure showing principal parts. 
C. V., contractile vaeuoles. T, trichocyst. AT, n, mega- and rnicronuclei. P, peri- 
stomial groove. M, mouth. O, O3.sophagus, with undulating membrane, U. M. F. V., 
food vacuoles. (After Lang.} 

connected. (See Chapter IV.) Secretory cells are often distinguishable 
not only by the accumulations of secretion products in their cytoplasm, 
but also by the peculiar forms assumed by their nuclei (Fig. 17, A, C). 
The cells of connective tissue (Fig. 6, A) form many long interlacing pro- 
cesses and lie in a supporting matrix which represents their secretions. 
Cartilage and bone cells (Fig. 6, ) are likewise imbedded in their secre- 
tions, which are here produced in relatively enormous amounts and, where 
present, constitute the main supporting framework of the body. 

We thus see that the life of the complex multicellular organism is 
dependent upon the correlated activities of a multitude of cells per- 
forming many diverse special functions. It is a remarkable fact that 


all of the functions delegated, as it were, to different cells (contractility, 
motility, mechanical support, the reception and conduction of stimuli, 
secretion, and excretion), as well as those general functions common to 
all cells (nutrition and reproduction by division), may in the protozoa 
and protophyta be carried on within the limits of a 'single cell. Such a 
cell as, for example, the body of a Paramcecium (Fig. 7), exhibits a cor- 
responding regional differentiation in structure, certain functions being 
localized in definitely developed organs. Differentiation is therefore 
something which, fundamentally, does not require multicellular struc- 
ture for its expression; in fact the most important single step ever taken 
m differentiation was that which set apart nucleus and cytoplasm, giving 
the type of organic unit common to all subsequently evolved organisms. 
It is further evident, however, that the evolution of the higher organisms 
has unquestionably been very largely conditioned by the multicellular 
state, and has involved a progressive division of labor in a very real sense. 
The many functions of a single cell have become distributed among a 
number of cells in such a way that there has been produced a harmonious 
whole which is efficient, adaptable, and progressive to a degree not other- 
wise attainable. 

Bibliography 2 

See Bibliography I A for general works on the cell and for reviews of early cell 
literature. For the latter see especially the works of Bovori, Flemming, Koernieke, 
Mark, Meves, Riickert, Waldeyer, Whitman, and Zimmermann. Other works 
referred to in Chapter II: 
HANSTEIN, J. 1880. Das Protoplasrna als Triigcr der pflanzlichcn und thierischen 

Lebensvorrichtungen . Heidelberg . 

HARPER, R. A. 1919. The structure of protoplasm. Am. Jour. Bot. 6: 273-300. 
MOORE, B. 1912. The Origin and Nature of Life. N. Y. and London. 



In his famous essay on protoplasm in 1868 Huxley very fittingly 
Inferred to., it as u the physical ba^is of life." With a realization of the 
full significance of this phrase there comes the conviction that protoplasm 
is the most interesting and important substance to which we can turn our 
attention, for with it the phenomena of life, in so far as we know them, 
are invariably associated. 

In spite of the enormous amount of work which has been done upon 
protoplasm during many years, our knowledge of it must still be regarded 

We can scarcely yet say definitely 

that a given kind of protoplasm is not a single complex chemical com- 
pound, as is held by one prominent school of biochemists: all ordinary 
analysis seems to indicate that it represents a somewhat looser combina- 
tion of substances, many of which are in turn very elaborate in composi- 
tion; and further that these substances probably differ from those found 
elsewhere not in any fundamental manner, but only in the degree of their 
complexity. (Proteins, fats, crystalloids, water, and other compounds 
make up protoplasm, but protoplasm is not a mere mixture of these 
materials; it is organized it is a system of complex substances, the 
activities of which are fully coordinated.} Only if we recognize in pro- 
toplasm an organization can we conceive of it as a physico-chemical 
substratum for those peculiar orderly activities characterizing living 
substance, namely, synthetic metabolism, reproduction, irritability, and 
adaptive response. 

Physical Properties. Certain early ideas regarding the physical 
nature of protoplasm may be briefly reviewed at this point. 

Protoplasm appeared to its earliest observers merely as a colorless^ 
viscid substance containing minute granules. Two general opinions 
soon developed: some held that protoplasm consists of but a single fluid, 
whereas others regarded it as a combination of two fluids. Briicke 
(1861), who was one of the first to lay emphasis on the fact that pro- 
toplasm is an organized Substance, looked upon the cell body as a con- 
tractile, semi- solid material through which there streams a fluid carrying 
granules. Similar to this was the idea of Cienkowski (1863),, who be- 
lieved he saw ii\ the protoplasm of myxomycetes two fluids, one of them 
hyaline and only semi-fluid (the "ground substance")* and the 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 sub- 
stance, contractile throughout, but showing many local differences due to 
varying water content. To this general view the work of Hanstein 
(1870, 1880, 1882) lent support. 

Much more prominent have been the structural theories associated 
with the names of Klein, Flemming, Altman, and Biitschli, and known 
j-espectively as the "reticular," "fibrillar," "granular," and "alveolar" 

The reticular theory, which was formulated by Fromman (1865, 
1876, 1884), was developed especially by Klein (1878-9) and supported 
by van Beneden, Carnoy, Leydig, and others. These workers saw in 
protoplasm & reticulum or fine network of a rather solid substance 
(spongioplasm) , which holds a fluid and granules in its meshes/) This 
view was adopted for a time by Strasburger. 

The fibrillar, or filar, theory, announced by Velten (1873-6) 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 22iita2i6Jind the 
fluid bathing them paramitome. Some observers asserted that the fibrils 
are in reality minute canals filled with a liquid, the granules seen by 
others being merely sections of these canals. An extreme view was that 
of Schneider (1891), who thought the entire cell might consist of but a 
single greatly convoluted filament. 

To the followers of the reticular and fibrillar theories the fluid held 
between the fibers was known variously as ground substance, enchylema 
(Ha-nstein 1880), hyaloplasma (Hanstein), paramitome, and inter-filar 
substance. The granules were known generally as microsomes (Hanstein). 

^According to the granular theory protoplasm is a ^compound oL in- 
numerable minute granules which^ alone form the essential active basis for 
the phenomena exhibited; the observed fibrillar and alveolar structures 
are of secondary importance. Martin (1881) held that fibrils and net- 
works are due entirely to certain arrangements of these granules, or 
microsomes. Pfitzner (1883) pointed out that the granules are semi- 
solid and float in a more fluid ground substance. For Altman (1886, etc.), 
who was the most prominent exponent of the theory, the granules were 
actual elementary living units, or bioplasts, the liquid containing them 
being a non-living hyaloplasm. The cell was therefore looked upon not 
as a unit, but as an assemblage of bioplasts, "like bacteria in a zooglcea," 
and the bioplasts were believed to arise only by divisk 
(omne granulum e granulo!}. 

The alveolar theory, also known as the emulsion, or foam, theory, was 
elaborated principally by Biitschli (1882, etc.), and is of special interest 
in View of our present-day notions of protoplasmic structure. According 


to Blitschli protoplasm consists of minute droplets (averaging I/A 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. Butschli supported his theory 
by making artificial emulsions with soaps and oils which showed amoeboid 
movement and other striking resemblances to living protoplasm. 

The above four theories have been termed "monomorphic theories," 
for the reason that each of them stated that protoplasm has a single 
characteristic physical structure. Strasburgcr in 1892 and thereafter 
maintained that the protoplast is regularly composed of two portions; 
an active fibrillar kinoplasm, concerned primarily with the motor work of 
the cell, and a less active alveolar trophoplasm, chiefly nutritive in func- 
tion. It was shown by von Kolliker, Unna (1895), and others, moreover, 
that one type of structure may be transformed into another. Flemming 
later adopted the view that no single type characterizes protoplasm, but 
that the latter may be homogeneous, alveolar, fibrillar, or granular 
i.e., it is " polymorphic." Wilson (1899) found that all four states are 
successively passed through in the echinoderm egg. This observation, 
which was made upon both living and fixed material, showed in a striking 
manner the colloidal nature of protoplasm (see below), since it is now 
known that colloids may assume very diverse structures under the in- 
fluence of changing environmental conditions. The work of A. Fischer 
(1899), who treated non-living proteins with cytological fixing reagents 
and so produced artifacts similar to alveolae, reticula, and granules, should 
make one cautious in drawing conclusions regarding protoplasmic 
structure from fixed material. It should be understood that the only 
trustworthy observations are those which are made at least in part on 
living material, for it is not difficult to discover all four types of struc- 
ture in prepared slides: the protoplasm has there been coagulated by 
fixing reagents, and we know that in the coagulation of such substances 
as compose protoplasm an entirely new structure may be assumed. 

Protoplasm as a Colloidal System. For adequate reasons it is now 
customary to speak of protoplasm in terms of the physics and chemistry 
of colloids. Colloids are those glue-like substances which are uncrystal- 
line, semi-soird, an3~very slightly~br~ riot at "all osmotic. They have a 
highlmrf ace 'tension,' coagulate readilj, and conduct the electric TfUffenfT 
V^iy^pOt^^ Heterogeneous sytems, i.e., they consist 

essentially of particles larger than molecules of a substance or substances 
m a medium of dispersion which may be water or some other fluid" 
(Child 1915 1 )- The particles range in size from those visible to the riated 

1 These paragraphs on colloids are based largely upon the convenient summary 
given by Child (1915, pp. 20 ff.). See also Czapek (19116), Bayliss (1915), Hatschek 
(1916), Bechhold (1919), and Robertson (1920). 


eye down to single molecules and ions. Ijn.thelatterjcase we hjiye a.true, 

sotutionTBeTween colloid and crystalloid the line of demarcation is thus a 
purely arbitrary one. In many cases the suspended particles are too 
small to be seen with the ordinary microscope, which will not render 
visible a body with a diameter less than about 0.20 to 0.25 jw; but with 
the ultramicroscope, which will reveal particles about one-fortieth of 
this size, they may be clearly seen. Again, the ultramicroscope is insuffi- 
cient in the case of certain colloids, in which the presence of suspended 
particles can still be shown, however, by the Tyndall effect (a milky 
appearance when a beam of light is passed through them). Most proto- 
plasmic colloids are of tjiis last type. I 

In a colloidal solution the particles are. separata .from., one .another, 
(sol), whereas in the denser "set" condition (gel) they are more closely 
aggregated and hence not free to move upon one another. A colloid 
may be made to pass from the sol to the gel state or vice versa; in some 
cases this change is reversible, but in others it is not. 

Colloids are usually classified as suspensoids and emulsoids. Sus- 
pensoids, in which the particles are solid, are comparatively unstable; 
are readily precipitated or coagulated by salts; carry a constant electric 
charge of definite sign; are not viscous; do not show a lower surface 
tension than that of the medium of dispersion alone; and are mostly 
only slightly reversible. Emulsoids, in which the suspended particles 
are fluid, are comparatively stable; are less readily coagulated by salts; 
are either positively or negatively charged; are usually viscous; have a 
lower surface tension than the medium of dispersion^ form surfacfe mem- 
branes; and are highly reversible. Most organic colloids are emulsoids, 
and there can be no doubt that many of the characteristics of living or- 
ganisms are due to their presence. 

In an emulsion each physically homogenous constituent is known as 
a phase. In mayonnaise dressing, to cite a familiar example, there are 
three phases: a water phase, consisting of water and substances dissolved 
in it; an oil phase; and a protein phase (egg). These three physically 
diverse substances are brought into the emulsified state by beating; one 
of them is the medium of dispersion (external phase) and the others 
(internal phases) are suspended in it as liquid particles or droplets. In 
such an emulsion a given phase usually consists of more than one chemi- 
cal substance: the water phase, for example, is not pure water, butjan 
aqueous solution of salts and othef water-soluble substances. These dif- 
ferent chemical substances, including the solvent* which make up a single 
phase, are known as components. 

It is $iown by certain investigators (Bancroft, Clowes) that the drop- 
lets of a suspended phase in a stable emulsion are bounded by films of 
different constitution : between the Aliases of an alkaline water-oil emul- 
sion, for example, there appear to be delicate films of a soapy nature. 


These films not only prevent the coalescence of the droplets, but also, 

through alterations in surface tension, influence the transposition or 
inversion of phases which occurs under certain conditions, whereby the 
suspended phase becomes the medium of dispersion and vice versa (Fig. 
8). Such inversion probably plays an important role in many cases of 
transformation of sol into gel and of gel into sol. 

FIG. 8, Diagram of a colloidal emulsion, illustrating transformation of emulsion of oil 

in water to emulsion of water in oil. 

A, aqueous phase. B, oil or other non-aqueous phase. C, surface film of soap or other 
dispersing agent. (After Clowes, 1916.) 

The properties and behavior of colloidal substances in general appear 
to be due primarily to the enormous extent of the reacting surface be- 
tween the constituent phases which results from the finely divided state 
of one or more of them. In the accompanying table is shown the amount 
of surface which a given mass of matter may expose when subdivided 
into successively smaller particles. 


: Length of edge of cube 

Number of cubes 

Total surface exposed 


1 cm. 


6 sq. cm. 

1 mm. 


60 sq. cm. 

100 M 


600 sq. cm. 


10 9 

6,000 sq. cm. 


10 12 

6 sq. m. 



60 sq. m. 



600 sq. m. 


10 21 

6,000 sq. m. 

The evidence at hand supports the view that protoplasm is essentially 
a colloidal^solution of the emulsion type. It consists of at least three 
principal phases: a water phase, containing a number of dissolved compo- 


nents; a fat phase, consisting of fats and fat-soluble components; and a 
complex protein phase. Since the water phase is here the medium of 
dispersion protoplasm is classed as a "hydrosol" in its ordinary state, 
or as a "hydrogel" in the set condition. There are doubtless additional 
minor phases present, protoplasm being in reality a "complex polyphase 
colloidal system. " 

The presence of water in protoplasm is a matter of fundamental im- 
portance. As emphatically stated by Henderson (1913), " . . . the 
physiologist has found that water is invariably the principal constitu- 
ent of active 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 kidneys, lungs, and sweat glands]. 
Indeed, as clearer ideas of the physico-chemical organization of proto- 
plasm have developed it has become evident that the organism itself is 
essentially an aqueous solution in which are spread out colloidal sub- 
stances of great complexity [Bechhold 1912]. As a result of these condi- 
tions there is hardly a physiological process in which water is not of 
fundamental importance" (pp. 75-77). 

The amount of water in protoplasm varies greatly under different 
conditions, Jnit L normally _it is present in large proportions. It makes up 
85 to 95 per cent of the weight of actively streaming protoplasm such as 
is seen in Elodea and 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, in which case the protoplasm becomes very 
viscous. The percentage differs constantly in different parts of the cell; 
nucleus, cytoplasm, and plastids, though all are composed primarily of 
protoplasm, contain very different amounts of watgrjl Since active pro- 
toplasm is a liquid, the phenomena of surface tension and other properties 
of liquids v must enter largely into explanations of its behavior. 

The colloidal nature of protoplasm is manifested in many of its prop- 
erties. Its power of adsorption, which lies at the basis of many cell 
reactions and certain staining processes, is similar to that of other 
colloids, protoplasm, like other colloids, is semi-permeable: a semi-per- 
meable region is probably present wherever protoplasm comes in contact 
with other substances, such as water; and the permeability of a vacuolate 
cell is in general the resultant of the permeabilities of the ectoplast, 
cytoplasm, and tonoplast. 

Protoplasm shows most strikingly its colloidal character in the changes 
of physical state which it undergoes as the effects of variations in the 
external conditions. The alterations due to changes in temperature will 
serve for illustration. Above a certain temperature the colloid gelatin 
exists in the sol state it is a hydrosol. If the temperature is sufficiently 


lowered the gelatin "sets" it becomes a hydrogel. This setting is a 

reversible process: if the temperature is again raised the sol state is 

resumed. On the contrary, egg albumen is a hydrosol at ordinary 

temperatures and becomes a hydrogel when heated; in this case the 

change is an actual coagulation and is not reversible. Many of the 

colloids of the cell are of this non-reversible type. "The evidence that 

in this colloidal condition the transition from liquid to solid, from 

sol to gel, tends especially to pass into an indefinite series of gradations 

gave a basis for the explanation of that mixture of the properties of solids 

and liquids which has puzzled students of protoplasm" (Harper 1919). 

Protoplasm is thus easily coagulated, not only by a high temperature, 

but by a variety of chemical substances. The "fixation" of the cell 

structures by the reagents employed in cytological technique is primarily 

a coagulation phenomenon, and in the act of coagulation a substance, 

especially one as complex as protoplasm, undergoes an alteration in 

physical structure. Although such fixing fluids preserve very well the 

general structure of the cell, the effects of coagulation should always be 

borne in mind in interpreting finer details in preparations of fixed cells, 

and in evaluating the results of those who have made special studies on 

the ultimate structure of protoplasm. ^ 

Microdissection. Much has been added to our knowledge of tho 
physical nature of protoplasm in recent years through microdissection. 
Certain workers, notably Barber (1911, 1914), Kite (1913), Chambers 
(1914, 1915, 1917, 1918), and Seifriz (1918, 1920) have developed a 
technique (fully described by Barber 1914, and Chambers 1918) whereby 
they have been able to dissect living cells under the high powers of the 
microscope, thus opening a most promising field for investigation. Kite, 
working on the cells of several plants and animals, found that protoplasm 
exists in the form of sols and gels of varying consistency, that of plant 
cells being as a rule more dilute and less rigid than that of animals. The 
cytoplasm is commonly somewhat more viscous than is usually thought, 
having the consistence of a "soft gel," while the nucleus may often be 
surprisingly firm. (See Chapter IV.) 

Chambers (1917), who gives a convenient bibliography of the subject, 
states that in the early germ cells and eggs of certain animals the proto- 
plasm is in the sol state with a surface layer in the gel state, whereas 
adult cells are usually gels. He further asserts that the surface gel is 
readily regenerated after injury, a new gel film being formed over the 
injured area. As regards the structure of protoplasm, he finds it to 
consist of a hyaline fluid carrying microsomes and macrosomes, which 
measure less than 1/z and from 2-4ju in diameter respectively. Upon dis- 
organization the macrosomes, which are more sensitive to injury than 
are the microsomes, swell and go into solution, while the hyaline fluid 
flows out and mixes with water or coagulates, forming a reticular or 
granular structure. 


Seifriz (1920) has investigated with care the viscosity of the proto- 
plasms of a number of myxomycetes, algae, pollen tubes, protozoans, 
and echinoderm eggs. He finds the degree of viscosity to vary widely, 
from a very watery to a fairly rigid gel condition, not only in the different 
organs of the cell but also in the protoplast as a whole at different stages 
of its development. He warns against accepting viscosity alone as an 
index of the gel or sol state of the protoplasm, since it is physical structure 
and not viscosity which determines these states in an emulsion. 

It is to be hoped that the methods employed by the above investi- 
gators will be further developed and applied more widely, for through 
them many misconceptions will undoubtedly be corrected. 
It should be evident from all these considerations that there is prob- 
ably no sinlge visible structure characteristic of protoplasm at all times. 
Any fundamental structure which it may have remains to be discovered 
in the ultrarnicroscopic constitution of the colloids and other materials 
of which it is composed, and in the physical relations which these bear 
to one another. It should be pointed out, however, that in the idea of 
protoplasm as a complex colloidal emulsion we have the best hypothesis 
yet offered as a basis for the interpretation of the behavior of living 

/ Chemical feature of Protoplasm. Chemically, as well as physically, 
protoplasm is exceedingly complex, and {He study of its constitution has 
opened a field of research which is continually broadening. Only a brief 
summary of some of the more important chemical facts can be presented 
here; for more detailed accounts special works on the subject must be 
consulted. 1 

As already pointed out, the substances of which protoplasm is com- 
posed are probably not fundamentally different from those found else- 
where, but show rather a greater complexity and a high degree of 
organization. Protoplasm is an intricately organized system of water, 
proteins, enzymes, fatty substances, carbohydrates, salts, and other 
minor constituents. The often cited analysis by Reinke and Rodewald 
(1881) of the myxomycete Mthalium septicum (Fuligo) showed the proto- 
plasm of this form to have the following composition : 


Proteins 40 Cholesterin (lipoid ) 2.0 

Albumins and enzymes 15 Ca salts (except CaCOa) 0.5 

Other N compounds 2 Other salts 05 

Carbohydrates 12 Resins 1.2 

Fats 12 Undetermined 6.5 

The protein matter of protoplasm exists in relative complex forms. 
"The chief mass of the protein substances of the cells does not consist of 

1 See especially the books of Hammarsten (1909), Wells (1914), Czapek (1915), 
Bayliss (1915), Mathews (1916), Palladia (1918), Robertson (1920), and the review by 
Zacharias (1909). 



protcids 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 beginning with the pioneer work 
of Miescher, Hoppe-Seyler, and Reinke, have shown that these nucleo- 
proteins are essentially combinations of nucleic acid with proteins, 
sometimes with the simpler his tones or the still simpler protamines. 

The nucleus as a rule is free from or very poor in uncombined carbohy- 
drates, fats, and salts, but is characterized rather by the abundance of a 
nucleo-protein called nuclein, isolated in 1871 by Miescher, who gave it the 
formula C29H 4 9N9P3O22. It was shown by Altman (1889) that nuclein, 
like the other nucleo-proteins, could be split into two substances: nucleic 
acid and a form of albumin (protein), the two existing in chemical com- 
bination like an ordinary salt. Nucleic acid from yeast was given the gen- 
eral formula CioHsgNuC^ 2P2Oo, and that from fish sperm C^HseNnO 
i 6 2P 2 O 5 . Nucleic acid was further analysed into phosphoric acid and 
certain bases. The relation of these simple substances to nuclein, and 
also the relation of nuclein to more complex nuclco-protcinsjare shown in 
the following scheme (mainly from Wells) : 





(albumins, etc 


Phosphoric acid 

Nucleic acid 

f Levulinic acid 
i Purin bases 
1 Py rim id ins 



I Pentoses 

The nucleo-proteins of the nucleus (chromatin) contain very little of 
the protein constituent and are thus relatively rich in phosphorus. 
Glaser (1916) accordingly speaks of chromatin as "a conjugated phospho- 
protein group with a nucleic acid group, the latter group being a complex 
of phosphoric acid and a nuclein base." Kossel (1889, 1891, 1893) 
even concluded that in certain instances (during mitosis) chromatin 
might be simply nucleic acid. 

In the cytoplasm, on the contrary, the proportion of the protein 
constituents is relatively high. The cytoplasm probably has no true 
nuclein, but is rich in nucleo-albumins, albumins, globulins, and pep- 
tones, which, unlike nuclein, have little 'or no phosphorus. As a result 
its reaction is alkaline, in contrast to the acidity of the nucleus. Accord- 
ing to Hammarsten (1909), "the globulins and albumins are to be con- 
sidered as nutritive materials for the cell or as destructive products in 


the chemical transformation of the protoplasm/' Granules of " volutin " 
formed in the cytoplasm are also looked upon as a food substance used 
by the nucleus in the elaboration of chromatin. 

The fatty components of the cell comprise both ordinary fats and 
lipoids (fat-like bodies not decomposed by alkalis); among the latter 
lecithin and cholesterin are of great importance, particularly in the cells 
of animals. 

The carbohydrates found in protoplasm are chiefly pentoses and 
hexoses, which are as a rule combined with proteins and with lipoids. 
Glycogen exists free in the cells of many tissues and serves as a source of 
heat and energy. The important r61e played by pentosans in the activity 
of the plant cell is strongly emphasized by Spoehr (1919) and Macdougal 
(1920); in fact these authors speak of protoplasm as "an intermeshed 
pentosan-protein colloid." 

Inorganic salts are present in considerable variety, as shown by the 
presence of the following elements in the ash of Fuligo protoplasm: Cl, 
S, P, K, Mg, Na, Ca, Fe. 

Because of their failure to find any new types of chemical compounds 
in their analysis of protoplasm Ileinke and Rodewald (1881) thought it 
probable that the peculiarities of protoplasm are due to its structure 
rather than to its chemical composition. It has since been found, how- 
ever, that certain of the life processes continue for a time after the pro- 
toplasm has been ground up mechanically. Moreover, more refined 
analytical methods have enabled chemists to isolate from protoplasm 
certain extremely complex and unstable proteins (the " protoplasmids " 
of Etard), which differ greatly in degree of cpmplexity, if not otherwise, 
from proteins encountered elsewhere. ^ 

Varieties of Protoplasm. From the foregoing rdsum6 it is plain that 
in protoplasm, because of the many combinations possible among con- 
stituents present in such great variety, we have a substance which may 
exist in a vast number of different forms. When it is further recalled 
that many of the constituents exhibit singly the phenomenon of stereo- 
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 one billion stereoisomers, and some albumins probably 
have more than 700 carbon atoms. Albumin, moreover, is only one of 
many complex substances present in protoplasm. Hence, the state- 
ment that all living cells are composed of the same substance, proto- 
plasm, 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 hydrocolloidal state the protoplasms of different 
organisms vary widely in the relative amounts of these leading con- 
stituents. For example, the lipoids are much more abundant in the 
protoplasm of animals than, in that of plants, and the carbohydrate- 


protein ratio also shows notable differences in the two kingdoms. Ana- 
logous 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 upon the relation of this great 
diversity in the constitution of protoplasms to the amazing variety 
observed among living organisms by Kossel, Reichert, and a number of 
other writers. As Reichert states, the evidence seems to indicate that 
"in different organisms corresponding complex organic substances that 
constitute the supreme structural components of protoplasm and the 
major synthetic products of protoplasmic activity are not in any case 
absolutely identical in chemical constitution, and that each substance 
may exist in countless modifications, each modification being character- 
istic of the form of protoplasm, the organ, the individual, the sex, the 
species, and the genus. " With regard to the integration of the various 
protoplasmic constituents, Mathews (1916) says: "Protoplasm, that 
is the real living protoplast, consists of a gel, or sol, which. is composed 
of the colloids of an unknown nature which include protein, lipin and 
carbohydrate. Whether these colloidal particles consist of one large 
colloidal compound in which enzymes, protein, phospholipin and car- 
bohydrate are united to make a molecule which may be called a biogen 
[Verworn 1895, 1903], cannot be definitely stated, but it seems probable 
that something of the sort is the case." 

The Plasma Membrane.. It was recognized very early that there is 
at the surface of the protoplast a thin layer of relatively resistant, hya- 
line protoplasm which Hanstein called ectoplasm, distinguishing it thus 
from the granular endoplasm within. Pfeffer (1890) employed the cor- 
responding terms hyaloplasm and polioplasm. The ectoplasmic envelope, 
which is best seen on "naked" masses of protoplasm, such as amoebae, 
myxomycetes, and the zoospores and gametes of algae, has been variously 
referred to by different writers as the ectoplast, plasma membrane, Haut- 
schichty and Plasmahaut. 1 

The proponents of the reticular and fibrillar theories of the structure 
of protoplasm looked upon this external layer as a region in which the 
fibrils are more closely compacted or interwoven, whereas Butschli re- 
garded its relative firmness as due to a compact radial arrangement of 
alveolae. Pfeffer (1890) held that such a limiting membrane, which 
living protoplasm always produces on an exposed surface and which 
consists mostly or entirely of protein substances, is not itself truly proto- 
plasmic, whereas the majority of cytologists have thought it to be a 

1 A discussion of ectoplasm and endoplasm based upon a large number of ob- 
servations on Amoeba is given in a new work by Schaeffer (1920). 


special protoplasmic layer: Strasburger, for instance, believed it to be 
composed of kinoplasm. 

The microdissection studies of Kite (1913) and Chambers (1917) 
mentioned above have extended our knowledge of the physical nature 
of the plasma membrane. Both of these observers describe the ecto- 
plast of an Amceba as a concentrated gel. Seifriz (1918), as a result of 
such studies on the Fucus egg and myxomycetes, states that the mem- 
brane is a definite morphological structure, very elastic and glutinous, 
and capable of constant repair. He further asserts that membrane form- 
ation is a physical process dependent upon the physical state of the 
protoplasm and not upon that of the medium, and that it does not occur 
after death. 

That the formation of such a limiting membrane at the surface of 
protoplasm is the result of the tendency of colloidal particles to accumu- 
late on any interface has been pointed out by physical chemists. Citing, 
by way of illustration, the film which forms on the surface of cooling 
milk, Moore (1912) says: "The chief colloid of the milk, on account of 
its affinities, accumulates on the surface, the accumulation gives increased 
concentration, the presence of the increased concentration causes the 
multi-molecules to build together, the larger molecules fall out of solu- 
tion as particles, and these join to form a close network or film." In a 
similar manner the unicellular organism or other mass of naked proto- 
plasm develops its resistant envelope, and the enclosed protoplast of 
the higher plant its ectoplasmic layer and tonoplast. 

Permeability. The physico-chemical nature of the plasma mem- 
brane has been a subject of much discussion among physiologists. On 
the assumption that the permeability of the cell is a case of solubility in 
the ectoplasm, E. Overton (1895, 1899, 1900) developed a theory of the 
constitution of the ectoplast. It was pointed out first, that the ectoplast 
is not miscible with water; second, that in plant and animal cells the only 
bodies which are not miscible with water in the ordinary state are fats and 
oils; third, that the ectoplast is more or less permeable to substances ac- 
cording as the latter are more or less soluble in fats and oils; and fourth, 
that any substance insoluble in another substance will not pass through a 
membrane composed of the latter. It was therefore concluded that the 
ectoplast is made up of some lipoid compound, such as lecithin, which 
acts as a semi-permeable membrane. This theory, though very sug- 
gestive, was effectively opposed by Ruhland (1909, 1915) and a number 
of other investigators, who called attention to many substances which 
do not behave according to the requirements of the theory stated in 
so simple a form. A more nearly adequate conception of the constitution 
of the ectoplast has thus been souhgt. 

Of the more recent theories which have been offered in connection 
with the problem of permeability the most promising are those which 


interpret the ectoplast as an emulsion. According to Czapek (1910, 
1911, 1915) the ectoplast is an emulsion of lipoids, proteins, and other 
substances, the lipoids forming a suspended phase. "Protoplasm is a 
colloidal emulsion of lipoids in hydrocolloidal media, the latter containing 
proteins and mineral salts." Lepeschkin (1910, 1911) advanced the 
contrary view that the lipoids form the medium of dispersion. In at- 
tempting* to account for changes in permeability Clowes (1916) points 
out that inversion of phases probably plays an important role, while 
Spaeth (1916) ascribes changes in permeability to alterations in the 
degree of dispersion of the colloids, with resulting changes in the vis- 
cosity of the membrane. A more definitely stated hypothesis of the 
.latter type is that tentatively suggested by Lloyd (1915) and Free (1918). 
Colloids are known that "have two liquid phases which differ in composi- 
tion only in the relative proportion of water and of the substance of the 
colloid" (Free). It is accordingly possible that 
alterations in permeability may be due to changes 
in the distribution of water between two such 
phases present in the plasma membrane. When 
water passes from the internal (suspended) to the 
external (continuous) phase, the droplets of the 
former would become very small; when the move- 
ment is in the opposite direction they would bo- 
come very large and closely packed. As a result 
there would be such changes in the physical 
cct. X ^L) nature of the membrane as would aid in interpret- 
^ . ing the behavior of the latter toward substances 

Fio. 9. Amceba, show- . .1,1 

in ectoplasm, cndo- entering or leaving the cell. It is held that such a 
plasm, and contractile hypothesis accounts more readily for the gradual 

vacuolc. / ^ . J , 

changes in permeability observed than does the 
inversion theory of Clowes, according to which the change might be ex- 
pected to occur suddenly. It is pointed out, however, that both 
processes are probably involved. 

Whatever the degree of correspondence between the above inter- 
pretations and reality may be, it is scarcely open to doubt, especially 
since the work of Bancroft (1913) and Clowes (1916) on colloids, that in 
such theories we have our best prospect of reaching an adequate knowl- 
edge of the plasma membrane, which, because of its great importance in 
the life of the cell, is to be regarded as a definite "osmotic organ/' 

Protozoa. It is in the Protozoa that the ectoplast shows its most 
elaborate structural differentiations. (See Minchin, 1912, Chapter V.) 
Here the ectoplast clearly has several functions: protective, motor, excre- 
tory, and sensory. In most forms other than the Sarcodina there is a 
resistant envelope of some sort. This may represent (a) the entire ecto- 
plast modified (the "periplast" of Flagellata); (6) a superficial modified 



layer of the ectoplast (the " pellicle " of Infusoria and some Amoeba?) ; (c) a 
secreted layer ("cell membrane ") rather than a modification of the 
ectoplast. In certain cases definite actively protective organs, the tri- 
chocysts, are differentiated in the ectoplasm. 

Among the ectoplasmic structures with a motor function the simplest 
are the pseudopodia; in the larger ones there is a core of endoplasm (Fig. 
9), but the more delicate "filose" ones consist entirely of ectoplasm (Fig. 
10). The flagellum of Euglena was reported by Biitschli to have an elas- 

Fio. 10. Gromia oviformis, 
showing filose-reticulate pseu- 
dopodia composed of ectoplasm. 
(From Minchin, after Schultze.) 

FIG. 11. 

A, flagellum of Euglena, showing endoplasmic core 
and ectoplasmic sheath. ( After Biitschli.) B, Trypano- 
soma tinea, with undulating membrane. (After Min- 
chin.) C, Trypanosoma percce, showing myonemes. (After 
Minchin.) D, flagellum of Euglena. (After Dellinger.) 

tic endoplasmic core with a contractile ectoplasmic sheath (Fig. 11, A), 
but the later figure of Bellinger (1909) represents it as composed of four 
twisted filaments ending within the animal as a system of branching 
rootlets (Fig. 11, D). Cilia, which are short and numerous and show 
rythmic pulsation; cirri, which are formed of tufts of cilia; membranellce, 
representing fused rows of cilia; and undulating membranes, which are 
sheet-like extensions of the ectoplasm (Fig. 11, B), are all essentially 
ectoplasmic organs. A further motor differentiation is seen in the 
minute contractile fibrils known as myonemes, which are analogous to a 



system of muscle fibers (Fig. 11, C). In ciliated forms they run beneath 
the rows of cilia. 

Contractile vacuoles, which exercise an excretory function, originate 
in the ectoplasm, although later they may lie much deeper. 

A sensory function is performed by the "eyespot," which is sensitive 
to light, and also by the flagellae and cilia, which are often receptors of 
tactile stimuli. The eyespot seems in some instances to be plastid-like 
in character, and will be discussed in Chapter VI. 

Protoplasmic Connections. The fine protoplasmic strands (Plasma- 
desmen) connecting many plant cells 'through pores in the intervening 
walls are extensions of the ectoplasm (Fig. 12). Several early workers 

FIG. 1 2. -= Protoplasmic connections in vascular plants. 

A, B, Pinus pinea: cells of cotyledon. X 375. (After Gardiner and Hill, 1901.) C, 
Phytelephas ("vegetable ivory"): endosperm cells with greatly thickened walls (w), 
showing spindle-shaped bundles of connecting strands, m, middle lamella. Semidia- 

suspected the presence of such connections before they were able to see 
them, and even the coarse strands passing through the sieve plates of 
sieve tubes, though often observed, were not well known until the time 
of Hanstein's work in 1864. The finer strands of other plant tissues 
where described in a large number of researches between 1880 and 1900. 
Among these may be mentioned those of Wille (1883) and Borzi (1886) on 
the Cyanophycesp; Kohl (1891), Overton (1889), and Meyer (1896) on 
the Chlorophycese; Hick (1885) on the Fucacese; Hick (1883), Massee 
(1884), and Rosenvinge (1888) on Floridese; and, on vascular plants, 
those of Tangl (1879), Russow (1882), Strasburger (1882, 1901), Goros- 
chankin (1883), Terletzki (1884), Wortman (1887, 1889), Haberlandt 
(1890), Kienitz-Gerloff (1891), Jonsson (1892), Kuhla (1900), Gardiner 
(1884, 1897, 1900), Hill (1900, 1901), and Gardiner and Hill (1901). 

With respect to the origin and development of these connecting 
strands very little is accurately known. Some observers have claimed 
that the pores through which they pass are present from the time the 
primary wall is first formed, no wall substance being laid down at these 
points. Gardiner (1900) believed them to arise directly from the median 


portion of the fibers of the achromatic figure at the close of mitosis. His 
observations were made on the endosperm of Lilium and Tamus. Others, 
on the contrary, have regarded them as secondarily developed structures. 
Their absence from the walls between Cuscuta and Viscum and their 
hosts (Kienitz-Gerloff, Kuhla, Strasburger 1901), and also from many 
cells which glide over one another during growth, is a fact opposed to the 
latter interpretation. Although they have been demonstrated in a 
number of kinds of tissue they probably do not occur so widely as some 
have supposed ; but it may nevertheless be true that in many cases their 
apparent absence is due to the fact that the special methods often neces- 
sary to their demonstration have not been widely employed. 

As to their function, it can scarcely be doubted that they may serve 
to transmit stimuli of one kind or another from cell to cell (Pfeffer 1896). 
Noteworthy in this connection is their presence in tissues of plant parts 
known to be particularly responsive to external stimuli, such as the leaves 
of Mimosa (Gardiner 1884) and Dioncea (Gardiner 1884; Macfarlane 
1892), the stamens of Berberis (Gardiner 1884), and the sensitive label] um 
of the orchid, Masdemllia muscosa (Oliver 1888). Their extensive 
development in storage tissues, such as the endosperm of seeds (Tangl 
1879; Gardiner 1897), would also indicate that they are in part responsible 
for the readiness with which nutritive materials are translocated in such 
specialized tissues. 

Vacuoles. Vacuolcs in the cytoplasm are more characteristic of 
plant than of animal cells. They are usually absent in the very young 
cell, but appear as growth and differentiation progress. In case they arc 
very small and numerous the cytoplasm takes on an alveolar appearance, 
but more commonly they coalesce to form one large vacuole which 
may occupy a volume greater than that of the protoplast itself (Fig. 2). 
This condition is characteristic of many mature cells of plants, but is 
comparatively rare in animals. 

The ordinary vacuole is essentially a droplet of fluid, consisting of 
water with differentiation products in solution, surrounded by a delicate 
limiting membrane. DeVries (1885) developed the theory that vacuoles 
are derived from "tonoplasts." The tonoplasts were believed to be 
small bodies imbedded in the cytoplasm and multiplying by fission. 
Through the absorption of water they swell and become vacuoles, the 
vacuole wall thus being made up of the material of the tonoplast body. 
We still refer to the vacuole wall as the tonoplast. De Vries looked upon 
the vacuole as a body with an individuality somewhat similar to that 
of a nucleus, since the tonoplast from which it develops was supposed to 
arise from a preexisting tonoplast by division. The theory was supported 
by certain other workers, but it does not enjoy wide acceptance today 

It has been found by Bensley (1910) and others that there is in the 
cytoplasm of certain comparatively young cells a system of fine canals 



FIG. 13. Cell from root 
tip of Allium cepa, showing 
canaliculte. (After Cham- 

which later open up to form vacuoles (Fig. 13). The fixing reagents 
commonly employed in cytological technique destroy these cancdiculce; 
and since Bensley, by using special reagents, demonstrated such canals 
in the familiar cells of the onion root tip, it is highly probable that they 
occur very widely. It seems more reasonable oo suppose that the fluid 

differentiation produces, when they are first 
forming, gradually come to move along certain 
paths, forming canals, and later accumulate in 
the form of vacuoles, than to suppose that the 
vacuoles originate in such individualized units 
as the tonoplasts of deVries. 

Fluids other than water may also occur in 
the form of vacuoles; oil vacuoles, for example, 
are not uncommon in certain cells. If fats, oils, 
and other products of metabolism take their 
origin in chondriosomes, as some suppose (see 
Chapter VI), it is not improbable that some- 
thing at least analogous to the above mentioned 
tonoplast behavior may occur in the case of 
certain substances appearing in the cell. The cell sap and other 
differentiation products in the cytoplasm will be discussed further in 
Chapter VII. 


Since the true significance of protoplasm was first recognized in the 
middle of the last century many suggestions have been ventured regard- 
ing the nature of the relation existing between life and its physical basis. 
A full discussion of this subject obviously cannot be entered upon here, 
but theories of two types, the micromeric and the chemical, may be 
cited by way of illustration. 

Micromeric Theories. Many years ago there were developed certain 
speculative " micromeric theories" of the constitution of protoplasm; 
these became particularly prominent during the latter half of the nine- 
teenth century. According to these "atomic theories of biology" the 
principle of life was held to reside in ultimate fundamental particles. 
The particles were supposed to be for the most part of ultramicroscopic 
size, capable of independent growth and reproduction, and associated 
like members of a vast colony in protoplasm. Such vital units were 
compared by some to chemical molecules, but they were generally 
regarded as something much more complex. Examples of such units 
were the "organic molecules" of Buffon, the "microzymes" of Bchamp, 
the "physiological units" of Spencer, the " plastidules " of Maggi and 
Haeckel, the "bioplasts" of Altman, the "vital particles" of Wiesner, 


the "gemmules" of Darwin, the "biophores" of Weismann, the " pan- 
gens" of de Vries, and the "ergatules" and " generatules " of Hatschek. 

In a somewhat similar manner a number of the later investigators 
occupied with the study of the ultimate structure of protoplasm have 
often been led to inquire which of the constituents of protoplasm are the 
actually living elements. Among those who viewed protoplasm as a 
reticular structure some held the material of the reticulum to be the true 
living substance, the liquid ground substance, being lifeless, whereas 
others held the reverse to be true. Many of those who saw in protoplasm 
a granular structure regarded the granules as the ultimate living units, 
and more recently there has even been a tendency on the part of some 
investigators (Beijerinck, Lepeschkin), who have emphasized the emul- 
sion nature of protoplasm, to view the droplets of the suspended phase in 
a similar light. To Btitschli the continuous phase was the essential 

By most modern biologists such attempts to assign the principle of 
life to any particular constituent unit of protoplasm or of the cell, whether 
this unit be an observed structural component or a purely imaginary one, 
are regarded as not in harmony with an adequate modern conception 
of the term "living." It has been repeatedly emphasized that life should 
be thought of not as a property of any particular cell constituent, but 
as an attribute of the cell system as a whole (Wilson 1899) ; or, as Brooks 
(1899) put it, not merely as a property but as a relation or adjustment 
between the properties of the organism and those of its environment. 
This recalls Herbert Spencer's characterization of life as a "continu- 
ous adjustment of internal relations to external relations." As Sachs 
(1892, 1895) and others urged, the various elements in the cell should be 
referred to as active and passive rather than living and lifeless. These 
elements play various roles in the cell's activity: each contributes to the 
orderly operation of the whole. When any part fails to function properly, 
or when the proper adjustment is not maintained, the whole system of 
correlated reactions, the resultant of which we call life, must become 
disorganized. As Child (1915) remarks, the theories postulating vital 
units only transfer the problems of life from the organism to something 
smaller; the fundamental problem of coordination is no nearer solution 
than before, and the whole question is placed outside the field of experi- 
mentation. Harper (1919) also points out that modern cytology no 
longer looks upon protoplasm as a substance with a single specific struc- 
ture, or as one made up of ultimate fundamental units of some kind, 
but rather as a colloidal system or group of systems of varying structure 
and composition. "The fundamental organization of living material is 
expressed in the structure of the cell." The cell itself, and not some 
hypothetical corpuscle, is the unit of organic structure. Protoplasm is 
accordingly not made up of structural units arranged in various ways to 


form the cell organs, but is rather a colloidal system in which special 
processes and functions have become localized and fixed in certain regions; 
and this in turn has resulted in the evolution of organs possessing more 
or less permanence. 

Chemical Theories. Much more suggestive, if not conclusive, have 
been certain attempts to place the phenomena of the organism upon a 
purely chemical basis. With the development of organic chemistry from 
the time of Wohler's (1828) synthesis of urea onward there has grown 
up the idea that life processes and chemical reaction not only resemble 
each other but are actually the same fundamentally. When protoplasm 
was subjected to chemical analysis and found to consist chiefly of water 
and proteins, and when these substances became more intimately known, 
the task of explaining the activity of protoplasm in terms of the chemis- 
try of proteins was undertaken. One group of workers developed the 
hypothesis that peculiarly labile protein molecules are responsible for 
the organism's reactions, "death" being primarily a change from the 
labile to the -stable condition on the part of these molecules. Such 
molecules were called "biogens" by Verworn (1903). The molecule 
itself was not thought of as alive, but its constitution was held to be the 
basis of life, which " results from the chemical transformations which its 
lability makes possible. " Accordingly, "life itself consists in chemical 
change, not in chemical constitution" (Child 1915). 

Adami (1908, 1918) contends that life is thus "the function, or sum of 
functions, of a special order of molecules." These ultimate molecules of 
living matter he calls biophores (not to be confused with the biophores 
of Weismann, which were molecular complexes), and he locates them in 
the nucleus, the cytoplasm having merely "subvital" functions. They 
arc proteidogenous in nature, i.e., they compose an active substance 
which takes the form of relatively inert proteins when subjected to 
chemical analysis. The biophore is conceived by Adami to have the 
form of a ring or a ring of rings of the benzene type a ring of amino acid 
radicles with many unsatisfied affinities or bonds. The biophore grows 
in a manner analogous to that of the inorganic crystal : ions and radicles 
from the surrounding medium become attached as side chains to the free 
bonds of the central ring and take on a grouping similar to that of the 
latter; in this way the biophoric molecules are multiplied. Since side 
chains can be detached and new ones of other kinds added, the biophore 
is changeable and may exist in many different forms. Although the 
central ring is thought to be relatively stable and fixed, the variety of side 
chains and their many possible arrangements probably give to each 
species a distinct kind of biophore. On this hypothesis the molecule of 
living matter (biophore) is one "of extraordinary complexity, and in a 
state of constant unsatisfaction, built up by linking on other simple 
molecules, and as constantly, in the performance of function, giving up 


or discharging into the surrounding medium these and other molecular 
complexes which it has elaborated" (Adami 1918, pp. 251-2). "All 
vital manifestations are manifestations of chemical change in proteidogen- 
ous matter, are, in short, the outcome of arrangement of that matter 
with the necessary liberation or storing up of energy" (p. 225). Accord- 
ingly, life is "a state of persistent and incomplete recurrent satisfaction 
and dissatisfaction of ... certain proteidogenous molecules" (1908, 
Vol. I, p. 55). 

Pictet (1918) also associates the phenomena of life with a special 
structure of the organic molecule. Only the arrangement of the atoms in 
open chains, he asserts, permits the manifestation of life and its main- 
tenance; the cyclic structure is that of substances which have lost this 
faculty; and death results, from the chemical point of view, from a 
cyclization of the elements of the protoplasm. 

To the theory that the vital processes are bound up with a special 
form of protein or protein-like molecule many have objected. For 
example, Hober (1911) has contended that there are present in the 
organism only those kinds of proteins which may be formed in the 
laboratory. He urges that life should not be thought of as a single 
process, or as dependent upon any particular kind of molecule, but rather 
that it should be looked upon as the result of many correlated processes 
occurring between many substances under certain conditions. "If we 
accept this idea," says Child (1915, p. 19), "we must abandon the 
assumption of a living substance in the sense of a definite chemical 
compound. Life is a complex of dynamic processes occurring in a certain 
field or substratum. Protoplasm, instead of being a peculiar living 
substance with a peculiar complex morphological structure necessary for 
life, is on the one hand a colloidal product of the chemical reactions, and 
on the other hand a substratum in which the reactions occur and which 
influences their. course and character both physically and chemically. 
In short, the organism is a physico-chemical system of a certain kind." 

Harper (1919) is also opposed to theories based upon the conception 
of protoplasm as a single complex chemical substance, as well as to those 
which hold protoplasm to be a relatively simple two-phase colloidal 
system the alveolar and granular theories, for example. "The crude 
simplicity and general inadequacy of these . . . conceptions . . . 
have done much to bring the whole subject of protoplasmic organization 
into disrepute. On the other hand the conception of protoplasm as an 
aggregate of complex compounds, a polyphase colloidal system or system 
of systems, seems to do much more adequate justice to the observed 

Conclusion. As stated at the opening of the present chapter, it is 
with protoplasm that the phenomena of life, in so far as we know them, 
are invariably associated. The complex behavior of the living organism 


can receive scientific explanation (i.e., be fitted into an orderly scheme 
of antecedents and consequents), if at all, only on the basis of the 
constitution and properties of the materials composing protoplasm; the 
structural organization of protoplasm; the relation of the reactions and 
responses of protoplasm in the form of organized units or cells to the 
environmental conditions; the chain of energy changes occurring in 
connection with all of the organism's activities; and the correlation of 
all these conditions and events. It is largely the effort to account for 
organization and regulatory correlation, and the consequent behavior of 
the complex organism as a versatile and consistent unit or individual as 
something more than a cell aggregate that has led to certain present 
day vitalistic theories, as opposed to those which would hold life to be 
dependent upon " nothing but' 7 the correlated physico-chemical reac- 
tions and interactions occurring in protoplasm. 

Whatever our ultimate judgment in this matter shall be for any 
decision at present is premature it is scarcely to be denied that the 
hypotheses that have thus far been most stimulating to research in 
biological science and most valuable in analysing the data afforded by 
this research are those which seek to formulate vital activity in terms of 
what the physicist for convenience calls matter and energy; and which 
hold life to be not the manifestation of a super-organic, non-perceptual 
entity, or even of a distinct perceptual but hypothetical vital energy, 
but rather the resultant of the many correlated interactions involving 
only energies of known kinds. The way must not be closed, however, 
against possible new categories of energy. The description (reduction 
to order) of our perceptual experience of organic nature, which is the 
primary task of biological science and which has been scarcely more than 
begun, must for the present be made as far as possible in terms applicable 
also to inorganic nature. It is here that achieved results would seem to 
justify the judicious use of a " mechanistic" working hypothesis, whereby 
the attempt is made to " describe the changes in organic phenomena by 
the same conceptual shorthand of notation as suffices to describe inor- 
ganic phenomena" (Pearson). To what extent our ultimate biological 
theory is to show the need of non-mechanical energies or principles will 
depend very largely upon what this scientific description (orderly formu- 
lation) turns out to be like as investigation proceeds, and also upon the 
degree of success with which the physicist will resume the phenomena of 
inorganic nature in mechanical formulae. Thus, as Professor D'Arcy W. 
Thompson forcefully says : 

" While we keep an open mind on this question of vitalism, or while we lean, 
as so many of us now do, or even cling with a great yearning, to the belief that 
something other than the physical forces animates the dust of which we are made, 
it is rather the business of the philosopher than of the biologist, or of the biologist 
only when he has served his humble and severe apprenticeship to philosophy, 


to deal with the ultimate problem. It is the plain bounden duty of the bioloigst 
to pursue his course unprejudiced by vitalistic hypotheses, along the road of 
observation and experiment, according to the accepted discipline of the natural 
and physical sciences. . . It is an elementary scientific duty, it is a rule that 
Kant himself laid down, that we should explain, just as far as we possibly can, 
all that is capable of such explanation, in the light of the properties of matter and 
of the forms of energy with which we are already acquainted. " (Presidential 
address before the Zoological Section of the British Association for the Advance- 
ment of Science, 1911.) 

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FLEMMING, W. 18H2. Zellsubstanz, Kern und Zelltheilung. Leipzig. 
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FHEK, E. E. 1918. A colloidal hypothesis of protoplasmic permeability. Plant 

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FROMMAN, C. 1865. Ueber die Straktur der Bindesubstanzzellcn des Riickenmarks 

Centr. f. Med. Sci. 3. 
1875. Zur Lehrc von der Strtiktur der Zellen. Jenaische Zeitschr. 9. (Other 

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1884. Untersuchangen liber Struktur, Lebenserscheinungen und Reaktionen 

thierischen und pflanzlicher Zellen. Ibid. 17: 1-349. pis. 3. 

GARDINER, W. 1884. On the continuity of the protoplasm through the walls of vege- 
table cells. Arb. Bot. Inst. Wlirzburg 3 : 52-87. 

1897. The histology of the cell wall, with special reference to the mode of con- 
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1900. The genesis and development of the wall and connecting threads of the 

plant cell (Prelim. Cornm.) Ibid 66. 186-188. 

GARDINER, W. and HILL, A. W. 1901. The histology of the cell wall with special 
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GATENBY, J. B. 1919. Identification of intra-cellular elements. Jour. Roy. Micr. 
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1920. The cytoplasm ic inclusions of the germ-cells. VII. The modern technique 
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GLASER, O. 1916. The basis of individuality in organisms. Science 44: 219-224. 


GOROSCHANKIN, J. 1883. Zur Kcnntniss der Corpuscula bei don Gymnospermen. 

Bot. Zeit. 41: 825-831. pi. 7. 
HABERLANDT, G. 1890. Das Roizleitcndo Gewebesystem dor Sinnpflanzen. 


HAMMARSTEN, O. 1909. A Textbook of Physical Chemistry. 5th ed. N. Y. 
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1880a. Das Protoplasma als Trager der pflanzlichen und thierischen Lebens- 

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18806. Einige Ziige aus der Biologic des Protoplasmas. Hanstein's Bot. Abhandl. 

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HARPER, R. A. 1919. The structure of protoplasm. Am. Jour. Bot. 6: 273-300. 
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HENDERSON, L. J. 1913. The Fitness of the Environment. New York. 
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Pinus sylveslris and other allied species. Proc. Roy. Soc. London 67 : 437-439. 
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HOBER. 1911. Physikalische Chemie der Zelle und der Gewebe. 3d ed. Leipzig. 
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1881. Physiologische Chemie. Berlin. 
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KASSOWITZ, M. 1899. Allgemeine Biologic. Vienna. 
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KITE, G. L. 1913. Studies on the physical properties of protoplasm. I. Am. Jour. 

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KOHL, F. G. 1891. Protoplasmaverbindungen bei Algen. Ber. Deu. Bot. Ges. 

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KOSSEL, A. 1880. Ueber das Nuclein der Hefe. Zeit. Physiol. Chem. 3, 4. 
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KUHNE, W. 1864. Untersuchungen tiber das Protoplasma und die Contractilitat. 

LECOMTE, H. 1889. Contribution a T6tude du liber des angiospermes. Ann. Sci. 

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It is now half a century since the modern period of 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 
have to many outstanding biological problems, including that of heredity, 
it is largely in nuclear phenomena that cytological interest has con- 
tinued to center throughout the period. The most striking of these 
phenomena form the subjects of several subsequent chapters: at this 
point we shall consider the nucleus only as it appears in the "resting" 
cell, i.e., in the cell not undergoing division. 

Occurrence. The most conspicuous, and in some respects the most 
important of the cell organs is the nucleus. Whether or not we shall say 
that every living cell contains a nucleus will depend upon what we are to 
include under the term. If the chromatin or chromatin-like substances, 
no matter whether distributed throughout the cell in the form of granules 
or aggregated to form a well defined organ, be regarded as constituting a 
nucleus, then it follows that all plant and animal cells normally have 
nuclei. If, however, as certain protozoologists prefer, the term nucleus 
be employed only with reference to a distinctly delimited organ, we must 
regard those lowly organized cells with scattered chromatic material as 
devoid of nuclei, although they possess, as all cells apparently do, material 
which performs at least the nutritive functions of a nucleus. This latter 
type of organization, which is found in certain members of the Protozoa 
and Bacteria, and also some Cyanophycese, will be discussed later on in 
connection with nuclear structure (p. 66) and cell-division (Chapter X). 
In myxomycetes, where simple and primitive conditions might be expected, 
Jahn (1908, 1911) and Olive (1907) have demonstrated the presence of 
definite nuclei showing mitosis and the phenomenon of chromosome 

General Characters. The vast majority of cells have one nucleus 
each. A few exceptions may be noted. In tapetal cells, laticiferous ves- 
sels, the internodal cells of Characese, and certain other cells there are 
often several nuclei arising by the division of one. In the Siphonese among 
green algae (Fig. 14, V) and the Phycomycetes among fungi there are no 
cross walls in the filamentous and much branched vegetative body, so that 




largo numbers of nuclei are associated in one extensive mass of cyto- 
plasm. Such a body is called a ccenocytc, and the ccenocytic condition is 
found in a number of the lower organisms. In the Uredinese (rusts) the 
typical life history is made up of two phases, with uninucleate and 
binucleate cells respectively. Jn certain Infusoria two kinds of nuclei 
are regularly present. Thus in Paramoecium caudatum (Fig. 15) there is 
one small micronucleus which divides by a peculiar form of mitosis, and 
one large meganucleus (macronucleus) which divides amitotically. In 
P. aurelia there are two micronuclei and one meganucleus, whereas in 

FIG. 14. 

V, portion of body of Vauchcria, showing 
cceriocytie condition; nuclei dark and 
plastids in outline. C, portion of body of 
Cladophora, showing semi-coenocy tic- 
condition . 

FIG. 15. Paramwcium can datum un- 
dergoing fission; mega- and micronuclei 
dividing. (From Minchin, after Biltxchli 
and Schewiakoff.) 

Stentor there may be one meganucleus and several micronuclei. In 
general the meganucleus seems to be a storage organ of the cell; it may 
disappear and be replaced by a new one. The micronucleus performs 
the usual nuclear functions. The mammalian red blood corpuscle begins 
its life as a nucleated cell, but later on the nucleus is lost. 

The position of the nucleus in the cell 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-vacuolated cell it ordinarily occupies the center of the cytoplasmic 
mass, whereas 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. In the Cladophoracese (Carter 1919) it is regularly imbedded, 



\ I I 

at least partially, in the chloroplast, and this is true even in cells possess- 
ing a considerable amount of colorless cytoplasm. Its position is also 
related to the functions of the cell : in 
general it lies in the region character- 
ized by the most active metabolism. 
For example, in young growing root 
hairs (Fig. 16, B) and pollen tubes it ~T 
is commonly found where elongation is 
taking place, and in thickening epidermal A The' 1 thickening of 

Cells (Fig. 16, A) it frequently, though the inner wall of an epi 

not always, lies near the wall upon %%*?"* < 
which the thickening material is being root hairs in Pisum 
deposited. This relation opposition to (Aft( ' r "*"*"*> 
function was emphasized in the works 

of Haberlandt (1887) and Gerassimow (1890, 1899, 1901). 
In form the nucleus is typically spherical or ellipsoidal, its 
shape being determined by a number of physical factors. 
Under comparatively uniform conditions, as obtain where a small 
nucleus lies in a relatively large amount of non-vacuolated cytoplasm, 
aj[ spherical shape is assumed because of the phenomena of surface 
tension. Exceptions are often seen in cells with specialized functions. 

FIG. 17. Unusual forms of nuclei. 

A, portion of nucleus from spinning gland of Vanessa urticce, showing irregular form 
and finely divided state of the chromatin. (After Korxchelt, 1896.) B, Spirostomum 
ambiguum, with moniliform nucleus. (After Stein.) C, Nucleus from salivary gland of 
Chironomus: the chromatic material exists as a series of discs in a convoluted thread, which 
ends in two nucleoli. (After Balbiani, 1881.) /), Ch&nia teres, with chromatic granules 
scattered throughout the body. (After Gruber, 1884.) E, Nucleus from root tip of Mar- 
silia, showing concentration of chromatic material in the nucleoius. (After Beryhs, 1909.) 

In the cells of the spinning glands of Pieris and Vanessa (butterflies) 
the physiological conditions result in the assumption of very irregular 
forms whereby the nuclear surface is considerably increased (Fig. 17, A). 
Nuclei seem rather commonly to undergo amoeboid changes in shape; 


such active movement can be directly observed 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 dimensions, come to be 
correspondingly elongated. The nucleus may also be passively forced 
into very irregular shapes by the dense accumulation of starch grains 
and the diminution in the amount of cytoplasm, as in the endosperm 
cells of maize. In Stentor and Spirostomum the nucleus has the form 
of a string of beads (Fig. 17, B). 

In size the nucleus shows a wide variation, ranging in plants from 
the extremely minute nucleus of Mucor, 1^ 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 5ju 
in diameter, they may grow to a large size at certain stages. The primary 
nucleus of Synchytrium, for instance, reaches a diameter of over 60^. 
The majority of nuclei, however, fall between 5/x and 25//.. In spite of 
the wide range in the size of nuclei of different organisms, in a given 
tissue it is comparatively uniform. 

With respect to the physical nature of the nucleus as a whole, the 
researches of Kite (1913) and Chambers (1914, 1917) have shown that it 
ordinarily consists at least in part of a gel of higher viscosity than the 
cytoplasm, often being so firm that it can easily be handled without 
injury by means of the dissecting instrument. This obviously would be 
impossible were the nucleus merely a watery droplet or vesicle in the cyto- 
plasm. The germinal vesicle (nucleus) of the animal egg Chambers 
(1917) finds to be a sol droplet with a gel membrane; if it is pinched in two 
by the dissecting instrument the two halves will reunite if they come in 

The chemical nature of the nucleus has been dealt with in the preced- 
ing chapter. With regard to its electrical properties, the nucleus is 
apparently negative to the cytoplasm. R. S. Lillic (1903) found that 
Free nuclei and the heads of spermatozoa, which are almost entirely 
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. These results have been confirmed by Hardy (1913). 

Nucleoplasmic Ratio. Of more importance than the absolute size 
of the nucleus is the relation of its volume to that of the cytoplasm the 
so-called nucleoplasmic or Kernplasma relation. Many years ago it was 
held by Sachs (1892, 1893, 1895) and by Strasburger (1893) that the size 
of a meristematic cell in a plant, owing to a supposed limitation of the 
sphere of influence of the nucleus, maintains a very definite relation to 
the size of its nucleus. This conception has recently been emphasized 
anew by Winkler (1916), and parallel views have been expressed by 
several zoologists (e.g., Hegner on Arcella, 1919). In the case of certain 


terminal meristems of plants such a rule may well hold 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. 

The nucleoplasmic ratio has figured prominently in discussions of 
the problem of senescence. R. Hertwig in 1889 advanced the theory 
that senescence and natural death arc associated with an increase in the 
relative size of the nucleus. He later asserted (1903, 1908) that the nucleo- 
plasmic relation is self-regulatory within certain limits for each kind of 
cell, exercising thereby a control over many cell activities, including cell- 
division. Minot (1891, 1908, 1913), on the contrary, believed that the 
increase in the relative volume of the cytoplasm, in addition to its differ- 
entiation, is a fundamental factor in senescence and death. Conklin 
(1912), as a result of his work on Crepidula, denied the existence of a 
constant and self-regulatory nucleoplasmic relation, holding rather that 
changes in this relation are not causes of such cell activities as cell- 
division, but are results of the metabolic processes by which such cell 
activities are brought about. Child (1915) points out that in most 
animal tissues there is an increase in the relative amount of cytoplasm 
during senescence, whereas in plants, although the cell enlarges through 
vacuolation, the relative volume of cytoplasm often does not increase. 
He therefore concludes that the nucleoplasmic relation cannot be regarded 
as a universal factor in senescence ; it is rather an indication of the kind 
and rate of metabolism. The differentiation of the cytoplasm, apart 
from its mere change in volume, Child, with many other workers (Minot, 
Delage, Jennings, etc.), regards as a matter of the greatest importance in 
senescence. Further discussion of this subject is deferred to Chapter VII. 

Not only has it been held that there is a certain relation between the 
mass of the nucleus and that of the cytoplasm, whatever the significance 
of this relation may be, but there also seems to be a size relationship 
between the nucleus and its contained chromosomes. In 1896 Boveri 
showed that the size of the nuclei in merogonic echinoderm larvae (see 
p. 325) is dependent upon the number 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 proportional to both. Gates (1909), however, 
adduced evidence to show that this rule is by no means universal. 

Structure. Having reviewed the general features of the nucleus as 
a whole, we may next give attention to its structure, as seen in typical 

The nucleus is bounded by a distinct nuclear membrane. The nature 


of this membrane has been a subject of much controversy. Some have 
regarded it as a precipitation membrane laid down when the newly 
formed karyolymph comes in contact with the cytoplasm at the time the 
daughter nuclei are reconstructed during the closing phases of mitosis, 
while others (Lawson 1903) have interpreted it as merely a denser limit- 
ing layer of the cytoplasm. The above cited work of Kite and Chambers, 
however, leaves no doubt that the membrane is a definite morphological 
structure belonging to the nucleus : although it is at times very delicate, 
it remains intact when the nucleus is pushed and pulled about by the 
dissecting instrument, and is thrown into folds when the karyolymph is 
withdrawn with a pipette. 

Within the nuclear membrane is a series of gels of varying consistency. 
The nuclear sap, or karyolymph, is a highly transparent substance which 
is generally looked upon as homogeneous, although it has been thought 
by some workers (Reinke 1894) to be made up of large, pale "cedamatin 
granules/' It may be in the sol or gel state. Imbedded in the karyo- 
lymph is a network or reticulum, which may be relatively uniform through- 
out the nucleus or only fragmentary and incomplete. It is usually said 
to be composed of a gel substance known as achromatin (Flemming 1879) 
or linin (Schwarz 1887). Supported on the linin reticulum is the chroma- 
tin (Flemming 1879). This highly stainable substance may exist in the 
form of small granules or droplets at the nodes of the reticulum, or 
apparently in many nuclei as a fluid thin enough to distribute itself more 
or less uniformly throughout the achromatic substance. In the latter 
case the whole reticulum appears to be composed of a single unevenly 
stained material, careful examination showing the "chromatic granules" 
and "achromatic support " to be its thicker and finer portions respectively 
(Fig. 51) (GrSgoire and Wyagerts 1903; Gregoire 1906; Sharp 1913, 
1920). According to Kite (1913) the granules in the living nucleus con- 
sist of a very concentrated gel, the supporting reticulum of a somewhat 
more dilute but not at all fibrous gel, and the karyolymph of a gel which 
is the most dilute of all. 

Heidenhain (1894) found imbedded in the colorless linin net two sorts 
of chromatin in the form of granules: oxychromatin, consisting largely of 
plastin, poor in phosphorus, and staining with the acid dyes; and basi- 
chromatin, composed mainly of nuclein, rich in phosphorus, and staining 
with the basic dyes. These two forms of chromatin apparently may 
change into each other by the addition or loss of phosphorus. The peri- 
odic changes in the staining reactions of many nuclei therefore indicate 
changes in the chemical composition of the chromatin, and these in turn 
point to the intimate association of the nucleus with the periodic physi- 
ological processes of the cell. As used by many writers the term oxy- 
chromatin includes also the linin, so that in much cytological literature 
linin and oxychromatin are more or less interchangeable terms, while 


"chromatin" refers to the basichromatin. Oxychromatin appears to be 
closely similar in composition to the achromatic structures in the cyto- 
plasm, such as spindle fibers and centrosornes. The prominent place 
occupied by the nucleus in cytology is due in large measure to the con- 
spicuous behavior of its chromatic substance at the time of cell-division 
and fertilization, topics which are to receive detailed consideration in 
subsequent chapters. 

In many nuclei basichromatin accumulates at certain points in the 
reticulum, forming karyosomes, also called "net knots " and chromatin 
nudeoli. These seem to be masses of surplus chromatin elaborated by 
the nucleus during the resting phase or in some cases chromatin which 
has flowed to these points from the other parts of the reticulum. During 
the next mitosis they are distributed with the rest of .the chromatin. As 
Rosen (1892) long ago showed by his studies of their staining reactions, 
they differ decidedly in composition from true nucleoli, although they 
may closely resemble the latter after treatment with certain stains (iron- 

One or more true nudeoli, or plasmosomes (Ogata 1883), are usually 
present in the nucleus. A single nucleolus is probably characteristic of 
most nuclei ; there are rarely many, and in some cases there is none. The 
nucleolus may be in close organic connection with the nuclear reticulum 
or it may lie entirely apart from it. In composition it consists largely of 
such oxychromatic substances as plastin and pyrenin, or of nuclein well 
saturated with protein (Zacharias). It usually stains with the acid 
dyes: by a proper selection of stains it may, therefore, be distinguished 
from the karyosomes, which, being composed of basichromatin, take the 
basic dyes as a general rule. In structure the nucleolus may appear to 
be homogeneous throughout, like an oil globule; in other cases it has an 
outer envelope of different consistency and staining reaction. Very often 
vacuoles, occasionally containing granules, are present in the interior. 
Crystalloid bodies are also frequently observed in the nucleolus (Digby 
on Galtonia, 1910; Reed on Allium, 1914; Kuwada on Zea, 1919). In 
the epithelial cells of the frog intestine Carleton (1920) finds one or more 
intranucleolar bodies which he calls "nucleolini." These appear to 
divide and pass to the daughter cells at the time of mitosis, and may 
possibly initiate the formation of new nucleoli in the daughter nuclei. 
Montgomery (1899) 1 concluded that the nucleolus grows in size by the 
apposition of smaller particles of nucleolar material on its surface, and 
by the intussusception of vacuolar substance arising outside the nucleolus. 

Function of Nucleolus. Various opinions have been entertained re- 
garding the function of the nucleolus. By many workers it has been 
looked upon as chiefly a passive by-product of no further use in the life 

1 An exhaustive review of the literature dealing with the nucleolua up to 1890 
is given in this paper. 


of the cell (Haecker). Strasburger (1895, 1897), who observed the dis- 
appearance of the nucleolus at about the time the spindle fibers appear 
during the prophases of mitosis, concluded that it is a mass of reserve 
kinoplasm which gives rise indirectly to the achromatic figure. While 
some have agreed in the main with this conclusion, many have denied 
the relationship of nucleolus and spindle, contending that the former is 
rather a reserve constituent for the linin reticulum (Eisen 1900) or the 
chromatin (Schurhoff 1918). Frequently the bulk of the basichrom- 
atic material of the nucleus is lodged in the nucleolus at certain stages. 
In the somatic nuclei of Marsilia (Fig. 17, E), for example, Befghs (1909) 
shows that it is transferred to the nucleolus during the telophases of 
mitosis, and returned to the reticulum in the following prophases. This 
phenomenon, which has an important bearing on the r61e of the chrom- 
atin and the individuality of the chromosomes, will be referred to again 
in Chapter VIII. 

In many cells, as shown by the work of the zoologists the nucleolus 
appears to be concerned in the elaboration of secretion and storage prod- 
ucts. In the eggs of certain animals Macallum (1890) showed that 
the nucleolar material, which appears to differentiate from the chrom- 
atin, passes into the cytoplasm and there combines with another 
substance to form the yolk globules. In the cells of the pancreas he 
further found that material often present in the form of nucleoli func- 
tions in a similar manner in the production of zyrnogen. Many other 
observations of this general nature have been reported. In the silk- 
gland cells of certain insects it has recently been shown by Nakahara 
(1917) that some of the nucleoli, which may originally be passive by- 
products, later pass into the cytoplasm and contribute to the formation 
of the secretion products. An extreme view of the importance of the 
nucleolus is that of Derschau (1914), who regards the nucleolus as the 
real center of the life of the cell. Granules of oxychromatin, he asserts, 
pass out from the nucleolus through the cytoplasm in the form of chon- 
driosomes, carrying basichromatin as a building material to the places 
where it is required. 

It is highly probable that the nucleolus has various functions in dif- 
ferent cells, b,ut in general we may conclude that it is a mass of accumu- 
lated material which is usually, though not always, utilized in the 
metabolic processes of the nucleus 

The Nuclei of Bacteria and Other Protista. The question of the 
nucleus in bacteria is one that it appears to be particularly difficult 
to settle satisfactorily. This is due not only to the minute size of these 
organisms, which makes special methods necessary and observation very 
difficult, but also to the fact that a variety of conditions seems to be 
present in the group. That the bacterial cell is devoid of a nucleus has 
been held by several investigators including Fischer (1894, 1897, 1899, 


1903), who looked upon the observed granules as reserve materials 
rather than nuclear substance. Migula (1894, 1897, 1904) regarded the 
existence of nuclei in bacteria as very doubtful. The majority of workers, 
on the contrary, have held that a nucleus or at least nuclear material ps 
present in some form. The most striking view is that which regards the 
whole cell in some cases as a naked nucleus (Hlippe 1886; Zettnow 1891, 
1897, 1899; Ruzicka 1908, 1909; and, in thfc case of small bacteria, 
Biitschli 1890, 1892, 1896, 1902). The evidence advanced in support of 
this hypothesis, however, is of very doubtful value 

In many bacteria, particularly the larger forms, there is present a 
granular substance which has certain characteristics of chromatin, and 
which in some species exists as a single well denned mass. The " central 
body" of the sulphur bacterium Btitschh regarded as the homologue of a 
nucleus, the peripheral portion of the cell being cytoplasm. In a careful 
study of the entire life cycle of Bacillus Butschlii Schaudin (1902) found 
that the chromatic material present during most of the cycle as chromidia 
unites at certain stages to form peculiar spiral figures; in the spores it 
takes the form of dense masses. Such scattered chromidia and "spiral 
filament nuclei" were also observed by Guilliermond (1908, 1909), who 
has given a review of the subject (1907). Nakanishi (1901), who employed 
both intra-vitam methods and fixed material, reported the presence of 
nuclei in the vegetative cells and spores of a number of species. 

The nucleus of the large Bacterium gammari was studied by Vejdow- 
sky (1900), who in 1904 described its division by mitosis. Mencl (1904, 
1905, 1907, 1909) demonstrated by careful methods the nuclei in many 
species and also reported mitotic division in Bacterium gammari. Doubt 
concerning the systematic position of this form, however, has been raised 
by some investigators, who think it not improbable that it is a yeast- 
like fungus rather than a bacterium. 

Dobell (1908, 1909, 1911), whose review of the subject has been of 
service in the preparation of this summary, has studied with much care 
many species of bacteria in their natural culture media. His conclusions 
are summarized in the following quotation (1911): 

"All bacteria which have been adequately investigated are like all 
other Protista nucleate cells. 

"The form of the nucleus is variable, not only in different bacteria, 
but also at different periods in the life cycle of the same species. 

"The nucleus may be in the form of a discrete system of granules 
(chromidia); in the form of a filament of various configuration; in the 
form of one or more relatively large aggregated masses of nuclear sub- 
stance; in the form of a system of irregularly branched or bent short 
strands, rods, or networks; and probably also in the vesicular form char- 
acteristic of the nuclei of many animals, plants, and protists. 

"There is no evidence that enucleate bacteria exist." 


The apparent discrepancy between this view of bacterial organization 
and that of Minchin, stated below, will be seen to be largely a matter of 

It is therefore among the Proitsta that the widest departures from 
the usual type of nuclear structure are found, certain of them in all prob- 
ability representing relatively primitive stages in the evolution of the 
true nucleus. Such an interpretation is evidently to be placed upon the 
" distributed nuclei " seen in certain bacteria, protozoans, flagellates, 
and Cyanophycese (p. 202), which consist of granules of a material akin 
to chromatin scattered throughout the cell, sometimes with a limiting 
membrane of some sort but often with none. It is doubtful if granules 
scattered with no definite limitations throughout the cell, as in Chcenia 
teres (Fig. 17, D) or Chroococcus turgidus (Fig. 72, A), should be spoken 
of collectively as a nucleus. As pointed out at the beginning of this 
chapter, it seems preferable to certain workers to limit the term to those 
chromatic aggregations which actually have the characters of a definitely 
localized organ. In discussing the advisability of so restricting' the appli- 
cation of the term Minchin (1912, Chapter VI) points out that "the word 
' chromatin' connotes an essentially physiological and biological con- 
ception ... of a substance, far from uniform in its chemical nature, 
which has certain definite relations to the life history and vital activities 
of the cell. The word 'nucleus/ on the other hand ... is essentially 
a morphological conception, as of a body, contained in the cell, which 
exhibits a structure and organization of a certain complexity, and in 
which the essential constituents, the chromatin particles, are distributed, 
lodged, and maintained, in the midst of achromatinic elements which 
exhibit an organized arranegment, variable in different species, but more 
or less constant in the corresponding phases of the same species. " Ac- 
cording to this interpretation the term "nucleus" would not be applicable 
to a mass of granules (chromidia) scattered throughout the cell. Minchin 
states further that " . . .as soon as a mass or a number of particles of 
chromatin begin to concentrate and separate themselves from the sur- 
rounding protoplasm, with formation of distinct nuclear sap and ap- 
pearance of achromatinic supporting elements, we have the beginning 
at least of that definite organization and structural complexity which is 
the criterion of a nucleus as distinguished from a chromidial mass." 

Those Protista of the lower (bacterial) grade, in which there are only 
scattered grains of chromatic material, are looked upon as "non-cellular" 
in organization by Minchin, who believes that from such a primitive 
state the "strictly cellular grade of organization has been evolved by 
concentration of some or all of the chromatin to form a nucleus." In 
its simplest condition such a nucleus consists of one or more chromatin 
granules in a sort of vacuole, and is known as a "protokaryon." In other 
cases the chromatin forms a single large mass at the center of the nucleus 


("vesicular nucleus")- Since "the chromatic particles are the only con- 
stituents of the cell which maintain persistently and uninterruptedly 
their existence throughout the whole life cycle of living organisms uni- 
versally/' Minchin (1916) believes that the earliest living things, which 
he calls " Biococci," were minute particles of a chromatin-like substance. 
These were the ancestors of the present chromatin grains and find their 
nearest modern representatives in certain pathogenic Chlamydozoa. Ac- 
cording to this view the cytoplasm was differentiated later in the evolu- 
tion of the cell, whereas the more general view probably is that chromatin 
and cytoplasm were coexistent as two substances in cells from the earliest 
known stages (Wilson). 1 

The Function of the Nucleus. It may be said without reservation 
that the nucleus dominates the morphological and physiological changes 
in the cell. Although the type of organization formed by a nucleus in 
combination with cytoplasm is required for the carrying on of cell activity, 
it is nevertheless evident from a huge mass of accumulated observations 
that in the nucleus is to be found the center of control for both the func- 
tional activities and for cell reproduction (cell-division). Many years 
ago Claude Bernard (1878) pointed out that while the cytoplasm is the 
seat of destructive metabolism, the nucleus is the seat of constructive 
metabolism, this physiological role offering "the key to its significance as 
the organ of development, regeneration, and inheritance " (Wilson). The 
inability of a cell deprived of its nucleus to carry on synthetic metabolism 
in any complete manner has often been noted, though such a cell may not 
perish for some time. The mammalian erythrocyte, for example, loses 
its nucleus at an early stage and may continue to exist in the enucleate 
state for from 15 to 30 days (Hunter, Quincke). Klebs found that 
enucleate cells of Spirogyra may continue for some time to form starch. 
But such cells are apparently unable to divide or to increase their bulk 
by the elaboration of new cell substance. Many ordinary activities, such 
as cell wall formation (Townsend 1897; Gerassirnow 1899, 1901), fail to 
occur. From such observations it is concluded that the nucleus is nec- 
essary for the synthetic processes associated with growth and reproduc- 
tion. This conclusion is supported by the facts of regeneration. 

The role of the nucleus in regeneration was strikingly shown by the 
well known experiments of Gruber (1885) and F. R. Lillie (1896) on Sten- 
tor. This unicellular organism, which has a nucleus like a string of beads, 
may be cut into fragments: any fragment containing a portion of the 
nucleus has the power of regenerating a complete new animal, whereas 
enucleate fragments, although they may live for a little time, undergo no 
regeneration and eventually perish. 

1 For more complete descriptions of the nuclei of Protista the works of Wilson 
(1900) and Minchin (1912) should be consulted. The behavior of such nuclei at the 
time of cell-division is briefly described in Chapter X of this book. 


A number of biologists (Gruber 1886, Hertwig 1898, Heidenhain 1894, 
Henneguy 1896, Conklin 1902) concluded that in general the chromo- 
somes (basichromatin) are concerned chiefly with differentiation and 
regulation, while the achromatin (oxychromatin) has to do with metabo- 
lism (Conklin 1917). Metabolism is in reality a great complex of 
reactions: the reactions are not independent of one another but are closely 
correlated, and thus constitute an intricately adjusted reaction system. 
Among these many reactions, according to modern physiology, the most 
important is oxidation, for the energy utilized by the organism is derived 
immediately from the union of protoplasm or of its constituent elements 
with oxygen. Oxidation has been called the "independent variable" 
(Loeb and Wasteneys 1911) upon which the other reactions largely 
depend: oxidation is the dominant factor in cell activity, and it is there- 
fore of the greatest importance to understand as well as possible the rela- 
tion of the parts of the cell to this process. 

Following the experiments of Spitzer (1897), who observed thatnucleo- 
proteiris extracted from certain animal tissues have the same oxidizing 
power as the tissues themselves, it was advocated by Loeb (1899) that the 
nucleus is the center of oxidation in the coll. 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), who 
later (1913) showed that rapid oxidation occurs both at the surface of the 
cell and at the surface of the nucleus, and also by Mathews (1915). Other 
workers (Wherry 1913, Schultze 1913, Reed 1915), however, have failed 
to agree. Osterhout (1917), who briefly summarizes the subject, found 
that "injury produces in the leaf-cells of the Indian Pipe (Monotropa 
uniflora) a darkening whicji is due to oxidation. The oxidation 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." 

The role of the nucleus in development and inheritance, which has 
been a subject of so much discussion in recent years, will be dealt with 
in later special chapters (XIV-XVIII), after the behavior of the nucleus 
in somatic cell-division, maturation, and fertilization has been described. 

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Beitr. z. Biol. d. Pfl. 5 : 443-459 pi. 16. 
RUZICKA, V. 1908. Sporenbildung und andere biologische Vorgange bei deni 

Bad. anthracis. Arch. f. Hyg. 64: 21&-294. pis. 1-3. 
1909. Die Cytologie der Sporenbildenden Bakterien und ihr Verhaltnis zur 

Chromidienlehre. Centr. Bakt. II 23 : 289-300. figs. 8. 
SACHS, J. 1892. Physiologische Notizen II. Beitrage zur Zellentheorie. Flora 

76: 57-67. 
1893. Physiologische Notizen VI. Ueber einige Beziehungen der specifischon 

Grosse der Pflanzen zu ihrer Organisation. Ibid. 77: 49-81. 
1895. Physiologische Notizen IX. Weitere Betrachtungen liber Energiden und 

Zellen. Flora (Erganzungsband) 81: 405-434. 
SCHAUDINN, F. 1902. Beitrage zur Kenntniss der Bakterien und verwandten 

Organismen. 1. Bacillus Biitschlii, n. sp. Arch. Protistenk. 1 : 306. 

1903. II. Bacillus sporonema, n. sp. Ibid. 2: 421. 

SCHULTZE, W. H. 1913. Die Sauerstofforte der Zelle. Verh. Deu. Path. Ges. 16: 

SCHURHOFF, P. N. 1918. Die Beziehungen des Kernkorperchens zu den Chronio- 

somen und Spindelfiisern. Flora 110: 52-66. figs. 3. 
SCHWARZ, FR. 1887. Die morphologischc und chemische Zusammensetzung des 

Protoplasm as. Breslau. 
SPITZER. 1897. Die Bedeutung gewisser Nukleoproteide fiir die oxidative Leistung 

der Zelle. Arch. f. Ges. Physiol. 67: 615-656. 
STRASBURGER, E. 1893. Ueber die Wirkungssphare den Kerne und die Zellgrosso. 

Histol. Beitr. 6: 97-124. Jena. 

1895. Karyokinetische Probleme. Jahrb. Wiss. Bot. 28: 151-204. pis. 2, 3. 
1897. Ueber Cytoplasmastrukturen, Kern- und Zelltheilung. Ibid. 30; 375-405. 

figs. 2. 
TOWNSEND, C. O. 1897. Der Einfluss des Zellkerns auf die Bildung der Zellhaut. 

Jahrb. Wiss. Bot. 30: 484-510. pis. 20, 21. 
VEJDOWSKY, F. 1900. Bemerkungen uber den Bau und Entwicklung der Bakterien. 

Centr. Bakt. II 6 : 577-589. 1 pi. 

1904. Ueber den Kern der Bakterien und seine Teiiung. Ibid. 11: 481-496. 

WHERRY, E. T. 1913. On the metamorphosis of an amoeba, Vahlkampfia sp., into 

flagellates and vice versa. Science 37: 494-496. 

WILSON, E. B. 1900. The Cell in Development and Inheritance. 2d ed. 
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in the echinoderm egg. New light on the "Quadrille of the Centers." Joar. 

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Jour. Exp. Zool. 2: 287-312. figs. 8. 
ZACHARIAS, E. 1881-1893. See Bibliography 3. 


ZETTNOW, E. 1891. Ueber den Bau den Bakterieii. Centr. Bakt. 10: 090. 
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Bakt. 146: 193. 

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plant groups.). 



For a full description of the morphology and behavior of the centro- 
some, based upon the large amount of work done on animal cells prior to 
1900, reference should be made to Wilson's book on the cell. In the 
present account attention will be devoted mainly to centrosomc structures 
in plants. The ccntrosomes of animal cells will be described only in 
general terms, their role in cell-division being dealt with in later chapters. 
Occurrence and General Characters. The centrosome is an organ 
which is characteristic chiefly of the cells of animals: in the great majority 
of these cells it has been found, at least during certain stages. In plants 
centrosomes are limited to the cells of algae and fungi and the spermato- 
genous cells of certain bryophytes and pteridophytes. If the blcpharo- 
plast be regarded as a modified centrosome, a question which will be 
discussed further on, all motile cells (spermatozoids) of bryophytes, 
pteridophytes, and gymnosperms must be looked upon as possessing 
centrosomes. During the last decade of the nineteenth century several 
botanists reported the presence of centrosomes in the cells of a number of 
angiosperrns, but these cases have all failed to stand the test of subsequent 
more critical research. 1 

It is scarcely possible to give a description which will apply to all 
centrosomes, since to any rule there are apparently exceptions. The 
"typical" centrosome, as seen in animal cells, is a very minute granule, 
which stains intensely with certain dyes. It is usually situated in the 
cytoplasm, but in some cases it is found within the nucleus (Fig. 18). 
It commonly lies in a more or less hyaline mass of material, called the 
centrosphere (Strasburger 1892), attraction sphere (van Beneden 1883), 
astrosphere (Fol 1891), or hyaloplasm sphere (Wilson 1901). 2 This centro- 
sphere may often show two or more concentric zones differing somewhat 
in structure and appearance (Fig. 60). At certain stages, especially 
during nuclear division, the centrosome becomes the focus of a system of 

delicate rays known collectively as the aster (Fol 1877). The aster will 


1 For a review of these cases see Koernicke (1903, 1906). 

8 There has been much confusion in the application these terms. (See Wilson 
1900, p. 324.) 




receive consideration in the chapter on the achromatic figure. 1 Very 
often there are two centrosomes lying side by side in the centrosphere, 

t r 

FIG. 18. Centrosomes in animal cells. 

A, attraction sphere above nucleus i/i spermatocyte of Salamandra. (After Rawitz; 
ace. also Fig. 59.) B-F, intranuclear centrosome in spermatocyte of Ascaris mcgaloce phala 
and its behavior during the prophases of mitosis; c, centrosphere; chr, chromosome tetrad. 
(After Brauer, 1893.) 

the two having arisen by the division of one, apparently in preparation 

for the next cell-division (Fig. 19). Von Winiwarter (1912) noticed 

that in interstitial testicular cells, which may 

have one, two, or four nuclei, there are re- 

spectively two, four, and eight rod-like cen- 

trosomes lying in midst of a granular mass 

("idiosome")- In some cells there may be a 

larger number of smaller "centrioles" rather 

then one centrosome, and occasionally there are 

one or more concentric scries of granules about 

the central centrosome. Several such types 

described by various writers are shown in 

Wilson's Fig. 152. It is questionable how far 

these are normal appearances, for Chambers 

(1917) asserts that several of them may be pro- 

duced in the animal egg by subjecting the latter 

to abnormal environmental conditions. 

Individuality, The centrosome was dis- 
covered and described by Flemming (1875) 
and independently by van Berieden (1876). In 
1887 van Beneden and Boveri, as a result of FIG. i9.~ 
their researches on the thread-worm, Ascaris 



epithelial cells. 

megalocephala, independently concluded that the ke ' s^om^Mc dand 
centrosome, like the nucleus, is a permanent cell of man. (After zimmcr- 
organ maintaining it 4; individuality throughout mann<) 

1 Because of the relation of the centrosome to the achromatic figure it will be 
necessary to make constant reference to the latter. Chapter IX should be consulted 
in this connection, 



successive cell generations. They observed that, prior to cell-division, 
the centrosome 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 not 
disappear, but remains visible in the cytoplasm through the ensuing 
resting stage. Because of this striking behavior at the time of cell- 
division (see further p. 177) the centrosome soon came to be known as 
"the dynamic center of the cell." 

The above facts seemed to constitute ample ground for the conception 
of the centrosome as a permanent cell organ, but many obstacles have 
been found in the way of its acceptance as a theory of universal applica- 
tion. At certain stages in the history of many animal cells its presence 


Fi<}. 20.- -Artificial cy tasters in the egg of Arbacia. (After Morgan, 1899.) 

cannot be demonstrated, and it is entirely absent from the cells of higher 
plants. Furthermore, Mead (1898) and Morgan (1896. 1898) found that 
the formation of centrosomes with asters may be induced in the eggs of 
certain animals by artifical means (treatment with NaCl and MgCl 2 
solutions) (Fig. 20), and it has been claimed that centrosomes so formed 
may function normally in the ensuing division (cleavage) of the egg. 
Contrary to the opinion of Boveri (1901), Wilson (1901) regarded such 
" artificial cytasters" as true asters with true centrosomes. Conklin 
(1912), however, contends that they do not function in mitosis. It is 
probable that no single conclusion can be drawn concerning this matter 
which will apply to all cases. There seems to be good evidence for the 
view that the centrosome in some tissues exists as a permanent cell organ, 
dividing at each mitosis and remaining visible through the resting stages, 



at least for a number of cell generations. In other cases it disappears at 
the close of mitosis, a new one being apparently formed just before the 
next mitosis. The fact that the formation of centrosomes may be 
brought about by artificial means suggests that the regular appearance of 
the centrosome in successive mitoses is closely associated with regularly 
recurring physiological conditions in the cell; and that its presence in 
successive cell-divisions does not require an uninterrupted morphological 
continuity through the intervening stages. Its constant presence in some 
tissues probably indicates the continuity of some physiological function. 
Centrosomes in Algae. 1 One of the earliest known centrosomes in 
plants was that of the diatom Surirella discovered by Smith (1886-7) 
and Biitschli, and fully described by Lauterborn (1896) and Karsten 
(1900). It lies near the nucleus, becomes surrounded by radiations, and 
divides to form the central spindle of the mitotic figure in a very 
peculiar manner. 

FIG. 21. Centrosomes in alga3. 

A, Ktypocaulon. (After Swingle, 1897.) B, Stypocaulon. (After Escoyez, 1900.) C, 
feiitrosphcre-like bodies in Polysiphonia. (After Yamanouchi, 1900.) I), E, Dictyota 
dichotoma. (After Mottier, 1900.) 

Centrosornos in the Sphacclariaceae have been described by Humphrey 
(1894), Swingle (1897), Strasburgor (1900), and Escoyez (1909). In the 
vegetative cells of Sphacelaria, according to Strasburger, the centrosome 
is situated in a centrosphere at the focus of an aster. Previous to mitosis 
it divides into two which take up positions at opposite poles of the 
spindle. In Stypocaulon (Swingle) essentially the same condition exists 
(Fig. 21). Escoyez later concluded, however, that the asters of Stypocau- 
lon are formed independently rather than by division, and that the 
central corpusclse arc probably not true centrosomes, but cytoplasmic 

1 This review of plant centrosomes and also that of the blepharoplast in subsequent 
pages are based upon similar reviews given by the author in his paper on Sperm ato- 
genesis in Equisetum (1912). 


In the oogonium and segmenting oospore of Fucus Farmer and 
Williams (1896, 1898) described two centrospheres containing granules 
and arising independently at opposite sides of the nucleus. Strasburger 
(1897) reported definite centrosomes with asters all through mitosis. 
In the sporeling he observed appearances indicating the division of the 
centrosome, and concluded that the latter represents a permanent cell 
organ. In a very detailed investigation Yamanouchi (1909) demon- 
strated in the antheridium and oogonium two very definite centrosomes, 
which appear independently of each other, become surrounded by con- 
spicuous asters, and occupy the spindle poles during mitosis (Fig. 61, C). 
He further showed that when the sperm reaches the egg nucleus a new 
centrosome appears on the nuclear membrane at the point where the 
sperm enters. 

In Dictyota dichotoma Mottier (1898, 1900) states that in the two 
divisions in the tetrasporocyte, in at least the first three or four cell 
generations of the sporeling, and in all the vegetative cells of the tetra- 
sporic plant curved rod-shaped centrosomes with asters occur at the 
spindle poles, the two having arisen by the division of one during the 
early phases of mitosis (Fig. 21, D, E). Williams (1904) further reports 
that the entrance of the sperm causes a centrosome to appear in the egg 
cytoplasm. Centrosomes in Nemalion were described by Wolfe (1904). 

In Polysiphonia violacea (Yamanouchi 1906) there are present during 
the prophases of every mitosis two centrosome-like bodies in the kino- 
plasm at opposite sides of the nucleus. A little later the small bodies 
disappear, while the kinoplasm takes the form of two large centrospherc- 
like structures (Fig. 21, C); during the later stages of mitosis these fade 
from view. Yamanouchi believes that these structures do not represent 
permanent cell organs, but are formed de novo at the beginning of each 
mitosis. Somewhat similar temporary centrospheres, with radiations 
but no centrosomes, are present in the tetrasporocyte of Corallina (Davis 
1898; Yamanouchi) 

Fungi. Among the fungi the best known centrosomes are those of the 
Ascomycetes (Fig. 22). Harper (1895, 1897, 1899, 1905) described granu- 
lar disc-shaped centrospheres surrounded by asters at the poles of the 
spindle in the asci of Peziza, Ascobolus, Erysiphe, Lachnea, Phyllactinia, 
and other genera. He regarded them as permanent organs of the cell. 
In a recent paper (1919) he speaks of the ascomycete centrosome as a 
structure differentiated "as a region of connection between nucleus and 
cytoplasm and for the formation of fibrillar kinoplasm. " Harper be- 
lieved the ascospore walls to be formed by the lateral fusion of the curved 
astral rays focussing upon the centrosome, a point disputed by Faull 
(1905) and others. Centrosomes in additional genera were figured by 
Guilliermond (1904, 1905). In GaUactinia succosa (Marie 1905; Guillier- 
mond 1911) a single centrosome, which arises within the nucleus with a 



cone of fibrils extending" toward the chromatin, divides into two which 
take up positions opposite each other at the nuclear membrane, at which 
time asters develop in the cytoplasm. Faull (1905) found centrosomes in 
Hydnobolites, Neotiella, and Sordaria; in the last named genus they 
appear to be discoid while the cell is in the resting condition but round 
and smaller during mitosis. In Humaria rutilans Miss Fraser (1908) 
observed two centrosomes lying near each other, each at the apex of a 
cone of fibers and surrounded by a faint aster. These move apart and 

FIG. 22. Centrosomes in ascomycetes. 

A-C, Phyllactinia corylea: division of nucleus in ascua, showing behavior of centro- 
somes. D, Erisiphe cichoracearum: formation of ascopore wall. (After Harper, 1905.) 

establish the spindle in the usual manner. Centrosomes are also figured 
in Ascobolus and Lachnea by Fraser and Brooks (1909); in Otidea and 
Peziza by Fraser and Welsford (1908); in Microsphcera by Sands (1907); 
and in Pyronema by Claussen (1912). 

In the Basidiomycete Boletus (Levine 1913) the centrosomes present 
during the last mitosis in the basidium attach themselves to the basidium 
wall, and in close connection with them the daughter nuclei are recon- 
structed. They mark the points of origin of the sterigmata and eventu- 
ally pass into the spores. 


Bryophytes. The first centrosome known in the liverworts was that 
of Marchantia described by Schottlander (1893), according to whom the 
centrosome in the spermatogenous cells divides during the'anaphases of 
mitosis, so that each daughter nucleus is accompanied by two (Fig. 27). 
In the gametophytic cells certain minute bodies with radiations at the 
poles of the elongated nucleus and of the spindle were believed by Van 
Hook (1900) to represent centrosomes. Centrospheres with conspicuous 
radiations but without true centrosomes were described in the mitoses of 
the germinating spore of Pellia by Farmer and Reeves (1894), Davis 
(1901), and Chamberlain (1903). Gregoire and Bcrghs (1904), however, 
pointed out that the centrospheres observed by the foregoing writers in 
Pellia are in reality only appearances due to the intersection of numerous 
astral rays, and are not distinct bodies. 

,. %"'%: * *'.',*<' 

V&r VlC.'.V ?"*"* Y*A 



\ < ' i -Vr "" % ,<' / 

' .iV\ ' 

'- * ''^W 1 * 3*$EL*^ tf f' ' : ' * '" 

A " n*V-:v" B ~ 

FIG. 23. Centrosornes in Prcisaia quadrata. 

A t in fertilized egg just prior to nuclear fusion, B> in cells of young embryo. (After 
Graham, 1918.) 

In the cells otPreissia quadrata Miss Graham (1918) has more recently 
made some observations of much interest. She describes and figures two 
distinct centrosomes with a few astral rays in the cytoplasm of the fer- 
tilized egg, at the time when the sexual nuclei are approaching each other 
and in contact (Fig. 23, A). This, together with Yamanouchi's observa- 
tion on Fucus and that of Williams on Dictyota, cited above, suggests 
that in certain plants, as in animals, the formation of centrosomes and 
asters in the egg cytoplasm is in some way induced by the entrance of the 
sperm. Similar appearances have been noted by Meyer (1911) in Cor- 
sinia and by Florin (1918) in Riccardia (Aneura). Centrosomes were 
also observed by Miss Graham in the four-celled embryo of Preissia 
(Fig. 23, B)j this being one of the only cases in which centrosomes have 
been seen in non-spermatogenous cells in plants above the algae. 

Conclusion. With regard to centrosomes in plants, it may be con- 
cluded from the above review that although there is no adequate evidence 
for their existence in the cells of angiosperms, they are clearly present in 
many algae, fungi, and probably certain bryophytes, where they perform 


definite functions in the life of the cell. The question of centrosoines in 
the spermatogenous cells of bryophytes, pteridophytes, and gymnosperms 
is dealt with in the following discussion of the blepharoplast. 


Occurrence. The blepharoplast, as indicated by the name given to 
it by Webber (1897), is the cilia-bearing organ of the cell. Blcpharo- 
plasts of one kind or another are found generally in the motile cells of 
plants and animals, such as motile unicellular organisms (Flagellata, 
Ciliata, etc.), swarm spores, spermatozoa, and spermatozoids; and also 
in cells which, though not freely motile themselves, have motile organs 
performing other functions, as in the case of ciliated epithelium. In 
plants blepharoplasts are most conspicuously displayed in the sperma- 
togenous cells of bryophytes, pteridophytes, and gymnosperms (cycads 
and Ginkgo), where their striking resemblance to ordinary ccutrosoincs 
has led to much controversy over their nature. Some cytologists have 
regarded the blepharoplast as a more or less modified ccntrosome, where- 
as others have contended that it is a special kinoplasmic or cytoplasmic 
organ distinct from the ccntrosome. In recent years the evidence has 
tended strongly to support the former view. 

In the following pages the blepharoplasts of various organisms and 
the manner in which they function in the development of the motor 
apparatus will be described in some detail. Attention will be given 
chiefly to the situations found in plants; the corresponding phenomena 
in animals will be more briefly considered. 

Flagellates. In the flagellates several types of flagellar apparatus 
are found (see Minchin 1912, pp. 82 ff., 262-3) : in one series of forms 
the cell contains a single nucleus and "centriole," the latter functioning 
both as a centrosome and as a blepharoplast. The centriole may lie 
either against or within the nucleus, so that the flagellum which grows 
from it appears to arise directly from the nucleus (Mastigina) ; in other 
forms (Mastigella) the centriole is quite independent of the nucleus. 

In a second series of forms a single nucleus and centrosome are present, 
and in addition one or more blepharoplasts. Three conditions have been 
distinguished here: (a) at the time of cell-division the blepharoplasts 
and flagella are lost, new blepharoplasts arising from the centrosomcs 
during or after mitosis; (6) the blepharoplasts may persist, dividing to 
form daughter blepharoplasts from which new flagella arise (Polytomella) ; 
(c) the centrosome divides to furnish a blepharoplast which subdivides to 
two: a distal blepharoplast or basal granule of the flagellum, and a 
proximal blepharoplast or " anchoring granule" at the surface of the 
nucleus, the two being connected by a delicate strand known as the* 
rhizoplast, rhizonema, or centrodesmose (Peranema trichophorum). Entz 
(1918) has recently reinvestigated the structure of Polytoma uvella, first 



described by Dangeard (1901), and finds the elaborate organization 

shown in Fig. 24. 

In a third series of forms two nuclei are present: a principal or trophic 

nucleus and an accessory or kinetic 
nucleus. Here there are apparently 
three conditions: (a) a single centrosome, 
associated with the kinetonucleus, acts 
both as a blepharoplast and as a division 
center; (6) usually both nuclei have 
centrosomes associated with them, the 

FIG. 24. FIG. 25. 

FIG. 24. Diagram of structure of Polytoma uvella. (After Entz, 1918.) 
a, end-piece of flagellum. b, uniform portion of flagellum. c, lateronema. rf, baso- 
plast or basal granule. e t contractile vacuole. /, cell envelope. 0, eyespot. A, rhizonema. 
i, karyoplast or anchoring granule, j, centronema. k, nucleolus. I, nuclear membrane, 
m, starch, n, surface of protoplast. 

FIG. 25. Trypanosoma theileri. 

A, flagellum inserted on basal granule. B, formation of new flagellum from daughter 
basal granule after division; nucleus dividing. (After Hartmann and Ndller, 1918.) 

one lying near or within the kinetonucleus acting as the blepharoplast; 
(c) it is possible that in some cases there is a blepharoplast distinct from 
the centrosomes accompanying the two nuclei. 

In the trypanosomes (Fig. 25) the recent researches of Kuczynski 
(1917) and Hartmann and Noller (1918) have shown that the flagellum 



is inserted on a " basal granule" (centrosome?) very near the "blepharo- 
plast " (kinetonucleus?). At the time of cell-division the trophic nucleus, 
blepharoplast, and basal granule all divide, the division of the blepharo- 
plast showing certain features suggesting mitosis. Although earlier 
investigators thought the flagellum also split, the above named workers 
find that the old flagellum remains attached to one of the daughter basal 
granules while a new flagellum grows out from the other daughter granule. 

In flagellate organisms, therefore, the centrosome and the blepharo- 
plast clearly stand in very intimate relationship with one another: in 
some of the forms they arc one and the same organ. 

Thallophytes. Among the earliest investigations of the blepharoplast 
in algse were those of Strasburger (1892, 1900). During the development 
of the zoospores of (Edogonium, Cladophora, and Vaucheria Strasburger 


^j '"/v.... 


'7x;i-r- r '^ 

\V^ ^S^^S 1 

c ^^vvyi^>^ 

FIG. 26. Blepharoplasts in Thallophytcs. 

AD, formation of the cilia-bearing ring in the zoospore of Drrhatia. (Afte 
1908.) R, Stemonitis flaccida: cilia growing from centrosomes during late stage of 
in the formation of swarmers. (After Jahn, 1904.) 

r Davis, 

found that the nucleus approaches the plasma membrane, which at that 
point forms a lens-shaped thickening. From this structure grow out the 
cilia, and at the base of each a small refractive granule is present. The 
blepharoplasts of the higher groups were believed by Strasburger to have 
been derived from such swollen ectoplasmic organs of the algae, and that 
all of them are morphologically distinct from centrosomes. Dangeard 
(1898) likewise found a deeply staining granule at the base of the cilia 
in Chlorogonium. 

In Hydrodictyon (Timberlake 1902) the cilia are inserted on a small 
body lying in contact with the plasma membrane and joined with the 
nucleus by a delicate protoplasmic strand. The possible relationship 
of this body with the granules seen occupying the spindle poles during 
the formation of the spore cells was not determined. In the young 



zoospore cell of Derbesia (Davis 1908) the nucleus migrates toward the 
plasma membrane, and from it many granules, which are not centrosomes 
move out along radiating strands of cytoplasm to the surface of the cell 
where by fusion they form a ring-shaped structure from which the cilu 
develop (Fig. 26, A-D). In the developing spermatozoid of Chare 
(Belajeff 1894; Mottier 1904) the blepharoplast arises as a differentiatior 
of the plasma membrane and bears two cilia. No centrosomes or othei 
granules were seen at the base of the cilia, although Schottlander (1893^ 
had previously reported centrosomes in the cells of the spermatogenous 

In the zoospore of the fungus Rhodochytrinm (Griggs 1904) there is a 
deeply staining body at the insertion point of the cilia; this is connected 
by fine cytoplasmic fibers with the nucleus. In the myxomyeete Stemo- 
nitis Jahn (1904) made an observation that is highly suggestive in con- 
nection with the question of the relationship of the centrosome and the 
blepharoplast. At the last mitosis in the formation of the swarmers the 
spindle poles are occupied by centrosomes, and during the anaphasej- 
the flagella of the resulting swarmers grow out directly from these cen- 
trosomes (Fig. 26, E), just as in the spormatocytos of certain insects 
(p. 95). 

FIG. 27. Spermatogenesis in Marchanlia. 

b, blepharoplast; c, centrosome; c. n., " chromatoider Nebenkorper;" n, nurleu.s. 
(After Ikeno, 1903.) 

Bryophytes. Among the bryophytes the blepharoplasts of Mar- 
chantia and Fegatella (Conocephalus) have received much attention. 
According to Ikeno (1903) a centrosome conies out of the nucleus at 
each spermatogenous division in Marchantia and divides to form two 
which separate to opposite sides of the cell, occupy the spindle poles, 
and disappear at the close of mitosis : it is possible that they are included 
in the daughter nuclei. After the last (diagonal) division, however, they 
remain in the cytoplasm as the blepharoplasts, elongating and bearing 
two cilia (Fig. 27). Another body, the chromatoider Nebenkorper -, is 



ulso present in the cytoplasm. Similar in most points is the account 
of Schaffner (1908). Miyake (1905), as the result of his studies on 
Marchantia, Fegatella, Pellia, Aneura, and Makinoa, believes that such 
liverwort centrosomes are merely centers of cytoplasmic radiation, and 
inclines toward the view of Strasburger that the blepharoplast and the 
centrosome are not homologous structures. Escoyez (1907) finds two 
" corpuscles" appearing in contact with the plasma membrane in each 
cell of the penultimate generation in the antheridia of Marchantia and 
Fegatella; they occupy the spindle poles and function as blepharoplasts 
in the spermatids (the cells which transform directly into spermatozoids). 
Bolleter (1905) believes the centrosome-like body in Fegatella to arise 
within the nucleus. 

In the antheridium of Riccia Lewis (1906) reported centrosome-like 
bodies in both the early and diagonal divisions. They apparently arise 
de novo in the cytoplasm prior to each mitosis, showing no continuity 
through succeeding cell generations except after the last mitosis, when 
they persist and become the blepharoplasts. 

FIG. 28.- Spermatogenesis in Blasia. 
b, blepharoplast; n, nucleus. X 4200. (After Sharp, 1920.) 

Woodburn (1911, 1913, 1915) has given accounts of spermatogenesis 
in Porella, Asterella, Marchantia, Fegatella, Blasia, and Mnium. He 
finds that the blepharoplast is first distinguishable as a special granule in 
the cytoplasm of the spermatid, and holds that it represents, as Mottier 
(1904) had formerly suggested, an individualized portion of the kinoplasm 
arising de novo in certain spermatogenous cells. In a more recent con- 
tribution (Sharp 1920) it has been shown that in Blasia (Fig. 28) a 
blepharoplast is present at each spindle pole during all stages of the last 
spermatogenous mitosis, and that in the spermatid it fragments as it 


becomes transformed into the cilia-bearing thread after the manner of 
the blepharoplast of Equisetum, described below. 

Spermatogcnesis in Pellia, Atrichum, and Mnium has been described 
by M. Wilson (1911). In Mnium and Atrichum the spermatogenous 
divisions show no centrosomes, whereas in Pellia centrospheres, and 
probably centrosomes, are present during the later mitoses. The origin 
of the blepharoplast as here described is very peculiar. In the spermatid 
of Mnium a number of bodies are said to separate from the nucleolus and 
pass out into the cytoplasm where they coalesce to form a limosphere. 
The nucleolus then divides into two masses, both of which pass into the 
cytoplasm; one functions as the blepharoplast and the other gives rise 
to an accessory body. In Atrichum the first body separated from the 
nucleolus becomes the blepharoplast, a second forms the limosphere, and 
a third the accessory body. In all three plants the blepharoplast goes 
to the periphery of the cell and grows out into a thread-like structure 
along the plasma membrane. The nucleus then moves against this 
thread and the two grow together to form the spirally coiled spermatozoid. 
Two cilia grow out from the anterior end of the blepharoplast. 

The most detailed and critical of all researches on the motile cells 
of bryophytes are those of C. E. Allen (1912, 1917) on Polytrichum 
(Fig. 29). The first of these papers contains a description of the cy to- 
logical phenomena accompanying the multiplication of the spermato- 
genous cells (androgones) up through the last mitosis, which differentiates 
the spermatids (androcytes) . In the cytoplasm of all the androgoncs 
there is a deeply staining kinoplasmic mass; in the early androgones this 
has the form of a flat plate, while in the later ones it consists of a group 
of granules (kinetosomes). Prior to each mitosis the plate or group 
divides to daughter plates or groups which pass to the daugher cells. 
In the cells of the penultimate generation (androcyte mother-cells) there 
are no kinetosomes, but instead a spherical "central body" with radia- 
tions. This body divides into two which move apart and occupy the 
spindle poles during the last mitosis. Each resulting androcyte therefore 
has one such body, which functions as the blepharoplast. Allen does not 
regard the kinetosomes as definite morphological entities, but rather as 
masses of reserve kinoplasm. The blepharoplast, however, is a definite 
cell organ, and although Allen inclines toward the view that it is the 
homologue of a centrosome he regards the question as an open one. 
Sapehin (1913) looks upon these bodies as plastids. 

Allen's second paper deals with the transformation of the androcyte 
(spermatid) into the spermatozoid. The blepharoplast elongates to 
form a uniform rod and develops two cilia from near its anterior end. 
The nucleus moves against the middle portion of the blepharoplast and 
the two elongate together in close union to form the body of the sperma- 
tozoid, the blepharoplast projecting beyond the anterior end of the 



nucleus. At about the time the blcpharoplast begins to elongate a 
limosphere appears in the cytoplasm and takes up a position near the 
anterior end of the blepharoplast. Here it divides, giving rise to a small 
apical body that remains visible at the end of the blepharoplast until a 
comparatively late stage. The remaining portion of the limosphere may 
be seen lying against the nucleus until the maturity of the spermatozoid 

FIG. 29. Spermatogenesis in Polytrichum. 

A~D t androgones, showing behavior of kinoplasmic plates and kinetosomes (k) during 
imitoss. E-G, androcyte mother-cells, showing division of central body. H, telophase 
of last mitosis; each androcyte has a blepharoplast (6). I-K, stages in the transformation 
of the androcyte into the spermatozoid: a, apical body; /, limosphere; n, nucleus; p, 
percnosorne. L, mature spermatozoid. X 2535. (After Allen, 1912, 1917.) 

Another body, the percnosome, is also seen in the cytoplasm at certain 
stages. In the opinion of Allen the limosphere is probably identical with 
the chromatoider Nebenkorper described by Ikeno in Marchantia, and the 
percnosome with what M. Wilson (1911) terms the accessory body. The 
apical body is here described for the first time by Allen. 

Pteridophytes. The early papers dealing with the spermatozoid of 
pteridophytes, such as those of Buchtien (1887), Campbell (1887), Bela- 



jeff (1888), Guignard (1889), and Schottlander (1893), give but little 
information concerning the development of the blepharoplast. Our more 
definite knowledge of this subject dates from 1897, when Belajeff published 
three short papers. In the first of these (1897a) it was stated that the 
fern spermatozoid consists of a thread-shaped nucleus and a plasma band, 
with a great many cilia growing out from the latter. In the plasma band 
is enclosed a thin thread which arises by the elongation of a small body 
seen in the spermatic!. In the second paper (18976) the blepharoplast of 
Equiaetum was first described as a crescent-shaped body lying against the 
nucleus of the spermatid; this body stretches out to form the cilia-bearing 
thread. The third contribution (1897c) is a short account of the trans- 
formation of the spermatid into the spermatozoid in Cham, Equisetum, 

FIG. 30. Sperrnatogenesis in Equisetum arvense, showing behavior of blcpharoplast 
(ccntroHonic) in last sperirwtogenous mitosis and in transformation of spermatid into sper- 
matozoid. X 1900. (After tfharp, 1912.) 

and ferns. In all these forms a small body elongates to form a thread 
upon which small swellings arise and grow out into cilia. In a comparison 
with animal spermatogenesis Belajeff here homologized the blepharoplast, 
the thread to which it elongates, and the cilia of the plant, with the 
centrosorne, middle piece, and tail (perhaps only the axial filament), 
respectively, of the animal. In the following year (1898) he figured the 
details made out in Gymnogramme and Equisetum. In Gymnogramme the 
two blepharoplasts appear at opposite sides of the nucleus in the spermatid 
mother-cell, whereas in Equisetum a single blepharoplast is first figured 
lying close io the nucleus of the spermatid. More recently it has been 
shown (Sharp 1912) that the blepharoplast of Equisetum (Fig. 30) appears 
first in the cells of the penultimate generation; there it divides to two 
which separate and establish between them the achromatic figure after 
the manner of animal centrosomes. At the close of mitosis the blepharo- 



plast in each spermatic! fragments into a number of pieces; these later 
join to form a continuous beaded thread from which the cilia grow out. 
In Equisetum the elongating nucleus and blepharoplast do not become 
closely joined, but are held together only by the rather abundant cyto- 
plasm. The spermatozoid is multiciliate like that of all other ptcrido- 
phytes with the exception of Lycopodium, Phylloglossum, and Selaginella: 
in these three genera the spermatozoids are biciliate like those of the 

The most careful work on the blepharoplast of homosporous ferns is 
that of Yamanouchi (1908) on Nephrodium (Fig. 31). In this form no 
centrosorncs are found. The two blepharoplasts, 
which arise de novo in the cytoplasm of the sperm- 
atid mother-cell, take no active part in nuclear 
division, merely lying near the poles of the spindle. 
In the spermatid the blepharoplast elongates spirally 
in close union with the nucleus to form the body of 
the spermatozoid. In Adiantum and Aspidium Miss 
R. F. Allen (1911) and Thorn (1899) see the blepharo- 
plast first in the spermatid. 

One of the most interesting blepharoplasts is that 
of Marsilia (Fig. 32), first described by Shaw (1898). 
According to Shaw a small granule, or "blepharo- 
plastoid," appears near each (laughter nucleus of the 
mitosis which differentiates the grandmother-cell of 
the spermatid (the second of the four spermatogenous 
mitoses). During the next (third) division the 
blepharoplastoid divides but soon disappears, and a 
blepharoplast appears near each spindle pole. In the 
next cell generation (spermatid mother-cell) the 
blepharoplast divides into two which are situated at 
the spindle poles during the final mitosis. In the 
spermatid the blepharoplast gives rise to several 
granules by a sort of fragmentation; these together 
form a thread which elongates spirally in close union 
with the nucleus and bears many cilia. The spermatozoid is of the usual 
fern type, with several coils and a cytoplasmic vesicle. Shaw saw in the 
foregoing facts no ground for the homolpgy of the blepharoplast and the 
centrosome. Belajeff (1899) found that centrosomes occur at the spindle 
poles during all, excepting possibly the first, of the four divisions which 
result in the 16 spermatids. He reported that after each mitosis the 
centrosome divides into two which occupy the spindle poles during the 
succeeding mitosis, and in the spermatids perform the usual functions of 
blepharoplasts. Belajeff regarded this as a strong confirmation of his 
theory that the blepharoplast and centrosome are homologous organs. 

FIG. 31.- T w o 
stages in the sperma- 
togenesis of Nephro- 

A, blepharoplasts 
near poles of ppindle 
in last spermatogeri- 
ous mitosis. B, elon- 
gation of blepharo- 
plast near nucleus. 
Nebenkorn at left. 
(After Yamanouchi, 



The results of Shaw were in the main confirmed by the later work of 
Sharp (1914), who, however, saw in the achromatic structures accom- 
panying the blepharoplast striking evidence in favor of Belajeffs view 
of its homology. In line with this conclusion the suggestion has recently 
been made (Sharp 1920) that the fragmentation of the blepharoplast 
in Blasia, Equisetum, Marsilia, and the cycads may be homologized with 
the normal division exhibited by ordinary centrosomes. 

FIG. 32. Spermatogenesis in Marsilia quadrifolia. 

A, first spermatogenous mitosis; no centrosomes. #, second mitosis, centrosomes 
present. C, third mitosis; centrosomes present; old centrosome divided and degenerating 
in cytoplasm. Z), penultimate spermatogenous cell; daughter centrosomes separating. 
E, last spermatogenous mitosis; blepharoplasts (centrosomes) becoming vacuolate. F, frag- 
mentation of blepharoplast in spermatid. G, transformation of spermatid into spermato- 
zoid. //, free swimming spermatozoici. X 1400. (After Sharp, 1914.) 

Gymnosperms. The first known blepharoplast in plants above the 
algae was discovered in Ginkgo by Hirasd in 1894. He observed two, one 
on either side of the body cell nucleus, and because of their great simi- 
larity to certain structures in animal cells he believed them to be attrac- 
tion spheres. In 1897 Webber observed the same bodies, and noted their 
cytoplasrnic origin. On account of certain differences between these 
organs and ordinary centrosomes he expressed the opinion that they are 
not true centrosomes, but distinct organs of spermatogenous cells. 
The blepharoplast of Ginkgo was later investigated by Fujii (1898, 1899, 
1900) and Miyake (1906). 



In 1897 and 1901 Webber described the blepharoplast of Zamia (Fig. 
33). Up to the time of the division of the body cell the two blepharo- 
plasts, which arise de novo in the cytoplasm, are surrounded by radiations, 
but they have no part in the formation of the spindle, which is entirely 
intranuclear. During mitosis they lie opposite the poles, increase greatly 
in size, become vacuolate, and break up to many granules : these in the 
spermatid coalesce to form a spirally coiled cilia-bearign band lying just 
inside the cell membrane. In his full account (1901) Webber gives an 
extensive discussion of the homology of the blepharoplast. 

FIG. 33. Spermatogenesis in Zamia. 

A-E, five stages in the vacuolation and fragmentation of the blcpharoplast during the 
mitosis differentiating the spermatids. F, the two spermatozoids in the end of the pollen 
tube; prothallial and stalk cells below. Compare Fig. 34. A-D, X 350; E, X 1200. 
(After Webber, 1901.) 

In Ikeno's (1898) account of gametogenesis and fertilization in Cycas 
it was shown that the blepharoplasts appear in the body cell, lie opposite 
the spindle poles during mitosis, and break up to granules which fuse to 
form the spiral band in a manner similar to that described by Webber for 
Zamia. The behavior of the blepharoplast in Microcycas (Caldwell 
1907) is essentially the same. 

Chamberlain (1909) observed in the cytoplasm of the body cell of 
Dioon (Fig. 34) a number of very minute " black granules " which he was 
inclined to believe originate within the nucleus. Very soon two undoubted 
blepharoplasts are present, and are apparently formed by the enlarge- 



ment of two of the black granules. Very conspicuous radiations develop 
about them, and after mitosis they form ribbon-liko cilia-bearing bands 
in the spermatids as in the other cycads. 

FIG. 34.- Spermatogenesis in Dioon edulc. 

A, "body cell," with black granules in cytoplasm. X 1890. B, two blepharoplasts 
differentiated. X 1890. C, body cell with two blepharoplasts; prothallial and stalk cells 
below. X 237. />, fragmentation of blepharoplast in spermatic! as spiral band begins to 
form. X 1890. E, portion of edge of spermatozoid, showing spiral band cut at two points 
and cilia growing from it. X 945. (After Chamberlain, 1909.) 

Ikeno in 1898 expressed the opinion that the blepharoplast of Ginkgo 
and the cycads is a true centrosome, a view shared by Chamberlain (1898) 
and Guignard (1898). Two additional papers dealing with this subject 
were published by Ikeno (1904, 1906). In the first of these he made 
comparisons with analogous phenomena in animals which he believed to 


sustain the homologies suggested by Belajeff. He pointed out that in 
Marchantia centrosomes are present in all the spermatogenous divisions, 
whereas in other liverworts they appear much later, and from this he 
argued that the bryophytes show various stages in the elimination of the 
centrosome. He strongly reasserted his belief that blepharoplasts are 
centrosomes, and spoke of the "transformation of a centrosome into a 
blepharoplast " in the development of a spermatid into a spermatozoid. 
The ectoplasmic blepharoplasts of the algae were also held to be derived 
from centrosomes. In the second paper he insisted less strongly upon the 
morphological identity of all blepharoplasts, separating them into three 
categories : (1) centrosornatic blepharoplasts, including those of the myxo- 
mycetes, bryophytes, pteridophytes, and gymnosperms; (2) plasmoder- 
mal blepharoplasts, including those of Chara and some Chlorophyceae; 
(3) nuclear blepharoplasts, found only in a few flagellates. 

For a further discussion of this question the student is referred to 
the present author's papers on Equisetum and Marsilia. The main 
conclusions reached may be stated in two extracts from the former paper: 

Although limited to a single mitosis in the anthcridium, the blepharoplast 
[of Equisetum] retains in its activities the most unmistakable evidences 6f a 
centrosome nature, and at the same time shows a metamorphosis strikingly like 
that in the cycads. In thus combining the main characteristics of true centro- 
somes with the peculiar features of the most advanced blepharoplasts, it reveals 
in its ntogeny an outline of the phylogeny of the blepharoplast as it is seen 
developing through bryophytes, pteridophytes, and gymnosperms, from a func- 
tional centrosome to a highly differentiated cilia-bearing organ with very few 
centrosome resemblances. 

The activities of the blepharoplast in Equisetum [Marsilia, and Blasia], 
taken together with the behavior of recognized true centrosomes in plants and 
analogous j henomena in animals, are believed to constitute conclusive evidence 
in favor of the theory that the blepharoplasts of bryophytes, pteridophytes, and 
gymnosperms are derived ontogenetically or phylogenetically from centrosomes. 

Animals. The early researches of Moore (1895), Meves (1897, 1899), 
Korff (1899), Paulmier (1899), and many other more recent investigators 
have established the fact that the centrosome (or centrosomes) of the 
animal spermatid plays an important role in the formation of the motor 
apparatus of the spermatozoon, the axial filament of the tail growing out 
directly from it (Fig. 35). Henneguy (1898) even saw flagella attached 
to the centrosomes of the mitotic figure in the spermatocyte of an insect, 
an observation which has been often repeated. Wilson (1900, p. 175) 
concludes that "the facts give the strongest ground for the conclusion 
that the formation of the spermatozoids agrees in its essential features 
with that of the spermatozoa . . . " and that the blepharoplast is 
without doubt to be identified with the centrosome. 



Although there is comparatively little question that the granule at the 
base of the flagellum in the flagellates, like the body from which the axial 
filament of the spermatozoon grows, is of centrosomic nature, the nature 
of the basal granules in Ciliata and in the ciliated epithelial cells of higher 
animals is much more difficult to determine. It was held by Henneguy 
(1897), Lenhoss^k (1898), Hertwig (1902), and others that these granules, 
like the basal granules of flagella, are modified centrosomes; whereas 
certain other investigators (Maier 1903, Studnicka 1899, Schuberg 1905) 
have found evidence in favor of a contrary interpretation. An extensive 

Km. 35. Spcrmatogenesis in Hclijc iHwiatin, KKJ. 36. Diagram of a ciliated epi- 

Hhowing growth of flagcllum from outer centre- thelial coll. (Constructed from figures of 
Home, and elongation of inner centrosome to Saguchi, 1917.) 
form axial filament of middle piece. (After 
Korff, 1899.) 

discussion of this question is given by Erhard (1911), who concludes that 
although the basal corpuscles arise from the nucleus in a manner similar 
to that of the centrosomes of such cells, the evidence is on the whole 
unfavorable to the theory of Henneguy and Lenhossek. 

Still more recent are the researches of Saguchi (1917), who describes 
in great detail the insertion of the cilia in epithelial cells. At the base 
of each cilium, which itself shows no internal structural differentiation, 
there is always a basal corpuscle (Fig. 36). These corpuscles, and hence 
the cilia, are in parallel rows; and 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 the cytoplasmic recti- 
culum. Cilium, corpuscle, rootlet, and cytoplasmic strand form one 
continuous structure. Saguchi believes that neither the cilium nor the 
rootlet causes the ciliary movement, but that the kinetic center of this 
movement is in the basal corpuscles, as Henneguy and Lenhossek thought. 
Contrary to the opinion of those authors, however, he regards the ciliary 


apparatus as entirely independent of centrosomes, holding rather that it 
is produced by the differentiation of chondriosomes, and that the resem- 
blance of ciliated cells to spermatids, in which centrosomes do produce 
the motor apparatus, is an accidental one. 

Conclusion. In conclusion it may be said that it is highly probable 
that cilia-bearing structures are not homologous in all plant and animal 
groups. It is beyond question that in animals the centrosomes of the 
spermatid produce the motor apparatus of the spermatozoon. That a 
similar interpretation is to be placed upon the blepharoplasts in the sper- 
matids (androcytcs) of bryophytes, pteridophytcs, and gymnosperms 
appears to be equally well demonstrated. The blepharoplasts of the 
flagellates are also probably centrosomic in nature, at least in certain 
cases. In the " plasmodermal blepharoplasts" of motile alga cells we 
have organs which, in the light of our present knowledge, do not appear 
to belong to the centrosomic category, but final disposition of them must 
await further information concerning those alga? which possess both cen- 
trosomes and blepharoplasts. It can scarcely be doubted that the basal 
corpuscles of ciliated cells represent organs belonging to various categories. 
It must be left for further research to determine just how far these 
structures, which arc functionally analogous, are homologous with each 
other and with other cell organs. 

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La Cellule 21: 193-238. pis. 1, 2. 
GRIGGS, R. F. 1912. The development and cytology of Rhodochytrium. Bot. Gaz. 

63: 127-173. pis. 11-16. 
GUIGNARD, L. 1889. Developpement et constitution des anthe'rozoidos. Rev. 

Gen. Bot. 1: 11-27, 63-78, 136-145, 175-194. pis. 2-6. 

1898. Centrosomes in Plants. Bot. Gaz. 26: 158-164. 

GUILLIERMOND, A. 1904. Rechcrchcs sur la karyokinese chez les ascomyce^tes. 

Rev. Gfri. Bot. 16: 129-143. pis. 14, 15. 
1905. Remarques sur la karyokinese des ascomycetes. Ann. Mycol. 3: 344-361. 

pis. 10-12. 
1911. Apergu sur 1'evolution nucleairc des ascomycetes et nouvelles observations 

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284. pis. 11, 12. 

1899. Cell division in sporangia and asci. Ann. Bot. 13; 467-525. pis. 24-26. 
1905. Sexual reproduction and the organization of the nucleus in certain mildews. 

Carnegie. Inst. Publ. 37. Washington. 

1919. The structure of protoplasm. Am. Jour. Bot. 6: 273-300. 
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Trypanosoma theileri. Arch. Protistenk. 38: 355-374. pis. 14, 15. figs. 6. 
HENNEGUY, L. F. 1897. Sur les rapports des cils vibratiles avec les Centrosomes. 

Arch, d' Anat Micr. 1 : 481-496. figs. 5. 
HIRASE, S. 1894. Notes on the attraction spheres in the pollen cells of Ginkgo biloba. 

Bot. Mag. Tokyo 8 : 359. 
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108-117. pi. 6. 
HUMPHREY, H. B. 1906. The development of Fossombronia longiseta Austr 

Ann. Bot. 20: 83-108. pis. 5, 6. figs. 8. 


IKENO, S. 1898. Untersuchungen iiber die Entwicklung der Geschlechtsorgane und 
den Vorgang der Befruchtung bei Cycas revoluta. Jahrb. Wiss. Bot. 32 : 557-602. 
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1903. Die Sperm at ogenese von Marchantia polymorpha. Beih. Bot. Centralbl. 
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1904. Blepharoplasten im Pflanzenreich. Ibid. 24: 211-221. figs. 1-3. 

1906. Zur Frage nach der Homologie der Blepharoplasten. Flora 96 : 538-542. 
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Schwarmern von Stemonitis flaccida Lister. Ber. Deu. Bofc. Gesell. 22 : 84-92. 

pi. 6 
KARHTEN, G. 1900. Die Auxosporenbildung der Gattungen Cocconeis, Surirella, 

und Cymatopleura. Flora 87 : 253-283. pis. 8-10. 
KOERNICKE, M. 1903. Der heutige Stand der pflanzlichen Zellforschung. Ber. 

Deu. Bot. Gesell. 21: (66)-(134). 

1906. Zentrosomen bei Angiosperrncn ? Flora 96: 501-522. pi. 5. 
VON KORFF, K. 1899. Zur Histogenese der Spermien von Helix pomatia. Arch. 

Mikr. Anat. 64: 291-296. pi. 16. 
KUCZYNSKI, M. H. 1917. Ueber die Teilung der Trypanosornenzelle nebst Benier- 

kungen z-ur Organization einiger nahestehcnder Flagellaten. Arch. f. Protistenk. 

38: 94-112. pis. 3, 4. 
LAUTERBORN, R. 1896. Untersuchungen tiber Ban; Kernteilung, und Bcwegung 

der Diatomen. Leipzg. 

VON LENHOSSEK, M. 1898. Ueber Fliinmerzellen. Verh. Anat. Ges. Kiel 12: 100. 
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crystallina. Bot. Gaz. 41: 109-138. pis. 5-9. 
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Arch. f. Protistenk. 2. 
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3: 123-154. pis. 3-5. 
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Jour. Morph. 14: 181-218. 
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maculosa. Arch. Mikr. Anat. 60: 110-141. pis. 7, 8. . 
1899. Ueber Struktur und Histogenese der Samenfaden dcs Meerschweinchens. 

Ibid. 64: 329-402. pis. 19-21. figs. 16. 
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wicklungsgeschichte des Sporogons der Corsinia marchantioides. Bull. Soc. Imp. 

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MINCHIN, E. A. 1912. An Introduction to the Study of the Protozoa. London. 
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1773-1780. figs. 10. 
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genesis of elasmobranchs. Quar. Jour. Micr. Sci. 38: 275-313. pis. 13-16. 
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339-361. pi. 19. 
1899. The action of salt solutions on the unfertilized and fertilized eggs of Arbacia 

and other animals. Ibid. 8: 448-539. pis. 7-10. figs. 21. 
MOTTIER, D. M. 1898. Das Centrosom bei Dictyota. Ber. Deu. Bot. Ges. 16: 

123-128. figs. 5. 


1900. Nuclear and cell division in Dictyota dichotoma. Ann. Bot. 14: 166-192. 

pi. 11. 

1904. The development of the spermatozoid of Chara. Ibid. 18 : 245-254. pi. 17. 
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Suppl. 223-272. pis. 13, 14. 
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159-180. pi. 11. 

SAGUCHI, S. 1917. Studies on cjliated cells. Jour. Morph. 29: 217-279. pis. 1-4. 
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Deu. Bot. Ges. 31: 14-66. fig. 1. 
SCHAFINER, J. H. 1908. The centrosomes of Marchantia potymorpha. Ohio Nat 

9. 363-388. 
SCHOTTLANDER, P. 1893. Beitrage zur Kenntniss des Zellkerns und der Sexual- 

zellen bei Kryptogamen. Cohn's Beitr. Biol. Pflanzen 6: 267-304. pis. 4, 5. 
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1914. Spermatogenesis in Marsilia. Ibid. 58: 419-431. pis. 33, 34. 
1920. Spermatogenesis in Blasia. Ibid. 69: 258-268. pi. 15. 
SHAW, W. R. 1898. Ueber die Blepharoplasten bei Onoclea und Marsilia. Ber. 

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und das Wesen der Befruchtung. Hist. Beitr. 4 : 49-158. pi. 3. 
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pis. 27, 28. 

1900. Ueber Reduktionstheilung, Spindclbildung, Centrosomen, und Cilienbildner 
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Beriicksichtigung der Centrosomenfrage. Sitz-Ber. K. Bohmisch. Ges. Wiss. 

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THOM, C. . 1899. The process of fertilization in Aspidium and Adiantum. Trans. 

Acad. Sci. St. Louis 9: 285-314. pis. 36-38. 
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Hydrodictyon. Trans. Wis. Acad. Sci. 13: 486-522. pis. 29, 30. 
VAN HOOK, J. M. 1900. Notes on the division of the cell and nucleus in liverworts. 

Bot. Gaz. 30 : 394-399. pis. 2 ; 3. 
WEBBER, H. J. 1897a. Peculiar structures occurring in the pollen tube of Zamia. 

Bot. Gaz. 23:453-459. pi. 40. 

18976. The development of the antherozoid of Zamia. Ibid. 24: 16-22. figs. 5. 
1897c. Notes on the fecundation of Zamia and the pollen tube apparatus of 

Ginkgo. Ibid. 24: 225-235. pi. 10. 

1901. Spermatogenesis and fecundation in Zamia. U. S. Dept. Agr. Pit. Ind. 
Bull. 2. pp. 100. pis. 7. 

WILLIAMS, J. L. 1904. Studies in the Dictyotaceae. II. The cytology of the game- 
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WILSON, E. B. 1900. The Cell in Development and Inheritance, (p. 175.) 

1901. Experimental Studies in Cytology. I. A cytological study of partheno- 
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WILSON, M. 1911. Sperm atogenesis in the Bryophyta. Ann. Bot. 25: 415-457. 

pis. 37, 38. figs. 3. 
VON WINIWARTER, H. 1912. Observations cytologiques sur les cellules interstiti- 

dlles du testicule humaine. Anat. Anz. 41 : 309-320. pis. 1-2. 
WOLFE, J. J. 1904. Cytological studies on Nemalion. Ann. Bot. 18: 607-630. 

pis. 40, 41. fig. 1. 
WOODBURN, W. L. 1911. Spermatogenesis in certain Hepaticae. Ann. Bot. 25: 

299-313. pi. 25. 

1913. Spermatogenesis in Blasia pusilla. Ibid. 27: 93-101. pi. 11. 
1915. SpermatogenesiH in Mnium affme, var. ciliaris (Grev.), C.M. Ibid. 29: 

441-456. pi. 21. 
YAMANOUCHI, 8. 1906. The life history of Polysiphonia violacea. Bot. Gaz. 42: 

401-446. pis. 19-28. 

1908. Spermatogenesis, ocigenesis, arid fertilization in Nephrodium. Ibid. 45: 
145-175. pis. 6-8. 

1909. Mitosis in Fucus. Ibid. 47: 173- 197. pis. 8-11. 

ZIMMBRMANN, A. 1893-1894. Sammel-Referate. 6. Die Centralkorper und die 
Kerntheilung. 12. Die Cilien und Pseudocilien. Beih. Bot. Centralbl. 3: 
342- 354; 4: 169-171. 



Next to the nucleus, the most conspicuous organ held within the 
cytoplasm of the plant cell is the plastid. Cytologists have long been 
aware of the important physiological roles played by plastids of various 
types in the life of the cell, but it is only recently that an added inter- 
est has been given these organs by the discovery that certain peculiar 
characters showing definite modes of inheritance are closely bound up 
with their behavior. Such problems are complicated by the relation 
apparently borne by plastids to chondriosomes. In the present chap- 
ter will be set forth some of the more important facts regarding these 
two classes of cell elements. 

General Nature and Occurrence. Plastids are differentiated portions 
of the protoplasm, as von Mohl long ago pointed out, and represent 
regions in which certain processes have become localized (Harper 1919). 
In view of their power of growth and division and their definite relation to 
certain important physiological functions they are to be regarded as 
distinct cell organs. 

Although plastids can be found in the cells of both animals and plants 
they are chiefly characteristic of the latter, where they are present in 
one form or another in all groups with the possible exception of bacteria, 
myxomycetes, and certain fungi. They are abundant only in those plant 
parts which have to do with specialized physiological functions. Within 
a single cell there may be regularly but one plastid, as in many a'gae, 
Anthoceros, and the meristematic cells of Selaginella (Haberlandt 1888, 
1905) ; or two, as in Zygnema; or a jjgher 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. Ihe positions which they assume within the cell are fre- 
quently related in a definite manner to certain external conditions: in 
the palisade cells of green leaves, for example, the chloroplasts are found 
near the upper surface if the incident light is weak, whereas they react to 
strong illumination by taking up less exposed positions along the lateral 

Plastids may be conveniently classified on the basis of their contained 
coloring matters. This difference in color, however, is secondary in 
importance; the fundamental distinction is that based upon the kind of 




physiological work being done, the various pigments being associated in 

intimate manner with different reactions occurring within the plastids. 

Leucoplasts. Leucoplasts are relatively small and colorless. They 

found commonly in the cells of meristematic tissue, and may be 

'ned in some kinds of differentiated cells, such as the glandular hairs of 

wnium. Kiister (1911) states that the leucoplasts of Orchis are 

iuid in consistency, undergoing amoeboid changes of shape and 

multiplying by irregular fission. The smaller leucoplasts appear to 

represent juve/rile stages in the development of plastids of more highly 

differentiated types, for under certain conditions they develop into the 

larger and more highly specialized leucoplasts known as amyloplasts, and 

into the various kinds off* Chromatophores mentioned below. 

Chromatophores. Chromatophores, or chromoplasts, arc plastids bear- 
ing one or more pigments, and having thus a more or less decided 
color. In green plants the most important of these pigments are chlo- 

FIG. 37. - Various forms of plastids. 

A, Draparnaldia. B, Spirogyra. C, Anthoccros. D, rhromoplasts of Ariscrma. E, 
cell of Selaoinella, showing position assumed by plastid in response to light (direction shown 
by arrow). A, B, and (' show pyrenoids. (E After Haberlandt.) 

rophyll, carotin, and xanthophyll. Chlorophyll is apparently a combi- 
nation of two simpler pigments, chlorophyll a and chlorophyll 6. The 
cells of the Phseophycese, Cyanophycese, and Rhodophycese are character- 
ized respectively by the presence of yellow carotin, blue phycocyanin, 
and red phycoerythrin, in addition to chlorophyll. The Cyanophycese 
exhibit an especially rich variety of pigments, which in many cases do not 
appear to be held within definite Chromatophores. 1 

Chromatophores are usually spherical, ovoid, or discoid in shape, but 
many peculiar forms are known, particularly among the green algae. In, 
Ulothrix the chloroplast has the form of a complete or incomplete hollow 
cylinder; in Draparnaldia (Fig. 37, -4), a hollow cylinder with very 

1 For the literature pertaining to plant pigments see Palladin 1918. See also 
Haas and Hill (1913), Willstatter and Stoll (1913), Jorgensen and Stiles (1917), 
Wheldale (1916), and Beauverie (1919). The distribution of carotin is discussed in 
an earlier paper by Tammes (1900). 


irregular ends; in jEdogoniuw, an irregular parietal net; in Spirogyra 
(Fig. 37, B), a spirally coiled ribbon; and in the desmids, a series of 
radiating plates (Carter 1919, 1920). The chromatophore of Antho- 
ceros (Fig. 37, C) is spindle-shaped, becoming chain-like in the elongated 
columella cells (Scherrer 1914). The chromatophore of Selaginella 
may also assume this form (Haberlandt 1888). The chromoplasts of 
Ariscema (Fig. 37, D) are frequently sharply angular. In the Clado- 
phoraceae (Carter 1919) the cell is completely lined by a thin chromato- 
phore which may be entire or fenestrated. In many cells irregular strands 
pass inward through the cell cavity. Indeed it seems not improbable 
that ia some such cases the plastid may be not at all sharply distinct 
from the rest of the cytoplasm, the two grading one into the other, and 
the chlorophyll at certain stages permeating all parts of the cytoplasm. 
The observations of Timberlake and Harper appear to show that such is 
the condition in the young cells of Hydrodictyon. Thus the physiological 
processes show various degrees of localization in the cell, causing manifold 
degrees of structural transformation and delimitation of the cytoplasmic 
regions involved (Harper). 

Of all chromatophores the chloroplasts stand first in importance, for 
they bear the green pigment, chlorophyll, which, in the presence of 
light, enables them to combine water from the soil or other surrounding 
medium with carbon dioxide from the atmosphere to form carbohydrates, 
the first visible product being starch. The chloroplasts are therefore 
the world's ultimate food producers. In addition to chlorophyll other 
pigments, notably xanthophyll, are usually present. Although the body 
of the chloroplast can be developed in darkness, the chlorophyll will 
usually not be elaborated unless light is present. Most young seedlings 
grown in the absence of light show a pale yellowish color, which is due to a 
substance known as chlorophyllogen, contained in the plastids. When 
such " etiolated" plants are placed in the light the plastids become green, 
apparently through an alteration of the chlorophyllogen to chlorophyll 
(Monteverde and Lubimenko 1911). Other conditions necessary for the 
development of chlorophyll are a favorable temperature and the presence 
of iron, oxygen, and certain carbohydrates. 

The structure of the chloroplast is an extremely difficult matter to 
determine, and has been the subject of some controversy. It is generally 
thought that the body of the plastid is composed of a finely fibrillar 
meshwork, the stroma, which may be somewhat denser at the periphery, 
and that the coloring matters are held in the meshes of the stroma in the 
focm of minute droplets. No limiting membrane is definitely known. 
The included droplets are apparently not composed of the pigments alone : 
it is probable that they are rather globules of some oily or fatty material 
containing the pigments in solution. The pigments may easily be dis- 
solved out with alcohol and other reagents. On the other hand, it has 



been held by some observers that the stroma is a homogeneous body in 
which the droplets of chlorophyll solution are imbedded, and that the 
reticular structure so often reported is an artifact due to the reagent 
employed in removing the chlorophyll. By others the pigment has been 
thought to form a layer about the plastid. In any case it seems evident 
that the chlorophyll is not uniformly distributed throughout the stroma. 
In chroma tophores other than chloroplasts the pigments may at times 
take the form of solid granules or crystals. 

Starch. After a period of photosynthetic 
activity the chloroplast contains starch, the first 
visible product of that activity, in the form of 
minute granules. This " assimilation starch" is 
formed within the body of the chloroplast, as 
Meyer originally showed (Fig. 38, A, B). It is 
later transformed through the agency of enzymes 
into some soluble compound, usually a sugar; in 
this 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 the ordinary 
"reserve starch/' or "storage starch." This de- 
position of reserve starch is brought about through 
the agency of amyloplasts, which are leucoplasts 
capable of changing already elaborated organic 
materials, such afe glucose, into starch (Fig. 38, C). 
Reserve starch, upon which we depend so 
largely for food, is a carbohydrate with a composi- 
tion expressed by the general formula (C 6 Hi 05)n, 
and exists in the form of granules ranging in size 
approximately from 2^ to 200//, in different plants. 
Potato-starch grains are usually about 90^ in 
diameter. The reserve starch grain is formed 
within the body of the arnyloplast, and is made 
up of a series of concentric layers successively 
laid down about a center, or "hilum" (Fig. 39, A). 1 In case the grain 
starts to form near the middle of the amyloplast it may develop sym- 
metrically, but commonly the developing grain lies near the periphery 
of the amyloplast, which becomes greatly distended as the grain grows. 
Material is thus deposited unevenly upon the grain so that the latter 
becomes very eccentric; in extreme cases the grain ruptures the amylo- 
plast and remains in contact with it only at one side, where all new 
material is then deposited. Several grains may start to develop simul- 

1 For the structure of the starch grain see the papers of Nageli, Schimper, Meyer, 
Binz, Dodel, Salter, and Kramer. 

FIG. 38.- Formation of 
starch by plastids. 
A, dividing chloro- 
plasts of Funaria, with 
grains of assimilation 
starch. X 940. (After 
Ktraaburger.) B, chloro- 
plast of Zygnema, with 
several large starch 
grains about a central 
pyrenoid. (After Bour- 
quin, 1917.) C, leuco- 
plast (amyloplast) in 
aerial tuber of Phajus 
grandifolius with grain 
of reserve starch. (After 



taneously in a single amyloplast, later growing together to form a 
" compound grain " with more than one hilum. In case the parts making 
up the compound grain are enveloped in one or more common outer 
layers the grain is said to be " half-compound." Potato starch is made 
up of simple, compound, and half-compound grains, whereas in oats 
and rice all or nearly all of the grains are said to be of the compound type. 
The successively deposited layers making up the grain differ mainly in 
water content, the innermost layers being richest and the outermost 
poorest in water. As a result of this non-uniform composition the grain 
often splits radially when dried. 


FIG. 39, Reserve starch grains from various plants. 
A, potato; simple and half-compound grains. B, Colombo starch. 
D, pea. E, maize; intact arid partially digested grains. F, rye. Cr, maize. 
7, bean. /, rice. K, wheat. (After Tschirch.) 

C, arrowroot. 
//, Euphorbia. 

As a result of his classic researches Nageli (1858) advanced the theory 
that the starch grain is made up of ultramicroscopic crystalline particles 
which he called "micelke," these being surrounded by water films of 
varying thickness. It was similarly held by A. Meyer (1883, 1895) 
that the grain is composed of radially arranged needle-shaped crystals 
known as "trichites;" these are composed of a- and /3-amylose which 
turn blue with iodine. In some starch amylodextrin and dextrin are 
also present, such grains turning red with iodine. Both Nageli and Meyer 
held the stratification of the grain to be due to the varying numbers of 
the crystalline units in the successive layers, and Meyer showed that in 
certain cases it is correlated with the alternation of day and night, and 
therefore with a periodic activity on the part of the plastid. This con- 
clusion was confirmed by Salter (1898). 

The statement made by Schimper (1880) and Meyer (1883, 1895) that 
starch is always formed by plastids still holds good in its essential feature : 
so far as is certainly known no primary product of photosynthesis is 
formed in the cytoplasm apart from plastids, although in some cases, 
such as the young cells of Hydrodictyon, according to Harper, it is very 
difficult or even impossible to distinguish the limits of these organs, Tjp$ t 


granules of paramylum in Euylena and those of "Florideaii starch" in 
the red algae first appear in the cytoplasm; but, although they are the 
first substances which are visible, it is highly probable that they arise 
through the transformation of a non-visible product (sugar?) of the 
photosynthetic activity of the plastids, and are not immediately built 
up from water and carbon dioxide. A similar interpretation may be 
placed upon corresponding appearances reported in the case of higher 
plants. Owing to the great difficulty of determining the true cell struc- 
ture of the Cyanophyceae (see p. 202) it is possible to speak of plastid 
activity in such forms only with great reserve. If, as Olive (1904) and 
Gardner (1906) hold, these cells are without plastids, the product of 
photosynthetic activity, commonly glycogen, must be elaborated in the 
cytoplasm without their aid. If, on the other hand, the peripheral 
portion of the protoplast represents a large chromatophore (Fischer 1898), 
or cytoplasm containing a large number of minute chromatophores 
(Hegler 1901, Kohl 1903, Wager 1903), the photosynthetic process, 
although it may result in the production of a different substance, is 
dependent upon the powers of definite protoplasmic organs much the 
same as in higher plants. Among bacteria and other low forms in which 
it seems more certain that plastids and the ordinary pigments are absent, 
widely different types of metabolism are met with. For further discus- 
sion of this subject, which lies outside the scope of the present book, 
more special physiological works should be consulted. 

The Pyrenoid. The term pyrenoid was applied by Schmitz (1882) 
to the refractive kernel-like bodies imbedded in the chromatophores of the 
algae. Pyrenoids are characteristic of the Chlorophycese especially, 
being present almost universally in the members of this group. They 
are known in a few representatives of the IJiodophyceae (Nemalion 
arid the Bangiaceae), but apparently do not occur in the cells of the 
Cyanophyceae, Phaeophyceae, and Characeae. Very rarely they are 
present in forms above the algae: a conspicuous example is the liverwort 
Anthoceros. The chromatophore may contain but one pyrenoid, as in 
Zygnema, or a larger number, as in Spirogyra, Draparnaldia, and many 
other forms (Fig. 37). 

As held by de Bary (1858), Schmitz (1884), and Schimper (1885), 
the pyrenoid appears to be composed of a protein substance with a thick 
gelatinous consistency. When a single pyrenoid is present in the chroma- 
tophore it may multiply by fission along with the latter when the cell 
divides, while in those forms possessing several pyrenoids this multiplica- 
tion may be much more extensive. Also, as pointed out by Schmitz 
and Schimper, and more recently by Smith (1914), the pyrenoid may 
disappear and arise de novo from the cytoplasm or from the plastid 

With regard to its function, the early workers referred to above ob- 


served that under certain conditions the pyrenoid is closely surrounded 
by a mass of starch grains, and concluded that it is an organ, or portion of 
an organ (chromatophore), intimately concerned in the process of starch 
formation, its action being somewhat similar to that of the amyloplast. 
The pyrenoid, in fact, has often been likened to a leucoplast imbedded in 
the chromatophore; Wiesner, for instance, believed the pyrenoid to 
contain several leucoplast bodies, each of which gave rise to a starch 
grain. In general, more recent researches have emphasized the close 
association of the pyrenoid with the starch forming process, although 
the precise nature of this process remains very much in doubt. Accord- 
ing to Timberlake (1901) the pyrenoid in Hydrodictyon is differentiated 
from the cytoplasm and is very active in starch production, segments 
splitting off from its periphery and forming starch within them. In 
this way the entire pyrenoid may become a mass of " pyrenoid starch," 
as distinguished from ordinary, or "stroma starch." McAllister (1913) 
describes a similar splitting up of the pyrenoid to form several starch 
grains in Tetraspora. Yamanouchi (1913), however, in his description 
of a new species of Hydrodictyon, states that some of the chloroplasts 
give rise to starch while others give rise to pyrenoids, and that the 
latter have nothing to do with starch formation. 

A similar diversity of opinion exists with respect to the role of the 
pyrenoid in Zygnema. Chmielewskij (1896), who looked upon the 
pyrenoid as a permanent cell organ multiplying only by division, held 
that starch grains arise wholly from the substance of the pyrenoid, 
plate-like extensions of the latter being present between and in intimate 
contact with the developing grains. More recently Miss Bourquin 
(1917) asserts that the pyrenoid has nothing to do with the appearance 
of starch, the body of the chromatophore alone being concerned. She 
observes the starch grains appearing first near the periphery of the 
chromatophore entirely apart from the pyrenoid, the later formed grains 
differentiating in positions progressively nearer the pyrenoid (Fig. 38, B). 

The pyrenoid of Anthoceros (Fig. 37, C) as described by McAllister 
(1914) is in reality a group of about 25-300 small " pyrenoid bodies" 
which are probably composed of a protein substance. The outermost 
bodies become starch, new ones apparently being formed by the fission 
of those lying on the interior of the group. McAllister states that no 
pyrenoid is visible in the young sporogenous tissue, starch being formed 
without its aid. Somewhat later several small bodies appear and 
aggregate to form the pyrenoid. 

Cleland (1919) recently reports a close association of the pyrenoid 
of Nemalion with the formation of Floridean starch. 

Elaioplasts and Oil Bodies. In 1888 Wakker discovered in the cells 
of Vanilla planifolia and V. aromatica certain plastid-like bodies to 
which he gave the name elaioplasts, since they seemed to be concerned in 



the elaboration of oil (Fig. 40, A). They were soon observed in a number 
of monocotyledons by Zimmermann (1893), Raciborski (1893), and Ktis- 
ter (1894); and some time later in the flower parts of a dicotyledon, 
Gaillardia, by Beer (1909). Politis (1914) has found them in monocoty- 
ledonous plants belonging to 19 different genera, and in five genera of 
dicotyledons (Malvaceae). 

There is a considerable lack of agreement in the opinions expressed 
on the subject of the origin and significance of elaioplasts. Wakker 
thought it probable that they represent meta- 
morphosed chloroplasts, which they often closely 
resemble in structure (Ktister), whereas Raciborski 
asserted that they arise as small refractive gran- 
ules in the cytoplasm and multiply by budding. 
In the zygospores of Sporodinia grandis and 
Phycomyces nitens Miss Keene (1914, 1919) reports 
the presence of a number of globular structures 
with which oil is associated from their earliest 
stages. These unite to form one or two large 
reticulate bodies which Miss Kcenc believes are 
related to the elaioplasts of higher plants. All of 
these investigators, with Politis, agree that elaio- 
plasts arc normal cell organs with a special func- 
tion, namely, the formation of oily substances 
having a role in nutrition. Beer, on the contrary, 
FIG. 40. states that in Gaillardia they are formed secon- 

A, elaiopiast forming darily by the aggregation of many small degen- 

oil droplets in epidermal , .* i i* i i ^.i i ./ 

cell of perianth of PoK- crating plastids and their products at one or 
anthes tuberosa; nucleus more points in the cell, all stages of the process 

being observed. Although the bodies so formed 
#, oil bodies in may, if green, produce starch, or, if colorless, an 

oily yollow pigment, Beer thinks it probable that 
(AfterGargeannc, they have no important special function in the life 

of the plant. 

Closely associated with investigations on elaioplasts have been those 
concerned with the oil bodies found in the cells of many liverworts (Fig. 
40, B). These bodies, discovered by Gottsche in 1843, were first carefully 
described by Pfeffer (1874). Pfeft'er stated that they arise by the fusion 
of many minute droplets of fatty oil appearing in the cytoplasm of very 
young cells, and later come to lie in the cell sap; he further believed them 
to possess a special membrane. Wakker (1888) held them to be analo- 
gous to leucoplasts and chloroplasts, multiplying by fission at each 
cell-division, and pointed out that they lie in the cytoplasm rather than in 
the cell sap. He was inclined to view them as products of elaioplasts, 
which Ktister (1894) supposed them to resemble in having a spongy 
stroma containing oil in the form of minute droplets, 

right. Sn (After 



Quite different were the views of Gargeanne (1903). According to 
him they arise from vacuoles, their limiting membranes thus being the 
original tonoplasts. While in the juvenile vacuole stage they may multi- 
ply by division, but when once fully formed they remain unchanged and 
divide no further. Gargeanne observed small oil droplets moving about 
freely within the oil body, and hence concluded that the latter has a 
fluid consistency rather than a spongy stroma as K lister thought. 

The most noteworthy recent observations on oil bodies are those of 
Rivett (1918), who finds them to be very conspicuous in the cells of 
Alicularia scolaris. Rivett holds that they are in reality only oil vacuoles 
that they originate by the coalescence of numerous minute oil droplets 
secreted by the protoplasm in a manner entirely similar to that in which 
the ordinary sap vacuole arises (cf. Pfeffer). Although they become very 
large and project well into the sap vacuole, they continue to be surrounded 
by a thin film of cytoplasm. The oil body, in the opinion of Rivett, is 
therefore in no sense a plastid, nor is it formed by any special claioplast: 
it is simply an accumulation of ethereal and fatty oils together with some 
protein substance. The "membrane" observed by Pfeffer is the limiting 
layer of the surrounding cytoplasm, which may be slightly changed by 
contact with the oil. 

Accumulations of oil apparently quite similar to those in liverwort 
cells have been described in the cells of various angiosperms by a number 
of writers. To these the term elaiospheres was applied by Lidforss (1893). 

The published figures of claioplasts and oil bodies in many cases 
bear striking resemblance to those of fat- and oil-secreting chondrio- 
somes (see below), and it is not improbable that the problem of their 
origin and significance will be brought nearer solution by further studies 
of the latter class of bodies. 

The Eyespot. The so-called eyespot present in the flagellate cell and 
in the zoospores and gametes of many algae has certain characteristics 
in common with plastids, and may therefore receive consideration here. 
This body, which nearly all workers agree is a light-sensitive organ, 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 associa- 
tion with the chromatophore and the plasma membrane. (Overtoil 
1889; Klebs 1883, 1892; Johnson 1893; Strasburger 1900; Wollenweber 
1907, 1908). With respect to its mode of origin, it has been variously 
reported to arise de novo in each newly formed zoospore in several green 
algae (Overton); to develop from a colorless plastid in the young 
antheridial cell in the case of the spermatozoid of Fucus (Guignard 1889) ; 
to arise as a differentiated portion of the plastid in the zoospores and 
gametes of Zanardinia (Yamanouchi) ; and finally to multiply by fission 
at the time of cell-division in flagellates (Klebs 1892). 

It is generally agreed that the eyespot in many instances consists of 



a finely reticulate stroma in which an oily red pigment with many of the 
characteristics of hsematochrom is held in the form of minute droplets or 
granules (Schilling 1891; Klebs 1883; FranzS 1893; Wager 1900; Wollen- 
weber 1907, 1908) (Fig. 41, D). As shown by the careful researches of 
Franz, the stroma may also bear one or more refractive inclusions, 
which in the Chlarnydomonadacese and Volvocacese consist of starch, and 

in the Euglenoidese of paramylum (Fig. 41, 
E). These inclusions were thought by 
Franz6 to increase the sensitivity of the eye- 
spot by concentrating the light at certain 

The eyespot of the zoospore of Cladophora 
(Strasburger 1900) appears to arise as a 
swelling of the plasma membrane, and consists 
of an external pigmented layer beneath which 
is a lens-shaped mass of hyaline substance 
(Fig. 41, B). InGonium and Eudorina (Mast 
1916) the lens-shaped portion lies outside with 
the cup-shaped opaque portion beneath it 
(Fig. 41, A), an arrangement strongly sug- 
gesting the primitive eyes of certain higher 
organisms. In neither portion could any finer 
structure be detected. Mast has shown that 
the orientation of the colony is brought about 
through changes in the intensity of the light 
falling upon the light-sensitive substance. As 
the unorientcd swimming colony rotates on 
its axis, those zooids turning away from the 
light have the hyaline portion of their eye- 

Fia. 41. Kyespots of various 


A , zooid of Eudorina; e, eye- 
spot. (From Mast, After Grare.) 
B, zoospore of Cladophora, 
(After Straxburuer, 1900.) C, 
anterior end of Euylcna viridis, 
showing eyespot at surface of 
oesophagus, and in front of it a 
swelling on one root of the 

flagellum ; face view of eyespot spots shaded by the opaque cup; this sudden 

reduction in the amount of light energy 
received brings about an increase in the 
activity of the flagellse of those zooids, with 
the result that the colony as a whole turns 
more directly toward the source of light. 

In Euglena viridis the morphological con- 
nection between the eyespot and the motor apparatus is particularly 
close. Here Wager (1900) has shown that the eyespot, which is a 
discoid protoplasmic body containing a layer of large pigment droplets, 
is situated at the surface bounding the oesophagus in close contact with a 
swelling on one of the basal branches of the flagellum (Fig. 41, C). 

In general it may be concluded that the eye&pot in some cases bears in 
its structure, and to a certain extent in its evident function, such a close 
resemblance to the ordinary plastid that a relationship of some sort 

at right, showing pigment gran- 
ules. (After Wager, 1900.) D, 
eyespot of Euglena velata. 
(After Frame, 1893.) E, eye- 
spot of Trachchmonas volvo~ 
cina, with pigment granules 
and crystalloid body. (After 


between the two seems highly probable; whereas in other cases (Gonium, 
Cladophora) it appears to represent a differentiation of the ectoplast. 
It is more than likely that light-sensitive organs have arisen more than 
once in the evolution of the lower organisms, and that they cannot all 
be placed in the same category, 

The Individuality of the Plastid. 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. 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. Since it is known, however, that chloroplasts 
and other differentiated chromoplasts may arise from leucoplasts through 
the development of pigments and other characters in the latter, and also 
that the individual plant arises from sex cells or a spore in which the 
plastids are usually in a colorless and relatively undifferentiated state, the 
problem of the individuality of the plastid is mainly one of determining 
whether these undifferentiated plastids, leucoplasts, or "plastid primor- 
dia" 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. At this point 
we may review certain cases in which the plastid has been followed 
through gametogenesis and fertilization. 

In Zygnema (Kurssanow 1911) 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 contrib- 
uted by the "male" gamete degenerate, leaving the two furnished by 
the "female" gamete as the plastids of the new individual* 

In Coleochcete (Allen 1905) each vegetative cell and gamete has one 
nucleus and one plastid : after the sexual union of the gamete nuclei the 
fertilized egg therefore contains one nucleus and two plastids. These two 
plastids divide at the first division of the fertilized egg but not at the 
second, the four resulting cells consequently having one plastid each. 
In the third cell-division the plastids algo divide, so that each cell of 
the several-celled structure developing from the fertilized egg has its 
single plastid. Each of the several cells eventually becomes a zoospore 
' which" germinates to produce a new Coleochcete body with a single plastid 
in each cell, the plastid dividing with the nucleus at each cell-division. 

A somewhat similar regularity in the behavior of the plastid is shown 
in Anthoceros (Davis 1899; Scherrer 1914). Each game tophy tic cell 



contains a single plastid which divides with the nucleus at each cell- 
division. The egg likewise contains a plastid, but the spermatozoid has 
none: the fertilized egg and sporophyte cells which it later forms are 
therefore characterized, like the cells of the garifetophyte, 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. As 
shown by Davis (Fig. 42), the sporocyte plastid divides twice during the 
prophases of the first (heterotypic) division of the sporocyte nucleus, so 
that each spore of the resulting tetrad receives one. Upon germination 
the spore produces ar gametophyte with one plastid in each cell, and the 
cycle is complete. 

FIG. 42. The behavior of the plastid in the sporocyte of Anthocerox. 
A, sporocyte with single nucleus and plastid. B, plastid divided; nucleus in prophase 
of mitosis. C, plastids divided to four; two nuclei present. D, three of the four spore 
cells, each of which has a single nucleus and plastid. (After Davis, 1899.) 

In all of the foregoing examples it is evident that the plastids, as 
stated by Scherrer for Anthoceros^ 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 (1915), who 
has also studied the behavior of the plastids in Selaginella and Isoetes 
(1911, 1913). In such cases the plastids each possess an individuality com- 
parable to that of nuclei, from which they differ conspicuously, however, 
in undergoing no fusion at the time of fertilization. The constancy in 
number is nevertheless maintained : by the degeneration of the plastids of 
one gamete in Zygnema; by their failure to divide at one cell-division in 
Coleochcete; and because of the fact that the male gamete carries no 
plastid in Anthoceros. It appears to be generally true that while the eggs 
in all plant groups contain plastids (usually leucoplasts), the latter are 
present in male gametes in the algae only. Sapehin (1913), however, 
believes that the blepharoplasts of the higher groups represent plastids. 

It should be said that only in a comparatively few forms has such a 
regularity in the behavior of the plastid as that outlined abov'e been 
demonstrated. A number of investigators, working on a great variety of 
cells, have been forced to conclude that plastids are either formed de novo 
as well as by division, or are carried through certain stages of the life 


cycle in some less conspicuous form. If they represent regional trans- 
formations of the cytoplasm resulting from the localization of certain 
processes, they might wellbe expected to differentiate anew as these 
processes begin in the life of the cell, and to preserve varying degrees 
of permanence depending upon the processes carried on (Harper). 
Their individual continuity through certain life cycles would accordingly 
be interpreted to mean that in such forms there is a persistence of certain 
types of physiological activity through all stages. 

In recent years a number of cytologists have described the develop- 
ment of plastids from minute granular primordia in the cytoplasm, and 
have attempted to show that these primordia are members of the class of 
cell inclusions known as chondriosomes. A general theory of the indi- 
viduality of the plastid must therefore involve the question of the relation 
of plastids to chondriosomes, and the further question of the origin of the 
chondriosomes themselves. These matters will be taken up in the fol- 
lowing pages. x" 


Notwithstanding the large amount of work which has been done upon 
chondriosomes during recent years, the condition of opinion as to their 
origin, behavior, and significance is still so unsettled that little more than 
a review and partial classification of the more prominent views will 
here be attempted. 

Chondriosomes were probably first observed many years ago by 
Flemming and Altman in the course of their studies on protoplasm. 
They were first clearly described by La Vallette St. George (1886), who 
observed them in the male cells of animals and called them "cytomicro- 
somes." In plants they were first described by Meves (1904) in the 
tapetal cells of the anthers of Nymphcea (Fig. 43, B). Benda in 1897 
and the following years discovered them in cells of many types, notably 
in the spermatogenous cells of animals, and applied to them the term 
"mitochondria." It was not until a decade later, through the researches 
of Meves, Regaud, Faure*-Fremiet, Lewitski, Guilliermond, and others 
that they came into prominence. Since that time they have been very 
intensively studied by both zoologists and botanists, and a special 
literature of considerable bulk has developed. 1 It now seems evident 
that the filaments ("fila") of Flemming, the/ ' bioplasts " of Altman, the 
" plastidules " of Maggi, the "archoplasmic granules " of Boveri, and the 
"mitochondria" of Benda are all one and the same thing chondriosomes 
(Duesberg 1919). 

General Nature and Occurrence. Chondriosomes occur in the cyto- 
plasm of the cell, commonly in the form of minute granules, rods, and 

1 Reviews of the subject are given by Duesberg (1911, 1919), Schmidt (1912), 
Cavers (1914). and Guilliermond (1919). S*e also Meves (1918). 



threads, but also in a great variety of irregular shapes (Fig. 43). At 
present it is customary with the majority of workers to refer to all types 
as chondriosomes or mitochondria. For | those which are definitely rod- 
and thread-shaped the terms chondriokonts and chondriomites are also 
used. It is not to be thought that the various forms constitute distinct 
clashes, for several investigators (N. H. Cowdry; M. and W. Lewis 19L5) 
have observed the chondriosomes undergoing marked changes in shape 
in living cells, granular ones becoming rod-shaped and filamentous, and 
vice versa. Schaxel (1911) and Kingery (1917) state, moreover, that in 
fixed material the shape of the chondriosomes is to a certain extent 
dependent upon the character of the microtechnical methods employed. 


FIG. 43. Chondriosomes in plant and animal cells. 

A, nerve cell from guinea pig. X 480. (After E. V. Cowdry, 1914.) B, tapetal cell 
of Nymphcea alba. (After Meves, 1904.) C, living epidermal cell of tulip petal. /), ascus 
of Pustularia vesiculosa. E, hypha of Rhizopus nigricans. F, portion of embryo sac of 
Lilium; chondriosomee clustered about nucleus. G, cell of root tip of Allium (C-F. 
After Guilliermond, 1918.) 

Although when first discovered chondriosomes were believed to be 
rather limited in distribution, they have now been reported in the cells of 
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. " They are present, 
furthermore, in the cells of all tissues. In plants it is probable that they 
are no less universally present, although] it has not yet been possible to 
demonstrate them with certainty in bacteria, Cyanophycese, and certain 
Chlorophyeese, such as the Conjugate and ConfervalesVGuilliermond 
1915). They are abundant in myxomjcetes (N. H. Cowdry 1918), 
Charales (Mirande 1919), brown and red algae, fungi, and all the higher 

A critical comparison of the chondriosomes of plants with those of 
animate has been made by N. H. Cowdry (1917), who concludes, contrary 


to the opinion of Pensa (1914), that there is every reason to regard them 
as homologous in the two kingdoms. jHe finds plant and animal chon- 
driosomes 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 the animal cell. In both cases they are most abundant in 
the active stages in the life of the cell. As the cell ages and becomes 
fully differentiated, i.e., as cytomorphosis proceeds, they diminish in 
number and may completely disappear. 1 

Physico-chemical Nature. With regard to the chemical and physical 
nature of chondriosomes, Regaud (1908), Faur^-Fremiet (1910), and 
Lowschin (1913), working respectively on mammals, protozoa, and plants, 
agree thatuiey are chemically a combination of phospholipin and albu- 
min. They closely resemble phosphatids, which are combinations of 
phosphoric and fatty acids, glycerol, and nitrogen bases. Lecithin is 
such a compound. Since chondriosomes are soluble in alcohol, ether, 
"chloroform, and dilute acetic acid, many of the fixing reagents commonly 
employed in microtechnique destroy them :| this accounts in part for the 
fact that they were not observed in many familiar tissues until a compara- 
tively recent date. VThey are well fixed by neutral formalin, potassium 
bichromate, osmium tetroxid, and chromium trioxid (chromic acid) ; and 
these, therefore, are the principal ingredients of the fixing reagents em- 
ployed in researches upon chondriosomes.^ Examples of such fluids are 
those of Altman, Benda, Benslcy, Helley, Kopsch, Regaud, and Zenker. 1 
Besides staining with hsematoxylin and several other dyes commonly 
employed with fixed material, the chondriosomes show a characteristic 
affinity for certain intra-vitam stains, such as Janus green B, Janus blue, 
Janus black I, and diethylsafranin, the reaction with the first of these 
being especially strong. After certain treatments the chondriosomes may 
closely resemble the "chromidial substance," or granules of nucleo- 
protein distributed throughout the cytoplasm in some cells.) That the 
two are not to be confused has been emphasized by Duesberg and by 
E. V. Cowdry. According to the latter author (1916) chondriosomes are 
"a concrete class of cell granulations, " and 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 staining reactions, resemble phospholipins and 
to a lesser extent, albumins. " 

Origin and Multiplication. The questions of the origin and multipli- 
of chondriosomes are much debated ones. Certain cytologists 

1 For convenient summaries of the effects of various reagents upon chondriosomes 
the student may refer to Kingsbury's (1912) paper on cytoplasmic fixation, E. \. 
Cowdry's (1914) on vital staining, and N. H. Cowdry's (1917) on plant and animal 


believe thaAthey have found good evidence for the view that chondrio- 
somes may multiply by division, and some (Guilliermond; Moreau 1914;. 
Terni 1914) have held this to be their sole mode of origin that they arise 
only from preexisting chondriosomes and are therefore permanent cell 
organs. Others are convinced that they may arise de novo in the cyto- 
plasm, and that the evidence for their division is unsatisfactoryNJOrman 
1913; Lowschin 1913; Scherrer 1914; Miss Beckwith 1914; Chambers 
1915; M. and W. Lewis 1915; Twiss 1919; and others). The investiga- 
tors of the foregoing group, together with Meves (1900), Lewitski (1910), 
and Forenbacher (1911), hold that the chondriosomes arise from the cyto- 
plasm, but certain others believe they take their origin from tbfi. nucleus. 
Tischler (1906) and Wassilief (1907), for example, state that they arise 
from surplus chromatin. Alexieff (1917) thinks that although cyto- 

, . , 

FIG. 44. Examples of regular behavior of chondriosomes in cell-division. 
A-C, spermatocyte of Gryllotalpa vulgaris, (After Vo'inov, 1916): A, chondriosomal 
material in cytoplasm about nucleus; B, heterotypic mitosis, showing chondriosomes (at 
sides) occupying the spindle with the chromosomes (at center) ; C, stages in the division 
of a chondriosome. D, Dividing cell of Geotriton fuscus, showing division of individual 
chondriosomes as cell constricts at equator. (After Terni, 1914.) 

iplasmic differentiation is due to them, they are at least in some cases 
of nuclear origin; and further that they are not fundamentally different 
from chromosomes and chromidia, a conclusion contradictory to that of 
Duesberg and E. V. Cowdry, cited above. Shaffer (1920) believes them 
to arise as the result of a chemical action of the nucleus upon products of 
assimilation in the adjacent cytoplasm. Wildman (1913) classifies the 
cytoplasmic inclusions present throughout spermatogenesis in Ascaris 
into two main types, both of nuclear origin: "karyochondria," equiva- 
lent to the mitochondria of other writers, and "plastochondria," which 
pass into the cytoplasm, form yolk within them, and fuse to form the 
food supply ("refractive body") of the spermatozoon. ^ 

TPhat the behavior of the chondriosomes at the time of cell^division 
is a matter of considerable importance has been generally recognized. In 
many cases their distribution to the two daughter cells seems to be quite 
fortuitous, whereas in some tissues more or less definite modes of distribu- 
tion have been described. According to Faur6-Fremiet (1910), Terni 
(1914), Korotneff (1909), and others, the individual chondriosomes divide 
at the time of mitosis (Fig. 44, D), a conclusion with which many others 
fail to agree (Orman 1913; Miss Beckwith 1914; etc.). In the cells of 


the grasshopper, Dissosteira Carolina, Chambers (1915) finds that the 
ch^nj^i^semal^material forms a granular ne.twork^urr.Qiujding the nucleus 
iuring the resting stages and the mitotic figure during division. During 
-he later phases of mitosis the strands and granules of this network 
*engthen into delicate filaments between the two daughter chromosome 
groups, and finally separate into two granular masses which gradually 
invest the daughter nuclei. ^ 

In the mole cricket, Gryllotalpa borealis, the distribution of the chon- 
driosomes to the daughter cells is accomplished with even greater defin- 
iteness. According to Payne (1916) they become thread-like and break 
near the middle, the halves passing to the daughter cells. Voi'nov (1916) 
states that the " mitochondria " in the spermatocyte of (?. vulgaris fuse to 
form a thread which then segments into a number (70 or more) "chondrio- 
somes." These are arranged on the spindle along with the chromo- 
somes, which they may closely resemble, and divide to form daughter 
bodies at both maturation divisions, so that they are equally distributed 
to the four resulting spermatozoa (Fig. 44, A-C). 

In certain scorpions also the chondriosomal material is distributed 
with surprising precision. In a species from Arizona (Wilson 1916) this 
material in the spermatocyte takes the form of a single ring-shaped body. 
This ring divides accurately, much like a chromosome, at both maturation 
divisions, each of the four spermatids, and hence each spermatozoon of 
the tetrad, receives a quarter of its substance. In a California species 
(Wilson) there is no ring formed, but instead about 24 hollow spherical 
bodies. At the two maturation divisions these show no evidence of 
division, but are passively separated into four approximately equal groups, 
each spermatid receiving six (occasionally five or seven) . A European 
species described by Sokolow (1913) agrees essentially with this. 

Function. Our knowledge of chondriosomes is yet too incomplete to 
warrant any categorical statements regarding their functions, but a 
number of opinions have been expressed, some of them based upon ob- 
servational evidence and others upon conjecture. Certain of the more 
prominent opinions may here be reviewed. 

It was in 1897 that Benda suggested that chondriosomes might be 
distinct cell organs with a special function. In a series of papers which 
began to appear ten years later Meves (1907 etc.) put forth and empha- 
Isized 'the theory that they playlnfimportant role in heredity that they 
carry the hereditary characters of the cytoplasm. Evidence supporting 
this view was seen by Meves and Benda in certain experiments of God- 
lewBki which seemed to show that the appearance of certain hereditary 
characters is dependent upon something present in the cytoplasm rather 
than in the nucleus./ (See Chapter XIV.) This theory has had the 
support of a number of investigators, among whom are the botanists 
Cavers (1914) and Mottier (1916). Voinov (1916) also believes that the 



regular distribution of the chondriosomal substance in Gryllotalpa 
strongly favors the view that this substance is of some significance in 
heredity. It is probable, however, that the majority of cytologists regard 
the evidence brought forward in support of the view as very inadequate. 
Wildman (1913) points out that the chondriosomes may be largely lost 
during spermatogenesis, and others have recalled cases in which the 
nucleus is the only portion of the male gamete which can be seen to enter 
the egg at fertilization. Meves (1911, 1915) and Benda, on the other 
hand, show that chondriosomes also enter, at least in the forms studied 
by them (Fig. 45). In the animal spermatid the chondriosomes appear 
most commonly to contribute to the formation of the Nebenkern of the 

spermatozoon? (La Vallette St. George 1886; 
Popoff 1907; Chambers 1915; Shaffer 1920; and 
others), in some cases later elongating into a 
sheath around the axial filament of~the tail 
(Shaffer 'on Cicada). Duesberg (19lSJ^states 
that although the fate of the chondriosomes of 
the spermatid varies in different animals, they 
are nevertheless always present in the sperma- 
tozoon, arid that it has not been clearly shown 
in any case that they do not enter the egg at 
fertilization. In many eggs which they do enter, 
however, they behave with great irregularity 
during the subsequent cleavage stages (Van der 
Stricht, etc.). (It is not at all improbable that 
they are in someVay concerned in the reactions 
through which hereditary characters are de- 
veloped in the individual, but the general 
opinion is that their apparent variability and 
indefiniteness in behavior in so many cases are 
against the view that they take any part in the transmission of factors 
upon whose presence the development of the characters depends 
(Gatenby 1918, 1919). The equal distribution of chondriosomes at 
the time of cell-division is thought, to be without any significance in 
this connection by Harper (1919). 

It is obvious that much work remains to be done before the possible 
relation of chondriosomes to heredity and development can be made 
clear. For the present it is safest to assume, as will be emphasized in 
later chapters, that hereditary transmission is the function of the nucleus, 
chiefly if not entirely, since the chromosomes afford a mechanism of 
precisely the kind required to account for the observed distribution of 
hereditary characters^ 4 

Meves (1907a6, 1909) and Duesberg (1909) have also called atteution 
to the close relation of chondriosomes to miimrt^i fibers in the developing 

FIG. 45. Fertilization in 
Filaria papillosa, showing 
chondriosomes of sperma- 
tozoon (at top) distributing 
themselves in the cytoplasm 
of the egg. (After Meves, 



chick embryo. They believe that the chondriosome elongates and 
directly becomes the young fibflJL.Gaudissart (1913), on the contrary, 
shows that the fib^tdoes not arise exclusively from the chondriosome, but 
that the primary basis is furnished by the plasmatic reticulum with 
which the chondriosomes cooperate in building up the fibttl 
the chondriosomes thus have a part in the genesis of the 
the latter is not a " modified filamentous chondriosome/ ' as Duesberg 
believed. \ 

Hoven (191 Oa) and Meves have similarly attempted to show that 
chondriosomes are concerned in the differentiation of neurofibrils and the 
collagenous fibers of cartilage. Regaud (1911), Guilliermond (1914), 

' * 

FIG. 46. 

A, formation of fat in cell of rabbit by granular and rod-shaped chondriosomes. (From 
Guilliermond, after Dubreuil, 1913.) B, formation of needle-shaped crystals of carotin in 
chromoplasts derived from chondriosomes in epidermal cell of Iris petal. (After Guillier- 
mond, 1918.) (7, chondriosomes and chloroplasts in young cell of Pinus banksiana. X 750. 
(After Mottier, 1918.) D, transformation of plastid primordia into leucoplasts in root 
cell of Pisum; some of the leucoplasts contain starch. (After Mottier.) 

Hoven (1910b, 1911), and Lewitski (1914) have thought that the cJjQn- 
driosomes may in some cases perform a secretory f u fi clT6TT7~affd Uubreuil 
(1913) has associated them with the production ofjat (Fig. 46, A). IE 
the oocyte of Cicada Shaffer (1920) finds them transforming into yolk 
spherules. The activity of bodies called " plastochondria " by Wildman 
(1913) in the elaboration of the food supply in the spermatozoon ol 
Ascaris has already been mentioned. 

Relation of Chondriosomes to Plastids. One of the most conspicuous 
views regarding the significance of chondriosomes is that which holds 
feome of them to be the primordia of plastids. After studying the cells ol 
Pisum and Asparagus Lewitski (1910) concluded that the chondriosomes 
are essential constituents of the cytoplasm, and that they develop into 
chloroplasts and leucoplasts in the cells of the stem and root respectively. 


Evidence in support of this conception was contributed by Forenbacher 
(1911), Pensa (1914), Cavers (1914), and others. Guilliermond (1911- 
1920) in particular was led by the results of his extensive researches on 
the subject to the view that the chondriosomes, arising only from preexist- 
ing ones ,by division, persist through the egg and embryonic cells 
and lafter become amyloplasts, chloroplasts, and chromoplasts. In 
this he saw strong evidence for the individuality of the plastid. In 
1915 he advanced the opinion that in fungi the chondriosomes function 
like the amyloplasts of higher plants, forming reserve products as the 
latter form starch. In this development of chondriosomes into plastids 
Guilliermond (1913-1915) and Moreau (1914) were able to show that the 
chondriosomes produce within them certain phenolic compounds which 
either appear at once as anthocyanin pigments, or as colorless products 
which may acquire color later through chemical alteration (Fig. 46, B). 

Among the most recent researches in this field are those of Mottier 
(1916, 1918) on the cells of Zea, Pisum, Elodea, Pinus, Adiantum, Antho- 
ceros, Pallavicinia, Marchantia, and several algse. He finds that leuco- 
plasts and chloroplasts are derived from small rod-shaped primordia 
(Fig. 46, C, Z>) which he regards as permanent cell organs of the same 
rank as the nucleus. Both primordia and mature chloroplasts multiply 
by fission. In the cells of Marchantia, Anthoceros, and the seed plants 
he finds also a second series of bodies, which he calls chondriosomes: 
these like the plastid primordia, are permanent cell organs multiplying 
by division, but they do not become chloroplasts or leucoplasts. Further- 
more, both chondriosomes and primordia are thought by Mottier to 
be concerned in the transmission of certain hereditary characters. 

It is also reported by Emberger (1920ab) that in the roots and spor- 
angia .of ferns two kinds of granular elements may be recognized at all 
times, one of them representing the initial stage of plastid development. 
Contrary to Mottier's opinion, however, he regards both kinds as true 
mitochondria. Guilliermond (1920) likewise distinguishes two such 
types in 7m germanica. 

P. A. and P. Dangeard (1919, 1920), as a result of their researches 
on the cells of barley, Selaginella, Larix, Taxus, and Ginkgo, distinguish 
three classes of cytoplasmic structures differing in reaction to reagents 
and in function. In their initial stages all have the granular form. The 
plastidomes first appear as minute "mitoplasts," which gradually enlarge 
and develop into plastids. The spheromes are at first recognizable as 
"microsomes," some of which may be seen to give rise to fat and oil 
globules while others appear to undergo no change. The vacuomes 
begin their history as "metachromes; " these elongate and form a peculiar 
network which later develops into a system of vacuoles. Guilliermond 
(1920) denies the metachromatic nature of this third class of bodies, and 
holds them to be quite distinct from mitochondria. 


The existence of such a genetic relationship between chondriosomes 
and plastids as that described above has been denied by many writers, 
among whom may be mentioned Lundegardh (1910), Meyer (1911), 
Rudolph (1912), Lowschin (1913, 1914), Scherrer (1914), Miss Beckwith 
(1914), Derschau (1914), von Winiwarter (1914), Sapehin (1915), 
Chambers (1915), M. and W. Lewis (1915), and Harper (1919). These 
workers for the most part hold that chondriosomes are not distinct cell 
organs at all* but regard them rather as more or less transient visible 
products of protoplasmic activity. Derschau asserts that they arise 
neither de novo nor by fission, but that they are merely small masses 
of plastin and nuclein concerned in nutrition, arising from basichromatin 
at the surface of the nucleus. Miss Beckwith speaks of them as differ- 
entiation products of the cytoplasm. Lowschin, who made some ex- 
periments in the production of artificial chondriosomes, believes them 
to be due to the emulsified state of the protoplasm and in some instances 
to the action of fixing agents upon it. To Chambers they appear in 
living cells not as persistent structures but as temporary physical states 
of the colloidal substances composing protoplasm. M. and W. Lewis 
have studied them in tissue cultures and observe that they are continually 
being formed and used up, and that they show no sharply distinct types. 
Faur6-Fremiet (1910a) distinguishes " mitochondria/ ; which have an 
individuality of their own and are permanent cell organs, from "lipo- 
somes," which are temporary accumulations of reserve substance. 

The almost universal occurrence of chondriosomes in the cells of 
Irving organisms, and their frequent alterations in number and appear- 
ance, suggest a connection with some fundamental process going on 
almost constantly and 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" (Kingsbury), 
has been regarded as highly probable by Kingsbury (1912), Mayer, 
Rathery, and Schaeffer (1914), N. H. Cowdry (1917, 1918), and others. 
Evidence favoring this interpretation is seen in the fact that the chondrio- 
somes occur so widely in the cytoplasm, which acts as a reducing sub- 
stance; and also in the close similarity between their chemical composition 
and that of phosphatids, which appear to be capable of auto-oxidation. 

Conclusion. From the foregoing review it should be more than plain 
that the state of our knowledge of chondriosomes is such that almost no 
definite final statements can be made regarding their origin and function. 
The evidence at hand apparently indicates that the class of cell inclusions 
known as chondriosomes comprises a variety of bodies which play differ- 
nt r61es in the life of the cell. It is scarcely open to doubt that some of 
them are temporary accumulations of substances involved in metabolism, 
appearing and disappearing in the cell in a manner somewhat analogous 
to that of starch. The most plausible hypothesis concerning the specific 


physiological role of such changeable types of chondriosomes is that they 
have to do with the processes of oxidation and reduction with cellular 
respiration. It is also becoming increasingly apparent that other chon- 
driosomes represent the juvenile stages in the development of plastids 
of various kinds, and that they are in some way concerned in the forma- 
tion of chlorophyll and other pigments. If this is true they are clearly 
of the highest importance. 

Whether or not any of the chondriosomes are to be considered as 
permanent cell organs is a question to which, in view of the conflicting 
testimony of competent observers, no final answer can at present be 
given. To determine whether these minute bodies arise de nova or 
always multiply by division is a matter of extreme practical difficulty. 
Until this question is settled it is obviously impossible to come to a deci- 
sion regarding the individuality of those plastids which appear to take 
their origin from chondriosomes, or to know what may be the possible 
relation of chondriosomes to inheritance. With respect to the latter 
point, the chondriosomes, like all other structures concerned in meta- 
bolism, may be indirectly associated with the development of hereditary 
characters, but the view that they transmit or represent differential 
factors for such characters is as yet unsupported by adequate evidence. 

From the fact that the chondriosomes may not preserve their indi- 
viduality at all times, however, it does not follow that they must be denied 
the rank of cell organs. Their great variability^mdifferent behavior at 
the time of cell-division in so many cases, and their unknown mode of 
origin are, as Kingsbury (1912) states, against the view that they are cell 
organs; and it is doubtless true that many chondHo^pmes should for such 
reasons be denied such rank. On the other hand, those chondriosomes 
which seem clearly to perform important and specific functions in the life 
of the cell should, like centrosomes appearing de novo at each cell-division, 
be looked upon as cell organs, though not as permanent ones with an 
uninterrupted continuity. 

In spite of the fact that the study of chondriosomes has so far raised 
more problems than it has solved, it has already proved of much value, 
for it has turned to the cytoplasm some of the attention so long directed 
almost exclusively to the nucleus, and it appears that many problems of 
much importance to cytology pertain to the cytoplasm. 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. Much has already been learned as the result of this 
study, but the solution of the principal problems involving chondriosomes 
must await the results of further research. 


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LOWSCHIN, A. M. 1913. "Myelinformen" und Chondriosomen. Her. Deu. Bot. 

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1914. Vergleichende experimental-cytologisehe Untersuchungen fiber Mifco- 
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1914. The pyrenoid of Anthoceros. Am. Jour. Bot. 1: 79-95. pi. 8. 
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19076. Die Chondriokonten in ihrem Verhiiltnis zur Filarmasse Flemrnings. 
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In the foregoing chapters we have described successively the various 
organs of the cell. Our account of the resting cell will now be com- 
pleted by passing in brief review some of its more conspicuous non- 
protoplasmic inclusions. We shall also call attention to another 
characteristic but imperfectly understood attribute of the protoplast, 
namely, its polarity. 

Metaplasm. In addition to their definite cell organs nucleus, 
cytoplasm, centrosomes, plastids, and possibly chondriosomes cells 
which have undergone any amount of differentiation usually contain a 
variety of other materials representing products of metabolism. Many 
of these substances are held in solution in the cell sap, itself a differentia- 
tion product, while others are present in insoluble form in the cytoplasm, 
often in special vacuoles. All such non-protoplasmic inclusions, partic- 
ularly those existing in some visible form, are referred to as metaplasm, 
a term introduced by Hanstein. Although it has been held by some 
(Kassowitz 1899) that metaplasm is always inactive and to be sharply 
set apart from active protoplasm, it is more probable, as Child (1915) 
contends, that no absolute distinction can be made between the two. 
Most of the products of differentiation, however, are clearly non-proto- 
plasmic and relatively inactive. 

In cells of many types, even in the comparatively undifferentiated 
cells of the root meristem, there often occur accumulations of chemically 
complex substances in the form of small globules or irregular masses in 
the cytoplasm. In many cases these more or less transient bodies, which 
often stain intensely with the nuclear dyes and are therefore referred to 
as " chromatic bodies/' show reactions indicating a composition closely 
approaching that of the extra-nuclear granules of nucleo-protein (chro- 
iftkHa; which R. Hertwig and Goldschmidt interpret as granules of escaped 
chromatin concerned in cell differentiation. Others resemble the fatty 
chondriosomes in form and composition. It is therefore a matter of some 
difficulty to distinguish between these various substances, which, as a 
matter of fact, probably do not represent sharply distinct classes. 

The most conspicuous non-protoplasmic inclusions represent food 
materials in transitory form or in the storage condition; they are conse- 
q\iently abundant in cells carrying a supply of reserve foods, such as 
spores and eggs, and in storage organs, such as many roots and the endo- 




sperm and cotyledons of seeds. In the animal egg the storage material 
commonly exists in the form of " yolk globules/' or "deutoplasm spheres/' 
which consist for the most part of relatively complex protein compounds. 
Fat or oil globules are usually present with them. In plants the most 
characteristic storage product is starch, the origin and characters of which 
were described in Chapter VI along with the plastids by which they are 
formed. In some organisms, including the fungi, glycogen appears to 
carry on the function performed by starch and sugar in the higher plants, 
jj^ats and, oils, usually in the form of droplets but sometimes of soft grains 
oy even crystals (nutmeg), comprise another important class of storage 
substances : these are especially prevalent in seeds and spores, where light 
weight is of advantage. In many cases oil may be produced anywhere in 
the cell, but in certain forms it has been found that special elaioplasts, and 

FIG. 47. Crystalline and other inclusions in the cells of various plants. 
A, cystolith in subcpidormal cell of Ficus leaf. B, crystal ceils in Arctostaphyhs. C, 
druse in cell of Rheum palmatum. D-K, aleurone grains: D, E, from Myristica; F, from 
Datura stramonium; G, from Ricinus communis; //, from Amygdalus communis; /, from 
Bertholletia excelsa; J, from Faeniculum; K, from Elceis guiniensis. L, raphides in leaf 
of Agave. M, inulin crystals in preserved cells of artichoke. (B-K after Tschirch.) 

possibly also chondriosomes, are concerned in this process. The peculiar 
oil bodies found in the cells of certain liverworts appear to represent oil 
vacuoles: these also have been discussed, together with elaioplasts, in 
Chapter VI. Large masses of intranuclear metaplasm are found charac- 
teristically in the eggs of gymnosperms. 

Aleurone grains occur in small vacuoles in the cells of many seeds, 
particularly in such oily ones as those of Ricinus, Juglans, and Bertholl- 
etia. In maize and wheat grains they are limited to a single layer of cells, 
the " aleurone layer.' 7 The aleurone grain varies much in structure and 
form, several types being described by Pfeffer in 1872. The grain con- 
sists primarily of an amorphous protein substance, often with an outer, 
somewhat more opaque shell. Some examples show no greater differen- 
tiation than this, but many are much more elaborate (Fig. 47, D-K). 
Those of Ricinus contain within them a single angular crystal of protein 
(albumen), often referred to as the " crystalloid," and a globule of a double 
phosphate of calcium mid magnesium with certain organic substances 


called the "globoid" (Fig. 47, G). The crystalline inclusions sometimes 
grow to be very large. It has been thought by certain workers thai 
aleurone grains are self-perpetuating bodies with an individuality com- 
parable to that of nuclei and certain plastids. That this view is correct 
has been rendered very improbable by the researches of East and Hayes 
(1911, 1915) and Emerson (1914, 1917) on the inheritance of aleurone 
characters in maize, and also by the work of Thompson (1912), who suc- 
ceeded in producing artificial aleurone grains in all essential respects 
similar to those elaborated by the plant. 

Crystals occur in great variety in the differentiated cells of plants. 
They may lie in the cytoplasm, in vacuoles, attached to or imbedded in 
the cell wall, and even in special cells. They are usually salts of calcium, 
calcium oxalate being especially prevalent. The bundles of needle- 
shaped crystals known as "raphides" (Fig. 47, L) found in the leaves of a 
number of plants are composed of the latter salt, as are also the spherical 
aggregations called "druses," or "sphserraphides" (Fig. 47, C). The 
curious clustered " cystoliths " of the Ficus leaf (Fig. 47, A) are made up of 
cellulose and calcium carbonate. Crystals of silica are very abundant in 
the thickened walls of wood cells and in many other tissues, such as the 
outer cells of the Equisetum stem. Crystals of albumen, aside from those 
found in aleurone grains, are frequently present in the cytoplasm of cells 
poor in starch, as in the outer portion of the potato tuber. The leucoplast 
of Phajus often contains a rod-shaped albumen crystal. Protein crystals 
of various shapes are occasionally observed within the nucleus (Stock 
1892; Zimmennaim 1893). 

Cellulose is a common storage material, existing as a rule in the form 
of laminae deposited upon the original cell wall. 

As already pointed out, the sap of vacuolated cells may contain a 
number of differentiation products in solution. The cell sap is usually 
slightly acid in reaction, owing to the presence or organic acids (malic, 
formic, acetic, oxalic) and their salts. Inogranic salts are probably always 
present. Amides, such as glutamin and asparagin, glucosides, sugars, 
proteins, tannin, and many other substances are of frequent occurrence 
in the cell sap of various plants. The carbohydrate inulin may be pre- 
cipitated out of the sap by alcohol: this accounts for the presence of 
nodules of radiating inulin crystals frequently encountered in preserved 
material (Fig. 47, M). Rubber is present in the form of a suspension of 
minute droplets in the cell sap of Ficus elastica and several other plants. 
Gutta-percha occurs in a similar state in Isonandra gutta. The cell sap 
in such cases has a characteristic milky appearance. The cell sap is 
often colored by red, blue, and yellow anthocyanin pigments (Wheldale 
1916; Palladin 1918; Beauverie 1919), some of which change color when 
the reaction of the sap is altered from acid to basic and vice versa. The 
striking colors of flowers are due to "(1) the varying color of the sap, (2) 


the distribution of the cells containing it, and (3) combinations of colored 
sap with chloro- and chromoplasts." Autumnal coloring is due to the 
formation of pigments as disorganization products : when cytoplasm and 
chlorophyll are the main disorganizing substances a yellowish color results, 
whereas if sugars are present in considerable amounts in the cell sap the 
brighter pigments are formed. 

Extruded Chromatin. 1 The actual extrusion of chromatin from the 
nucleus into the cytoplasm has been reported in a number of instances: 
in the microsporocytes of various angiosperms by Digby (1909, 1911, 
1914), Derschau (1908, 1914), West and Lechmere (1915), and others; 
in ferns by Farmer and Digby (1910); and in the Ascomycete Helvella 
crispa by Carruthers (1911). The extruded chromatin commonly takes 
the form of deeply staining globules or irregular masses in the cytoplasm; 
often a clear area suggesting a nuclear vesicle is present about them. In 
some cases, such as Gallonia candicans (Digby 1909) and Lilium candidum 
(West and Lechmere 1915), the chromatin may pass through the wall 
into an adjacent cell, where it forms a rounded mass connected by a 
chromatic strand with the nucleus from which it originated. 

The significance of this phenomenon is by no means apparent. It is 
not at all unlikely that nutritive materials passing from nucleus to cyto- 
plasm during the normal metabolism of the cell occur at times as visible 
globules at the nuclear surface. The extrusion of chromatin into neigh- 
boring cells, on the other hand, in many cases has every appearance of 
a phenomenon associated with degeneration or some other abnormal 
physiological condition. West and Lechmjere, however, view the process 
as one which occurs normally at certain stages, and which will probably 
be found to be more general in plants. Sakamura's (1920) extensive 
researches on chloralized cells have led him to regard the extrusion of 
large masses of chromatin as an abnormal phenomenon which occurs as a 
result of a disturbance of the metabolism of the cell. Its more frequent 
occurrence in sporocytes than in other cells is attributed to the unusual 
sensitiveness of the former to disturbing influences. 

The Senescence of the Cell. The accumulation of products of 
metabolism (''differentiation products ") has a direct bearing on the 
problem of protoplasmic senility. As its life progresses the cell gradually 
"ages," and if nothing occurs to prevent it the process eventually term- 
inates in death. What shall be taken as an index of the degree of senes- 
cence has been the subject of much discussion. We have already called 
attention to the attempts which have been made to correlate senescence 
with a progressive change in the nucleoplasmic relation, concluding 
that no constant correlation of the kind has been shown to exist (p. 63). 

Child (1915) has brought forward much evidence to show that the 

1 Extruded chromatin is not metaplasm, but it has been found convenient to 
treat it at this point along with other inclusions of the cytoplasm. 


relative rate of metabolism is the main criterion of the cell's physiological 
age, "young" cells having a high rate and "old" cells a relatively low 
rate, and a gradual decline in this rate occurring throughout the life of 
the cell. In embryonic (physiologically young) cells the cytoplasm ap- 
pears to be comparatively homogeneous and undifferentiated. Older 
cells, on the contrary, are ordinarily marked by the presence of products 
of differentiation in the cytoplasm. The true measure of age is there- 
fore not time, but physiological differentiation. 

In many cells a rejuvenating process may occur, whereby a high meta- 
bolic rate is restored and the products of differentiation lost: this is 
regarded as a "return to the embryonic state" a real physiological 
rejuvenescence. "Senescence is primarily a decrease in rate of the 
dynamic processes conditioned by the accumulation, differentiation, and 
other associated changes of the material of the colloid substratum. 
Rejuvenescence is an increase in rate of dynamic processes conditioned 
by changes in the colloid substratum in reduction and dedifferentiation " 
(Child, p. 58). Such a rejuvenescence occurs in connection with 
regeneration, vegetative and other asexual reproduction, and sexual 
reproduction. In each case the cell which begins the new life cycle the 
meristematic regenerating cell, the zoospore, or the zygote has a high 
metabolic rate and is comparatively free from the products of differentia- 

In the lower organisms cell differentiation in this sense is not so great 
but that almost any cell may retain the power to " dedifferentiate " and 
begin the development of a new individual vegetatively. In these forms 
asexual reproduction may occur repeatedly and keep the organism as a 
whole (in protozoa and protophyta) or the protoplasm of the race (in 
lower metazoa and metaphyta) physiologically young. Only when the 
metabolic rate falls very low does sexual reproduction, the most effective 
of all the rejuvenating agencies, ensue. 

In the higher plants the retention of the power of dedifferentiation 
is strikingly shown in the well known cases of Begonia and Bryophyllum, 
which can regenerate complete new individuals from a few leaf cells. 
In the higher animals cell differentiation is usually so great that the 
somatic cells can no longer dedifferentiate and reproduce the organism 
asexually. Here rejuvenation occurs only after the union of two gametes, 
which are themselves, unlike the zoospores of algae, physiologically old. 
Although local rejuvenescence may occur, as in secretory cells which are 
" younger" after secretion, and also in wound tissue, the differentiation 
of the body cells is carried so far that their metabolic rate falls low enough 
to make a recovery or rejuvenescence no longer possible. Thus it is 
only the functioning reproductive cells that endure: the ultimate cessation 
of all life processes in the body cells is the price which is inevitably paid 
by the complex multicellular organism for the advantages conferred by 
its high degree of differentiation. 


Of the highest importance in this connection are the results of at- 
tempts to maintain the cells and tissues of higher animals in the living 
condition in artificial culture media outside the body. It has been shown 
by the remarkable experiments of Carrel, Leo Loeb, Burrows, H. V. 
Wilson and others that cells may be isolated from any of the highly 
differentiated essential tissues of the body and kept actively growing and 
multiplying in vitro for a length of time frequently far exceeding that to 
which they would have lived in the body. They do not appear to grow 
old: indeed it is hot improbable that in such a constantly favorable 
environment somatic cells are as "potentially immortal" as the germ 
cells (see p. 403). In the words of Pearl (1921), "It is the differentiation 
and specialization of function of the mutually dependent aggregate of 
cells and tissues which constitutes the metazoan body which brings about 
death, and not any inherent or inevitable mortal process in the indivi- 
dual cells themselves." 


Polarity is a feature which is exhibited in some form by the cells of 
all higher organisms, and in at least many of the simpler ones, as shown by 
Tobler (1902, 1904) for certain algae; indeed it is probable that it is 
possessed in some form and degree by all cells. Harper (1919) calls 
attention to the fact that "in the presence of polarity and the various 
symmetry relations we have a fundamental distinction between cell 
organization and that of polyphase colloidal systems as they are com- 
monly produced in vitro.'' 

This polarity has two aspects, the morphological and the physiological. 
In the first place, the various constituents of the cell may be arranged 
symmetrically about one or more ideal axes, so that the cell has more 
or less distinctly differentiated anterior and posterior ends. This 
structural aspect of polarity has been the one chiefly emphasized by 
certain workers: van Beneden (1883), for instance, looked upon polarity 
as "a primary morphological attribute of the cell," the axis passing 
through the nucleus and the centrosome. Later writers, among them 
Heidenhain (1894, 1895), made this conception of morphological polarity 
the basis for interpretations of many of the phenomena of cell behavior. 
(See Wilson 1900, pp. 55-56.) However, as Harper (1919) points out, 
polarity "is apparently independent of the uni- or multinucleated condi- 
tion of the cell, which shows that it is in some cases at least a more 
generalized characteristic of the cell as a whole rather than a mere ex- 
pression of the space relations of the nucleus and cytoplasm . . ." Other 
investigators (Hatschek 1888; Rabl 1889, 1892) early laid emphasis upon 
the physiological expression of polarity. The cell shows a polar differ- 
entiation in physiological labor: the processes in one portion of the cell 
differ from those in another, this difference in the case of tissue cells 


being due to different environments in the tissue. For these workers 
this physiological differentiation is the essential element of polarity; 
any morphological polarity is due secondarily to it- 
Metabolic Gradient. The most suggestive physiological conception 
recently developed in this connection is that of Child (1911-1916). 
Child has shown in the case of Planaria and other lower animals, as well 
as in certain algae, that along each of the axes of symmetry there exists a 
"metabolic gradient/' or "axial gradient:" the rate of the physiological 
processes is highest at one end of the axis and diminishes progressively 
toward the other end. The anterior end of a planarian, for example, 
has a higher metabolic rate than the posterior portions. Furthermore, 
the portions of higher rate dominate and control the development of 
those portions having a lower rate, with the result that the young indivi- 
dual soon develops and 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. That polarity is here primarily a 
physiological matter is indicated by the fact that experimental altera- 
tions in the metabolic rate in different parts is followed by abnormalities 
in structural development. 

As to the means by which the dominance of certain regions over others 
is exercised, correlating the activities of the various parts of the or- 
ganism, there are two principal theories in the field. According to one 
theory chemical substances (hormones) are produced at certain places 
and transmitted through the body. Although the circulation of such 
hormones clearly has much to do with correlation in higher complex 
organisms, Child adduces good evidence in support of the second theory, 
namely, 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" 
(p. 224). 

It cannot at present be said to what extent this conception of polarity 
is applicable to the single cell. The work of Child shows in a very 
definite manner the coincidence of the morphological and physiological 
axes of polarity, which indicates that the two are but different aspects of 
one and the same polar differentiation. A similar coincidence exists very 
generally in the case of the single cell. In the cell, as in the organism as a 
whole, functional and structural differentiation are inseparably connected. 
In the present state of our knowledge the attempt to determine the real 
essence of polarity raises questions which cannot yet be answered. Does 
physiological polarity depend upon a polarized structure which is a 
fundamental attribute of the cell's ultimate organization? Or does a 
polarized morphological arrangement follow and depend upon a physio- 
logical division of labor arising as a difference in intensity or rate in proc- 


esses originally common to all parts of the cell? If so, to what internal 
or external factors is the establishment of this difference due in cells having 
no initial polarity? Analogies with electrical polarity have been resorted 
to in this connection, concerning which Harper (1919) says: "To pro- 
vide an adequate basis for understanding the observed facts of polarity, 
however, it seems to me that the conception of compound aggregate 
polyphase systems is more suggestive than these attempted analogies . . . 
In the spatial arrangement and interactions of these systems polar dif- 
ferences of the most diversified types are bound to arise in the mass as a 
whole and express themselves in the form and relative rigidity and surface 
tension of different parts, as well as in the interrelations between the cells 
of a group in contact." 

The polarity of the multicellular organism as a whole is closely bound 
up with the polarities of its constituent cells. Harper has clearly shown 
(1918) that in Pediastrum the position of the swarm -spores in the colony 
which they unite to form is directly dependent upon their polarity. 
This does not mean, however, that the polarity of the multicellular organ- 
ism is nothing more than the sum of the polarities of its constituent 
cells, unless we return to Schwann's simple conception of the organism as 
merely an aggregate of independent cells. (See p, 12.) The higher 
individuality, the colony, has its own polarity, which may be related to, 
but is not the same as, that of its individual cells. In the ordinary multi- 
cellular organism the polarity is an outgrowth of the polarity of the 
fertilized egg cell rather than of the polarities of the many adult tissue 

In polarity, then, we encounter another problem which must be 
brought nearer a solution before we can have any adequate understanding 
of the relation of the cell to the multicellular organism as a whole, and of 
the perplexing matter of organic individuality. 

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1915. Senescence and Rejuvenescence. Chicago. 

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DIGBY, L. 1909. Observations on "chromatin bodies" and their relation to the 

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DUESBERG, J. 19.11. Plastosornen, "Apparato reticolaro interne," und Chromi- 
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39:527-580. pi. 10. 


TSCHIKCH, A. 1889. Angewandte Pflanzenanatomie. Wien u. 

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WHKLDALE, M. 1916. The anthocyanin pigments of plants. ^Cambridge. 

WILSON, E. B. 1900. The Cell in Development and Inheritance. 

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Physiol. d. Pflanzenzelle 1: 54-79. pis. 2. 
18936. Ueber Proteinkrystalloide. Ibid. 2: 112-158. 

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13. Die Aleurone- oder Proteinkorner, Myrosin- und Emulsiorikorner. 14. 
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Since the time when the cell was pointed out as the unit of structure 
and function it has been recognized that the mode of origin of new cells 
is a matter of fundamental importance. We have seen in our historical 
sketch that cells were believed by the founders of the Cell Theory to 
arise de novo from a mother liquor, or "cytoblastema," a misconception 
removed by later investigations in which it was shown beyond question 
that cells arise only 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 "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 Butschli, 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 trans- 
formation of the nucleus to which Schleicher (1878) afterward gave the 
name karyokinesis. It soon appeared, however, that this mode of divi- 
sion was not of universal occurrence; and that cell-division is of two widely 
different types, which Van Beneden (1876) distinguished as fragmenta- 
tion, 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 (1882) 
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 
6r 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" (Wilson 1900, 
pp. 64-65). l 

1 The following additional historical data arc of interest. The chromosomes, 
though they appeared in the figures of Schneider (1873), were first adequately drawn 
by Strasburger in 1875. Longitudinal splitting was described by Flemming in 1882. 
The terms prophase, wctaphase, and antiphase were introduced by Strasburger in 




In view of the fact that the phenomena of growth, differentiation, 
reproduction, and inheritance are now known to be intimately bound up 
with the process of cell-division, it is obvious that a detailed knowledge 
of this process is an absolute prerequisite to a solution of many of the 
problems which confront us. In the present chapter the essential fea- 
tures of vegetative or somatic nuclear division will be described. After a 
preliminary sketch of the process of mitosis we shall take up in some 
detail the behavior of the chromosomes and the question of their individ- 
uality. In the following chapter attention will be devoted to other 
features of cell-division: the achromatic figure, the mechanism of mitosis, 
cytokinesis (the division of the extra-nuclear portion of the cell), and the 
formation of the cell wall. 


FIG. 48. Diagram of a typical case of somatic mitosis in plants. 

Preliminary Sketch of Mitosis. The main steps in a typical case of 
somatic mitosis in plants may be very briefly outlined as follows (Fig. 

The chromatic material of the "resting" nucleus, as described in 
Chapter IV, exists in the form of a more or less irregular reticulum. As 
the process of mitosis begins this reticulum resolves itself into a definite 
number of slender threads which represent chromosomes. These in 

1884, and Heidenhain in 1894 first used the term telekinesis (telophase). LundegSrdh 
(19126) added interphase. The chromosome was named by Waldeyer in 1888. 
Hermann in 1891 distinguished connecting fibers (central spindle) and mantle fibers. 
That the halves of each split chromosome go to opposite poles was shown by van 
Beneden for animals and by Heuser for plants in 1884. The achromatic spindle was 
first figured by Kowalevsky (1871) and Fol (1873), and first carefully described by 
Butschli (1875a&). 


many nuclei are distinct from each other from the first, whereas in other 
cases they may be arranged end-to-end in a more or less continuous 
thread, or spireme, which later segments transversely into independent 
chromosomes. The slender threads (chromosomes) now split longitu- 
dinally throughout their entire length. A progressive shortening and 
thickening of the split threads ensues, so that the nucleus is eventually 
seen to have a certain number of chromosomes which have become 
double through, a longitudinal cleavage. 

While the above changes are occurring, fine fibrils are differentiated 
in the cytoplasm near the nucleus and become arranged in two opposed 
groups. The nuclear membrane now disappears and the fibers extend 
into the nuclear region, where some of them (the " mantle fibers ") 
attach themselves to the double chromosomes, while others (the "con- 
necting fibers") pass through from one pole to the other. The double 
chromosomes quickly become arranged in a single plane at the equator 
of the cell, the fibers meanwhile forming the achromatic figure, or spindle. 
This stage is known as the metaphase; all the steps leading up to it, be- 
ginning with the initial changes in the resting reticulum, constitute the 

The daughter chromosomes (the halves of the longitudinally split 
chromosomes) now move apart toward the poles of the achromatic 
figure, where they soon form two closely packed groups with the central 
spindle of connecting fibers extending between them. The period during 
which the daughter chromosomes are thus moving apart is known as the 
anaphase. The two groups of daughter chromosomes now reorganize 
the daughter nuclei, in each of which the chromosomes again form a 
reticulum like that of the original mother nucleus. This reorganization 
period is called the telophase. During the telophase there is formed 
upon the connecting fibers (central spindle) a separating wall, which 
completes the division. of the cell. The nucleolus as a rule plays no con- 
spicuous part in mitosis: it usually disappears during the late stages of 
the prophase, new nucleoli being formed in the daughter nuclei in the 
telophase. In rapidly dividing cells the period between two successive 
mitoses is called the interphase. 

Mitosis in animals (Fig. 49) is closely similar to that in plants as 
regards the behavior of the chromosomes. It normally differs in two 
conspicuous features, namely, the presence of centrosomes and the 
mode of cytokinesis following the division of the nucleus. 

During the prophases the centrosome with its aster, if not already 
double, Divides. The two daughter centrosomes, each with its own 
aster, move apart, and a small bundle of fibers extends between them,; 
all these structures together form the amphiaster. The rays on the side 
toward the nucleus extend into the latter when the membrane dissolves 

and become attached to the chromosomes, often before the two centro- 



somes have reached polar positions. The centrosomes, surrounded by 
asters, remain at the poles of the achromatic figure during metaphase, 
anaphase, and telophass, and after mitosis has been completed they may 
disappear or remain through the resting stage to function in the next 
mitosis. (See p. 78.) 

The division of the cell following nuclear division is commonly 
brought about in animals by the formation of a cleavage furrow, which 
grows inward from the periphery as described in the following chapter, 
rather than by the formation of a wall on the spindle fibers as in 

Fiu. 49. Diagram of a typical rase of somatic mitosis in animals. 

Although the two above points serve in general to distinguish mitosis 
in animals from that in plants, the distinction is not a sharp one: cen- 
trosomes are regularly present in the cells of many lower plants, while 
cytokinesis by furrowing also occurs in certain cases, as will later be 
shown. The essential point to be borne in mind is that the significant 
feature of mitosis the division of the chromatin and its distribution to 
the daughter nuclei is fundamentally the same in both plants and 

The relative duration of the various phases of mitosis has been studied 
in a few cases. As an example may be taken the observations of M. and 
W. Lewis (1917) on the mesenchyme cells of the chick growing in tissue 
cultures. These investigators summarize the researches of others upon 
the subject and give the following figures for the chick cells: 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 cytokinesis, 2 to 13, 
usually 3 to 6; telophasic reconstruction of daughter nuclei, 30 to 120; 
total, 70 to 180 minutes. 


Detailed Description of the Behavior of the Chromosomes in Somatic 
Mitosis. 1 In the present account we shall depart from the order usually 
followed in descriptions of mitosis. Instead of commencing with the 
resting nucleus and tracing the steps leading to the formation of two 
daughter resting nuclei, we shall begin the description with the fully 
formed chromosomes as they appear at the metaphase and follow them 
through anaphase, telophase, resting stage, and prophase to the next 
metaphase, when they are again clearly seen. This is done in order that 
the account of the telophasic transformation of the chromosomes to 
form a resting reticulum, and the prophasic condensation of the latter 
to form chromosomes, may be given without interruption, which seems 
advisable in view of the nature of certain questions which are later to 
be discussed in the light of chromosome behavior. 

Metaphase (Fig. 50, A). As the chromosomes arrange themselves 
upon the spindle preparatory to their anaphasic separation their double 
nature is clearly evident. The two halves may lie very close together 
and in the case of long chromosomes may be somewhat twisted about 
each other. When they lie a little apart they may often show small 
connecting strands or anastomoses; in the immediately preceding stages 
(late prophase) the halves are usually pressed tightly together, so that 
these anastomoses appear to be due to mutual coherence at certain 
points when the halves move slightly apart after the disappearance of 
the nuclear membrane. As the double chromosomes take their places 
on the spindle, the spindle fibers become attached to them, not to all parts 
but to a particular portion of each. In the case of long chromosomes 
the point of attachment is often at about the middle, whereas in shorter 
ones it is commonly near one end. At their points of attachment to 
the spindle the double chromosomes all lie with their halves superposed 
(one half toward each spindle pole) and in a single plane; those portions 
to which no fibers are attached may extend in various directions with no 
regular arrangement. 

Anaphase (Fig. 50, B-D). Tjfce daughter chromosomes (the halves 
of the double chromosomes seen at metaphase) now begin to separate, 
first at the point of insertion, and gradually move away from the equa- 
torial plane. Owing to the different locations of the points of fiber attach- 
ment, and also to the fact that the free ends of the chromosomes occupy 
various positions, the chromosomes, unless they are very short, may now 

1 This description is based on the author's accounts of somatic mitosis in Vicia 
faba (1913) and Tradescanlia virginiana (1920). In these papers, especially in the 
first, there is presented a more extensive comparison of the results of other investi- 
gators than can be given here. Comparative studies have shown that in general 
the present description is widely applicable to mitotic phenomena in plants and ani- 
mals, although many modifications in detail are known, particularly in forms with 
small chromosomes. A useful list of works on mitosis in angiosperms is given by 
Picard (1913). 



be drawn into a number of peculiar shapes. In the case of long chromo- 
somes the portions to which the fibers are attached may have reached 
the poles of the syndic while the other portions are not yet separated 
at the equatorial plane. As soon as the daughter chromosomes become 
entirely free from one another they quickly draw apart and contract 
into two dense masses, which are often actually farther apart than were 

FIG. 50. Somatic mitosis in Tradescantia viryiniana: metaphase (A), anaphase (B-D), 
and telophase (E-G). At F are shown cross sections of chromosomes in the stage shown 
at E. X 1900. (After Sharp, 1920.) 

the poles of the spindle at metaphase. In these masses the individual 
chromosomes can be distinguished only with great difficulty or not at all. 
With this stage, which has been referred to by Gr^goire and Wygaerts 
(1903) as the tassement polaire, the anaphase ends and the telophase 

Telophase (Fig. 50, E Fig. 51, /). After remaining tightly pressed 
together for a short time the chromosomes of each daughter group begin 
to separate, their individual boundaries again becoming visible. As they 
do so they cohere at various points where their substance becomes 
drawn out to form anastomoses. It seems clear that the main connec- 


tions between the chromosomes of the reorganizing telophase nucleus 
are formed in this way, at least in mitoses showing a tassement polaire 
stage; but it is also probable, as several investigators have pointed out, 
that other anastomoses may grow out from one chromosome to another 
in the manner of pseudopodia (Boveri 1904; Gates 1912; Strasburger 
1905; Dehorne 1911; Mliller 1912; Lundegardh). 

Reactions taking place between the various chromosomes and espec- 
ially between them and the cytoplasm now result in the production of 
the nuclear sap, or karyolymph. Between the outermost chromosomes 
and the cytoplasm and also within the chromosome group droplets of 
clear karyolymph appear, and where these come in contact with the 
cytoplasm a nuclear membrane is formed. As the karyolymph increases 
in amount the nucleus enlarg/es and the chromosomes become more 
widely separated. 

The telophasic alveolation of the chromosomes, although it may in 
exceptional cases begin much earlier, usually commences at about the 
time the chromosomes first separate from one another in the early 
reorganization stages of the daughter nucleus. Within each chromosome 
vacuoles appear, first as obscure though rather sharply delimited circular 
or elongated areas. They lie not only along the axis but also near 
and against the periphery. This point is of importance in evaluating 
the claim advanced by certain investigators (Lundegardh 1910, 1912; 
Eraser and Snell 1911; Fraser 1914; Digby 1919) that the vacuolation 
is median and results in a splitting of the chromosomes during the telo- 
phase, rather than in the prophase. While the vacuoles develop into 
open spaces through the breaking down of the thin portions bounding 
them the nucleus increases rapidly in volume, so that each chromosome 
appears as an irregular net-like band joined to its neighbors by fine anas- 
tomoses. Careful study of the details of these telophasic changes (see 
cross sections of chromosomes in Fig. 50, F) shows that the alveolation 
proceeds with little regularity, and that each chromosome becomes an 
alveolar and then reticulate body with nothing which can properly be 
called a longitudinal split. 

In certain cases these internal changes, which result in the trans- 
formation of the chromosomes into a reticulum, and which as a rule do not 
begin until the telophase, may be initiated during the anaphase. In 
Allium, for instance, Miss Merriman (1904), Lundegardh (1910, 19126), 
and Nemec (1910) all report that the vacuolation of the chromosomes 
begins at this time. Even more striking is the case of Trillium (Gr^goire 
and Wygaerts 1903), in which the unusually large chromosomes may 
show vacuoles as early as the metaphase (Fig. 54, A). Internal changes 
of other types have also been described in anaphase chromosomes, but 
not with sufficient clearness to warrant their use in general interpre- 



According to Bonnevie (1908, 1911) the chromosomes of Allium, 
AscariSj and Amphiuma each give rise to an endogenous spiral thread 
during the telophases, this spiral thread persisting through the resting 
stages until the next prophase, when it again condenses to form a chromo- 
some (Fig. 54, J3). In his work on Salamandra Dehorne (1911) asserted 
that each chromosome is represented at telophase by two interlaced 
spirals arising from an anaphasic split, and further that these double 
structures are associated in pairs and persist in this condition through 
the resting stages. These two conceptions have been criticized by 
GrSgoire (1912), Sharp (1913), and de Smet (1914), who have inter- 
preted such appearances as occasional aspects of the alveolized chromo- 
somes .without the significance attributed to them by Bonnevie and 


FIG. 51. -Somatic mitosis in Tradescanlia virginiana: late telophase (//, I), inter- 
phase and resting stage (.7, K), and early prophase (L, M). X 1900. (After Sharp, 

In the young telophase nucleus the chromosomes may become ar- 
ranged in the form of a more or less continuous daughter spireme which 
is then transformed into the resting reticulum. This spireme stage, 
however, is not a necessary one; its absence is being reported with 
sufficient frequency to throw much doubt upon the view that it is a 
phenomenon of even general occurrence. 

/ The nucleolus usually makes its appearance during the early telophase 
as a small droplet or as several such droplets which may lat^gjMlow 
together. It seems to have little direct connection with tfie chromo- 
somes', but there can be no doubt that its appearance is closely associated 
with their physiological acti^ties. 

As ^ the telophasic changes proceed the chromosomes with their 
anastdmoses gradually form a more and more uniform reticulum, in 


which, however, the limits of tho component chromosomes can be 
distinguished until a very late stage. 

Interphase (Fig. 51, </). It often happens that in rapidly growing 
tissue, such as the meristem of the root tip, the mitoses succeed one 
another so rapidly that the telophasic changes may not proceed far 
enough to obscure the limits of the chromosomes in the reticulum 
before the changes of the ensuing prophase begin. In such tissue it is 
not always possible to tell whether a given nucleus will undergo further 
telophasic change or will at once enter upon the prophases. Such 
interphasic nuclei develop nucleoli, but karyosomes (in species which 
have these bodies) are usually not formed until a more advanced stage. 

Resting Stage (Fig. 51, J^K). In slowly growing tissue the successive 
mitoses do not follow one another with very great rapidity, and the 
telophasic changes are carried on until the condition characteristic of 
the typical resting nucleus is reached: the interphase here becomes the 
prolonged resting stage. The structure of the resting nucleus has been 
fully described in Chapter IV. In the reticulum the limits of the con- 
stituent chromosomes usually become indistinguishable, although it is 
known that in certain cases such nuclei, if properly sectioned and stained, 
may reveal heavier and lighter areas in the reticulum which represent 
respectively the chromosomes and the regions of anastomosis between 
them. The importance of these facts will be apparent in our treatment 
of the individuality of the chromosomes. 

Prophase (Fig. 51, L-Fig. 52). The first indication that the prophasic 
changes have begun is seen in the breaking down of the reticulum in 
certain regions. In the case of nuclei which show heavier and lighter 
areas in their reticula this breaking down occurs along the light portions. 
In view of what has been said concerning the origin of the reticuhmrat 
telophase it is apparent that the breaking up of the reticulum in the 
prophase represents in such cases the separation of the constituent 
chromosomes from each other along the lines of their telophasic union, 
and it has been inferred that a similar interpretation applies to those 
nuclei in which the reticulum is perfectly uniform or in which th$ nuclear 
material assumes more irregular forms. In this way there are developed 
from the resting reticulum a number of more or less distinct reticulate 
units, which, in view of their subsequent behavior, we know to be the 
chromosomes (Fig. 51, L, M). That these units are essentially the same 
as those which went to make up the reticulum at the preceding telophase 
seems highly probable; there can be little doubt on this point when the 
interphase is short. 

The material of each reticulate unit (chromosome) now gradually con- 
denses in a very irregular fashion about its open spaces and cavities. 
The thinner regions bounding these spaces and cavities become broken 
down, and the thicker portions remain as a very irregular pigzag thread of 


uneven thickness, which soon begins to straighten out (Fig. 52, P). At 
the same time the material composing the thread becomes more evenly 
arranged throughout its length, so that the chromosome eventually takes 
the form of a single slender thread. All of these changes condensa- 
tion, straightening, and equalization in thickness may be seen going 
on simultaneously in different chromosomes of the same nucleus, or even 
in different portions of a single chromosome. 

The formation of the slender prophase chromosomes from the retic- 
ulurn in the above manner was first described in detail by GrSgoire and 
Wygaerts (1903) and Grgoire (1906), and new cases have since been 
added. The above writers, together with Nemec (1910), Digby (1910), 




FIG. 52.- Somatic mitosis in Tradescantia virginiana: prophases. 

At N are shown cross sections of chromosomes in the stage shown in Fig. 51, M. 
X 1900. (After Sharp, 1920.) 

and Miiller (1912), believe that the separated portions of the reticulum 
may also condense directly into the slender threads without passing 
through the very irregular zigzag stage above described. It is probable 
that both methods are followed in different cases, direct condensation 
possibly being the rule in small nuclei. The view of Bonne vie (1908, 
1911) concerning the origin of the zigzag threads has already been 
mentioned in the paragraphs on the telophase. According to this worker 
and to certain others (Wilson 1912a6) the chromatic material forms a 
spiral thread within the chromosome during the telophase, this thread 
uncoiling and emerging from the chromosome in the following prophase. 
It is true that the zigzag threads occasionally have a strikingly regular 
spiral aspect, but in view of the many other aspects observed and the 
process which is known to give rise to them, it is probable that the 


formation of spirals in the manner described by Bonnevie is at least 
very exceptional. 

The true longitudinal splitting of the chromosomes is initiated in 
the slender threads of the early prophase (Figs. 52 and 53, Q). As soon 
as a thread becomes sufficiently equalized in diameter small vacuoles 
appear along its axis and rapidly develop into a more or less continuous 
split. Not all the threads, nor even all portions of the same thread, 
undergo the change at the same time. If we consider the whole nucleus 
at once, the processes of condensation, straightening, equalization, and 


FIG. 53. Somatic mitosis in Vicia faba: prophases. 
Stages P, Q, and S correspond with P, Q, and S of Fig. 52. X 1650. 

(After Sharp, 

splitting are all going on simultaneously; only in a given small portion of 
a thread do they follow in definite sequence. Furthermore, as soon as 
the threads become equalized they at once begin to shorten and thicken, 
so that when vacuolation and splitting are a little delayed they occur in 
somewhat heavier threads. 

The manner in which the vacuoles develop into the complete split 
should be carefully noted. The vacuoles quickly form openings which 
extend completely through the chromosome, so that the latter soon takes 
the form of two parallel strands connected by heavy cross pieces repre- 
senting the portions between the original vacuoles (Figs. 52 and 53, S). 


The material constituting the cross pieces gradually moves to the two 
side strands, the center portion of the cross piece becoming progressively 
thinner and the material accumulating on the side strands as a pair of 
chromatic lumps. Although some of the cross pieces may persist until a 
relatively late stage most of them soon disappear completely, and the 
material in the two chromatic lumps is gradually distributed more or 
less evenly along the parallel strands, which represent the daughter 
chromosomes resulting from the split. 

The double chromosomes now shorten and thicken, forming the 
" thick spireme" so conspicuous in prophase nuclei (Fig. 53, T, C7). As 
pointed out in the preliminary sketch of mitosis, the chromosomes in the 
prophase may form a more or less continuous spireme, but it is becoming 
increasingly apparent that this is not a universal phenomenon. It is 
certain that in many cases the chromosomes are separate from the first, 
and it seems therefore that any association in the form of a continuous 
spireme is a matter of secondary importance. As the shortening and 
thickening proceed the split may become obscured by the close 
association of the halves, but suitable methods reveal its presence. 

While indications of spindle formation are appearing in the cytoplasm 
the nucleolus disappears and the nucleus begins to contract, so that the 
thick double chromosomes become very closely packed together. While 
the contraction is at its height the nuclear membrane disappears, after 
which the chromosomes loosen up as an irregularly arranged group. 
This contraction stage evidently does not occur in many mitoses: the 
membrane may disappear while the nucleus has its full size. However, 
when it does occur it is of very short duration, so that it may take place 
in more cases than has been supposed. After the disappearance of the 
nuclear membrane the spindle fibers establish connection with the chro- 
mosomes, which quickly become arranged with their halves in superposi- 
tion at the equatorial plane, as described in the paragraph on the 
mctaphase. This brings us to the point with which our description, 

It should be added that in many descriptions of mitosis, notably 
those presented in general text books, the chromosomes are said to split 
during the metaphase, after they have become arranged upon the spindle. 
Such a late development of the split may indeed occur in some cases, but 
it is not improbable that" closer examination would often reveal the 
inception of the process at' a much earlier stage. Ag has been pointed 
out in the foregoing description, the early formed split frequently be- 
comes obscured during the later prophases owing to the shortening and 
thickening of the chromatin threads, and becomes conspicuous again 
only after the metaphase figure has been established. 

Chromomeres. One matter which should receive special attention is 
that of the chromomeres. It was held by Roux (1883) that the compli- 


cated process of mitosis is meaningless unless the chromatin is quali- 
tatively different in the various regions of the nucleus, and that tho 
arrangement of the material of the chromosome in the form of a long 
thread prior to its splitting is a means whereby all these qualities, ar- 
ranged in a linear series in the thread, are equationally divided and 
distributed to the daughter nuclei. The theory of Balbiani (1876) and 
Pfitzner (1881), that the chromatin granules visible in the nuclear reticu- 
lum arrange themselves in a series in the chromosome and by their 
division initiate its splitting, had much to do with the formulation of this 
hypothesis. . That the chromatic granules, or chromomeres (Fol 1891), 
represent the qualities of Roux is a theory which has been widely accepted 
by cytologists. It was the opinion of Brauer (1893) and many later 
workers that the granules or chromomeres, rather than the chromosomes 
themselves, are the significant units in the nucleus, and that their division 
is an act of reproduction. The division and separation of chromosomes 
was accordingly regarded as a means of distributing the daughter granules 
to the daughter cells. That the chromomere is made up of still smaller 
" chromioles" was held by Eisen (1899, 1900). Strasburger, Allen (1905), 
and Mottier (1907) also found the chromomere to be composed of smaller 
chromatic granules. 

FIG. 54. 

A t vacuoles in chromosomes at mctaphase in Trillium. X 1800. (After Grcgoirc and 
Wygaerts, 1903.) B, spiral arrangement of chromatin material within the chromosomes of 
Allium. (After Bonnevie, 1911.) C, D, stages of chromosome splitting in Najas marina, 
showing chromomeres. X 2250. (After Milller, 1912.) 

Although a large number of investigators, particularly those interested 
in the hereditary r61e of the chromatin, have placed much confidence in 
the importance of the chromomeres (Strasburger 1884, 1888), others 
have raised serious objections to the theory that they are significant units 
or individuals. Gr^goire and Wygaerts (1903), Martins Mano (1904), 
Gr^goire (1906, 1907), Marshal (1907), Bonnevie (1908), Stomps 
(1910), Lundegardh (1912), Sharp (1913, 1920), and others have found 
no such definite behavior on the part of the chromatin granules in the 
dividing chromosomes studied by them, and have suggested other ex- 
planations for the appearances observed. According to a modification 
of the chromomere theory adopted by Miiller (1912) the portions of the 
thread between the chromomeres split first, the division of the chromo- 


meres then following. It has been pointed out (Sharp 1913) that M tiller's 
figures (Fig. 54, C, Z>), which are very similar to the later ones of Stras- 
burger (1907), may be interpreted as steps in the division of a homogene- 
ous chromatic thread by the formation of vacuoles, and that the 
chromomeres in this case are merely the cross pieces between the halves 
of the incompletely split chromosome, as described in the foregoing account 
of the prophase (Fig. 53, S). 

It is becoming increasingly apparent that> the distinction between 
chromatin granules and supporting thread is not so sharp as has been 
supposed, since" the chromatic substance is often very fluid in consist- 
ency; and many have felt that the granules when present are far too 
inconstant in number and behavior to serve as the ultimate units which 
students of heredity hope to find. On the other hand, it should be said 
that the constancy in size and position of the chromomeres described 
by Wenrich (1U16) for the grasshopper, Phrynotettix (Fig. 155), argues 
strongly for the hereditary significance of these bodies, some of which 
can be seen to retain their identity through the resting stages. But 
whatever their importance may be, the arrangement of the chromatic 
material in the form of a long slender thread and its accurate splitting 
into exactly similar halves are very suggestive in connection with the 
theory of Roux that many qualities are arranged in a row and all 
divided at the time of nuclear and cell division. This subject will 
receive further attention in the chapters dealing with heredity. 

Summary. The chromosomes, after having arrived at the poles of the 
achromatic figure, become irregularly alveolized during the telophase and 
form ragged net-like structures. These are joined to each other by fine 
anastomoses and so make up the continuous reticulum of the resting 
stage. In the next prophase this reticulum breaks up into separate 
small nets or alveolar units, each of which represents a chromosome. 
The units condense in a peculiar manner and become long slender threads. 
These threads undergo a longitudinal splitting. The double threads so 
formed shorten and thicken, and become the double chromosomes which 
are arranged on the spindle at metaphase. The two halves (daughter 
chromosomes) making up each double chromosome separate and pass to 
opposite poles during the anaphase. 

The outstanding and significant feature of somatic mitosis is this: 
each chromosome is accurately divided into two exactly equal longitudinal 
halves which are distributed to the two daughter nuclei. The two daughter 
cells thus receive exactly similar halves of the chromatin of the mother celL 
Furthermore, as will be shown below, there is good evidence for the view 
that the chromosomes maintain an individuality of some sort, so that, 
since all the nuclei of the body arise by- the repeated equational division 
of a single nucleus, all the somatic (body) cells are qualitatively similar in 
chromatin content: they contain representatives or descendants of each and 


every chromosome present in the first cell of the series. ' The great theoretical 
importance of these facts will be apparent when we take up the subject 
of chromosome reduction, and the application of cytological phenomena 
to the problems of heredity. 


In later chapters the question of the significance of the nuclear struc- 
tures in heredity is to be considered. In connection with this question 
it is of the highest importance to determine whether or not the chromo- 
somes to which the reticulum gives rise in the prophase are in any real 
sense the same as those which went. to make up the reticulum at the pre- 
ceding telophase. That they do preserve their identity as individuals 
through the resting stage, arise only by division, an'd maintain therefore 
a genetic continuity throughout the life cycle, was held by van Benedcn 
(1883), Rabl (1885) and Boveri (1887, 1888, 1891) many years ago, and 
since that time the idea has received the support of a large number of 
investigators. We shall now briefly review some of the evidences which 
have led the majority of cytologists to the view that the chromosomes, 
"if . . . not actually persistent individuals, as Rabl and Boveri have 
maintained, . . . must at least be regarded as genetic homologues that 
are connected by some definite bond of individual continuity from gen- 
eration to generation of cells" (Wilson 1909). 

The Frequent Persistence of Visible Chromosome Limits in the 
Resting Reticulum. In the foregoing description of the behavior of the 
chromosomes in mitosis it was pointed out that in rapidly dividing tissue 
the telophasic alveolation of the chromosomes and their anastomosis to 
form the reticulum often do not proceed far enough during the interphase 
to obliterate the boundaries between the chromosomes, which separate 
again in the ensuing prophase without having lost their visible identity. 
In such nuclei there can be little doubt that the autonomy of the chromo- 
some is preserved. In other cases, however, the telophasic transforma- 
tion of the chromosomes is more complete and the resulting reticulum 
reacts very weakly to the stains, so that the limits of the constituent 
chromosomes disappear from view completely. Many workers have 
therefore objected to the statement that here also the chromosomes are 
present as! individuals, although invisible. Haecker (1902) and Boveri 
(1904) pointed out that this objection may be met by assuming that it is 
the achromatic framework of the alveolized chromosome, and not neces- 
sarily the basichromatic fluid held within it, that maintains a structural 
independence. This view had the support of the earlier observation 
made by Boveri (1887a, 1888a, 1891; also 1909) and confirmed by Herla 
(1893), that the chromosomes in the segmenting egg oi'Ascaris have a 
certain arrangement when they build up the nuclear reticulum in the 
telophase and reappear from the reticulum in the same position at the 
next prophase. 



Special emphasis was laid upon this interpretation by Marechal (1904, 
1007) as a result of his studies on the growth stage of animal oocytes. 
At this period in the development of the ovum the chromosomes assume 
a finely branched form (Fig. 86, C, D) and their ordinary staining capacity 
is lost completely. Although the chromatic fluid may flow from the 
rcticulum to the nucleolus and vice versa, and may periodically undergo 
chemical changes which radically alter its staining 'reactions, the achro- 
matic chromosomal substratum nevertheless maintains an uninterrupted 
structural continuity. Such a transfer of the basichromatic material 
from the persistent reticulum to the nucleolus during the telophase, and 
to the reticulum again during the succeeding prophase, has also been 

FIG. 55. Some evidences for chromosome individuality. 

A, chromosomal vesicles in Brachystoki mayna; x-chromosornc in vesicle at right. 
(After Sutton, 1902.) B, chromosomal vesicles in Fundulus embryo. X c,. 1800. (After 
Richards, 1917.) C, chromomere vesicle (c) on chromosome of Chorthippus. X 1500. 
(After W enrich, 1917.) D, prochromosomes in Pinguicula. X 4200. 

observed by Strasburger (1907) and Berghs (1909) in the somatic nuclei 
of Marsilia (Fig. 17, E). The chromosome, as Marshal urges, is not 
simply a mass of chromatm, but rather "a structure periodically chro- 
matic ;" hence the disappearance of stainable substance does not signify 
the loss of structural continuity on the part of the chromosome. 

The " chromosomal vesicles " (Fig. 55, A, B) observed by certain 
investigators constitute valuable evidence in this connection. In the 
spermatogonia of the grasshopper, Phrynotettix, for example, Wenrich 
1916) has shown that each of the alveolizing chromosomes forms its 
own vesicle about it at telophase, the several vesicles joining to form a 
common nucleus. In some cases the boundaries between the vesicles do 
not entirely disappear during the resting stages, and at the next prophase 


the chromatic material of each vesicle organizes in the form of a chromo- 
some. The same condition is found in the nuclei of Fundulus (Richards 
1917), Crepidula (Conklin 1902), and certain fish hybrids (Pinney 1918). 
From this it is evident that the morphological identity of the chromo- 
somes has not been lost between mitoses, although a very different type 
of organization has been assumed. 

In Carex aquatilis Stout (1912) has found a peculiar condition. Here 
the very small spherical chromosomes, which maintain a serial arrange- 
ment, are visible in the resting state, and can be traced continuously 
through all stages of the somatic and germ cell divisions with the excep- 
tion of synizesis. * 

The interpretations of Bonnevie (1908, 1911) and Dehorne (1911), 
according to whom the chromosomes persist through the resting stage as 
spirals or double spirals, have been mentioned in the description of 

Prochromosomes. Bodies known as prochromosomes have been 
described in the nuclei of a number of plants: in Thalictrum, CalycanthuSj 
Campanula, Helleborus, Podophyllum, and Richardia by Overton (1905, 
1909) ; in the Cruciferse by Laibach (1907) ; in Drosera and other forms by 
Rosenberg (1909); in Acer platanoides by Darling (1914); in Musa by 
Tischler (1910) ; and in a number of other forms. These prochromosomes 
appear as small chromatic masses in the reticulum (Fig. 55, Z>), and 
correspond approximately in number to the chromosomes of the species. 
They are generally looked upon as portions of chromosomes which have 
not undergone complete alveolation, and as centers about which the 
chromosomes again condense at the next prophase. This interpretation is 
in all probability a valid one in many of the described cases, but in others 
the significance of such chromatic masses is questionable. In Crepis 
virens de Srnet (1914), in harmony with the conclusions of Miss Digby 
(1914), finds them to be accumulations of material formed during the 
resting stages. If such is the case they are to be regarded as karyosomes. 

Persistence of Parental Chromosome Groups After Fertilization. In 
Chapter XII it will be shown that at fertilization there are brought 
together two sets of chromosomes, one set from each parent; and that in 
every nucleus of the resulting individual the chromosomes furnished .by 
the two parents are present together, all of them dividing at every mitosis. 
When the chromosomes of the male parent are similar to those of the 
female parent it is usually impossible to distinguish them in the nuclei 
of the offspring. In a number of cases, however, such as Crepidula 
(Conklin 1897, 1901), Cyclops (Haecker 1895; Ruckert 1895), and Crypto- 
branchus (Smith 1919) (Fig. 109), the two parental groups arc distinguish- 
able on the mitotic spindle, and often at other stages, through several 
embryonal cell generations. It is in hybrids that this phenomenon is 
shown most strikingly. In hybrid fishes obtained by crossing Fundulus 


with Menidia Moenkhaus (1904) washable to distinguish easily between 
the long (2.18 M) chromosomes of Fuwdulus and the short (1 M) ones of 
Menidia. Here, as in Crepidula and Cyclops, the paternal and maternal 
chromosomes form separate groups in the mitotic figure. A similar 
condition was seen by Tennent (1912) in hybrid echinoderms obtained by 
crossing in various ways Moira, Toxopneustes, and Arbacia. In the 
later cell-divisions the parental chromosomes mingle more or less, but are 
nevertheless distinguishable. In Fundulus X Ctenolabrus hybrids (Morris 
1914; Richards 1916), as well as in the normally fertilized Cryptobranchus 
(Smith 1919), the chromatin contributions of the two parents are dis- 
tinguishable even in the resting nuclei. 

Size and Shape of Chromosomes. One of the most striking evidences 
favoring the theory of individuality has been found in those plants and 
animals which show constant differences in size and shape among the 
various members of each parental chromosome group, so that particular 
chromosomes are recognizable in the group appearing at each mitosis. 
Since each parent furnishes a set of chromosomes to the new individual, 
each kind of chromosome is present in duplicate in the nuclei of this indi- 
vidual: it is therefore customary to speak of them as being present in 
pairs, although at most stages of the life history there is ordinarily no 
actual spatial pairing. 

Since the description of the chromosomes of Brachystola by Button in 
1902 (Fig. 101) the reported cases in which the different pairs of the 
chromosome complement possess different characteristic sizes and shapes 
have become increasingly numerous. This is notably true of insect 
cytology, as is evident in a review of the extensive researches of McClung 
(1905, 1914, 1917), Robertson (1916), Harman (1915), Carothers (1917), 
and many others. In the sea urchin, Echinus, Baltzer (1909) found that 
the 36 chromosomes have constant differences in length and shape, 
some being hooked and some horseshoe-shaped. In the flatworm, 
Gyrodactylus, (Gille 1914) there are six pairs, all different in length. In 
Ambystoma tigrinum Parmenter (1919) finds 14 pairs of graded sizes. 
In plants may be cited the cases of Crepis virens (Rosenberg 1909; de 
Smet 1914; M. Nawaschin 1915) (Fig. 56 bis, A), which has three pairs of 
different size; Vicia faba (Sharp 1914; Sakamura 1915), with five short 
pairs and one long pair (Fig. 56); smdNajas (Tschernoyarow 1914), in 
which there are seven distinguishable pairs (Fig. 56 bis, B). In Najas 
the smallest pair is attached to one of the larger pairs: Sakamura (1920) 
thinks that these together are really a single pair with pronounced 

Not only may certain chromosomes be distinguished on the basis of 
comparative length, but in some cases there may be other characteristics 
which serve as marks of identification. In the chromosomes of many 
plants and animals there are pronounced constrictions in some of the 



FIG. 56. The chromosome complement of Vicia faba. 

A, B, two successive sections of a mitotic figure in the root tip, showing together the 
12 split chromosomes, 2 of thorn about twice as long as the other 10. C, cross section of 
the group of chromosomes at anaphase: each of the long chromosomes, being drawn pole- 
wards by the middle, shows both ends, making the number apparently 14. D, E, two 
successive sections of a heterotypic figure in the microsporocyte, showing the 6 bivalents; 
the large one is at the left. F, polar view of heterotypic mitosis at metaphase, showing the 
bivalents. X 1400. (Original.) 


FIG. 56 bis. 

A, anaphase of somatic mitosis in Crepis mrens, showing 2 long, 2 medium sized, and 2 
short chromosomes passing to each pole. (After Rosenberg, 1920.) B, the chromosome 
complement in a somatic cell of Najas major, showing the 7 homologous pairs. (After 
TschernoyaroWj 1914.) 



members of the group. It has been shown in certain instances that these 
constrictions have constant positions in the chromosome. A careful 
study of this phenomenon bas been made by Sakamura (1915, 1920). 
In Viciafaba, for example ; he finds that each of the two long chromosomes 
("M-chromosomes") of the somatic group has two constant constrictions, 
one at the middle and one near the end ("m-constriction" and "e-con- 
striction") (Fig. 56, A). The m-constriction marks the point of attach- 
ment of the spindle fibers. There are also end-constrictions in 8 of the 10 
short chromosomes. On the basis of the widespread occurrence of con- 
strictions in the chromosomes of both plants and animals Sakamura has 
interpreted a number of puzzling phenomena, such as the apparent vari- 
ation in chromosome number within the species (see below) and certain 
features of the reduction process (Chapter XI) 

Such regularly situated constrictions have also been demonstrated in 
Fritillaria tenella by S. Nawaschin (1914). Here they are present at the 
middle of the largest chromosomes, nearer one end in the medium-sized 
chromosomes, and close to the end of the smallest ones. In Crepis virens 
(M. Nawaschin 1915) there are constrictions near one end in two of the 
three chromosomes of the haploid group in the pollen grain, in four of the 
six chromosomes of the diploid group in the somatic cells, and in six of 
the nine chromosomes of the triploid group in the endosperm cells. Such 
a definiteness in the location of constrictions was also seen earlier by Agar 
(1912) in the chromosomes of the fish, Lepidosiren. 

Somewhat similar evidence has been brought forward by Wenrich 
(1916), who finds that the chromatic lumps, or chromomercs, have a 
striking constancy in position as well as in size in the chromosomes of 
Phrynotettix (Fig. 155). Wenrich (1917) also reports that the small 
"chromomere vesicles" attached to the chromosomes of certain orthop- 
terans always appear at definite points along the chromosome (Fig. 55, C). 
It therefore appears that the chromosomes 'of a given group or comple- 
ment not only maintain a genetic continuity from cell to cell, but are also 
in some way qualitatively different from one another. They are conse- 
quently said to have a specificity as well as an individuality, or continuity. 
The relatively constant positions of the constrictions, chromatic lumps, 
and chromomere vesicles afford further visible evidences that the chrom- 
osome may possess some kind of lengthwise differentiation, a fact which, 
if clearly demonstrated, would be of the highest importance in connection 
with current views of the role of the chromosomes in heredity. (See 
Chapter XVII.) The significance of chromosome constrictions in this 
respect has been emphasized by Janssens (1909), S. Nawaschin (1915), 
and Sakamura (1920). 

Chromosome Number. 1 It was long ago noticed by Boveri, van 

1 For lists of chromosome numbers in plants see Ishikawa (1916) and Tischler 
(1916). For the numbers in animals see Harvey (1916, 1920). 


Beneden, and Strasburger that the number of chromosomes in any given 
species is relatively constant. It was largely upon this fact that the 
theory of chromosome individuality was originally based: the fact that 
the number of chromosomes appearing at every mitosis is almost invari- 
ably the same was taken to mean that the structural identity of the 
chromosomes is never lost. Certain observers (Fick 1905, 1909) have 
held that the apparent constancy in number is not due to a structural 
continuity or individuality of any sort, but rather to the fact that the 
successive nuclei have a relatively uniform amount of nuclear material, 
the chromosomes "crystallizing out" of this material in each prophase 
and going into solution at the close of mitosis. This idea was especially 
developed by Delia Valle (1909, 1912a6), who described the formation 
of chromosomes by the aggregation of fluid crystals during the prophase. 
These chromosomes he held to be in no sense morphologically continuous 
individuals, but only temporary chromatic accumulations which are in- 
constant in number and lose their identity in the telophase. Delia Valle's 
interpretation of chromosome formation has been criticized by a number 
of writers and his position shown to be untenable by Montgomery (1910), 
McClung (1917), and Parmenter (1919). 

Some of the experiments on echinoderm eggs with which Boveri (1895, 
1902, 1903, 19046, 1905, 1907) and others supported the theory of chromo- 
some individuality may be briefly reviewed. 

Boveri found that if the number of chromosomes is increased or do- 
creased by artificial means the altered number appears at every mitosis 
thereafter, (a) An enucleate egg fragment may be entered by a sperma- 
tozoon, and may then develop into a larva with half the normal number 
of chromosomes in every cell. (6) In another experiment the unfertilized 
egg of a sea urchin was caused to undergo division by artificial means, 
after which a spermatozoon was allowed to enter one of the blastorncres 
(daughter cells). A larva resulted in which one-half of the cells had regu- 
larly 18 chromosomes (half the normal number) while the other half had 
the normal 36. (c) Two spermatozoa occasionally fertilized one egg: 
the cells of the resulting larvae had 54 chromosomes, the triploid number. 
Abnormal mitotic figures were often formed in such dispcrmic eggs, 
bringing about an irregular distribution of the chromosomes. For 'ex- 
ample, a quadripolar spindle was produced, separating the 54 split chromo- 
somes (108 daughter chromosomes) into four groups, with 18, 22, 32, and 
36 chromosomes respectively (Fig. 127 Ws). The resulting abnormal 
larva ("pluteus") showed these four chromosome numbers in the cells 
of four different regions of its body. Boveri (1914) later suggested that 
malignant tumors might be due to such abnormal chromosome distri- 
bution, (d) The number of chromosomes was doubled by shaking th 
eggs while the chromosomes were split during the early stages of cell- 
division. In this manner larvae were produced with 72 chromosomes, tho 


tetraploid number, in all of their cells, (e) In the threadworm, Ascaris 
megalocephala, fertilization of an egg of the variety bivalens (two chromo- 
somes) by a spermatozoon of the variety univalens (one chromosome) 
resulted in a larva with three chromosomes in all its cells, the chromosome 
contributed by the male parent being distinguishable from the other two 
(Boveri 1888a; Herla 1893; Zoja 1895). 

Results such as the above led Boveri to the conclusion that the number 
of chromosomes arising from the reticulum in prophase is directly and 
exclusively dependent upon the number that went to make it up in the 
preceding telophase. If a nucleus is reconstructed in the telophase by an 
abnormal number of chromosomes as the result of a disturbance of the 

10 9 876 54321 


FIG. 57. The chromosome complement of Hcsperotettix viridix. 

A, the 12 bivalent chromosomes of the spermatocyte, including the accessory chromo- 
some (No. 4.) J5, complement from another individual, showing two "multiple chromo- 
somes." Nos. 11 and 12 have united temporarily, as have also Nos. 4 and 9. X 1800. 
(After McClung, 1917.) 

mitotic process, the altered number invariably appears in the succeeding 
prophase: if extra chromosomes are present they are not eliminated in 
any way during the resting stages, and if chromosomes have been lost 
during abnormal mitosis they are not replaced. These conclusions have 
been strikingly confirmed by Sakamura's (192D) work on cells subjected 
to the influence of chloral hydrate and other agencies causing aberrant 
chromosome behavior. 

Variations in Number. Although the number of chromosomes in a 
given species is on the whole remarkably constant, departures from nor- 
mal numbers are occasionally observed. Strasburger (1905) believed 
that the number, though determined by heredity, is not so rigidly fixed 
that all variation in the vegetative cells is excluded; only in the reproduc- 
tive cells did he hold constancy in number to be necessary. Much light 


has been recently thrown upon such apparent variations in number by 
McClung (1917) and Miss Holt (1917) in their researches on multiple 
chromosomes and chromosome complexes. 

McClung finds in his analysis of the chromosome groups of the 
orthopterans Hesperotettix and Mermiria that temporary associations 
often occur between various members of a group, with the resulting forma- 
tion of " multiple chromosomes" and a consequent decrease in the appar- 
ent number. In Hesperotettix, for instance^ the cells normally have 12 
pairs of chromosomes, but because of the formation of such multiple 
chromosomes individuals with apparently 11, 10, or 9 pairs are frequently 
found (Fig. 57). For a given individual the number so formed is Qxactly 
constant, since the members of a multiple remain together in all the cells 
of the body; but for the species it is variable within certain limits, owing 
to the varying numbers of chromosomes which may become involved in 
such multiple combinations. In all cases the full number of chromosome 
pairs is present, but some of them are so combined that there is an appar- 
ent, though not actual, variation in the number. A similar condition is 
found in other forms by Robertson (1916). 

In Culex there are three pairs of chromosomes in the somatic cells. 
During a certain stage in the insect's metamorphosis it has been shown 
by Miss Holt (1917) that the chromosomes may split repeatedly, giving 
cells with much larger numbers up to 72 in some cases. These larger 
numbers, however, are nearly always multiples of three, indicating that 
the subdivision of the chromosomes is an orderly process. The daughter 
chromosomes, moreover, that are formed by the subdivision of each of 
the original six, remain more or less closely associated as a " multiple 
complex/' which behaves as a single individual in mitosis. It therefore 
appears that the three pairs of chromosomes "are made up of quite 
distinct individuals differing from each other to such a degree that 
chromatin split from one cannot associate itself with that from another 
pair. . . . Chromosome individuality, alone, can account for these 
conditions. " 

Somewhat similar evidence has been brought forward by Hance (1917, 
1918a6). Hance finds that the chromosome number in the spermatogo- 
nia of the pig is regularly 40, whereas in the somatic cells it varies from 
40 to 57. Similarly in (Enothera scintillans, which has 15 chromosomes 
in its microsporocytes, there may be from 15 to 21 chromosomes in the 
somatic cells. Measurements of the members of the various chromosome 
groups show that the larger numbers are due to a fragmentation, prob- 
ably of the larger chromosomes, in the somatic cells. Such fragments 
divide normally, and it appears probable that the fragments of a single 
original chromosome are held together by colorless portions and behave 
as a unit, much as do the multiple complexes of Culex. 

Sakanuira (1920) believes that the chief reason for frequently reported 


inconstancies in chromosome number is to be found in the chromosome 
constrictions, which under certain conditions become especially pro- 
nounced and temporarily divide one or more of the chromosomes of the 
group into loosely connected smaller parts. This suggestion, which 
Sakamura supports with much direct evidence, is probabty one of the 
most fruitful which has been made in this connection. 

The theory of chromosome individuality is believed by McClung 
and Hance to be strengthened, rather than weakened, by such instances 
of numerical variation as those described above. McClung emphasizes 
the point that the composition of a given chromosome can be fully under- 
stood only if something is known of its genetic history, for what appears 
as a chromosome may often be either an aggregation of two or three 
chromosomes, or, on the other hand, only a portion of the true chromo- 
some individual. How widely this interpretation may be applicable to 
other reported cases of numerical variation and to chromosome structure 
in general cannot at present be stated, but it promises to lead to signifi- 
cant results. 

Discussion and Conclusions. The author's views on the subject of 
the individuality of the chromosomes can be most effectively stated in 
the words of McClung (1917): 

" . . . the practical matter before us is to decide whether the metaphase chromo- 
somes of two cells are individually identical organic members of a series because 
they were produced by the observed reproduction of a similar series of the parent 
cell, or whether the resemblance is independent of this genetic relation and due to 
chance association of indifferent materials, or to a reconstituting action of the cell 
as a whole. " 

"If it were possible for chromosomes to reproduce themselves and still pre- 
serve their physical configuration unchanged, there would probably be little 
question of their continuity and individuality the demonstration would be self- 
evident. But it happens that the necessities of the case require that each newly 
produced chromosome should take part in the formation of a new nucleus, through 
whose activities the cell as a whole and each chromosome, individually, is enabled 
to restore the volume diminished by the act of division. During this process the 
outlines of the chromosomes become materially changed and in their extreme 
diffusion can no longer be traced in many cases. Because of our limitations in 
observational power they appear to be lost as separate individuals and we are 
thus deprived of the simple test of observed continuity. Later, in the same cell, 
there reappears a series of chromosomes severally like those which seemed to 
disappear during the period of metabolic activity. We confront two alternative 
explanations for this reintegration of the chromosomes; either they actually 
persist as discrete units of extremely variable form, or they are entirely lost as 
individual entities and are reconstituted by some extrinsic agency. There is no 
other possible explanation and we must weigh the facts for one or the other of the 

All the facts which indicate order and system in chromosome features speak 
for the former, those which demonstrate variability and indefiniteness, for the 


latter. The case for discontinuity is strongest in the absence of any chromosome 
order, and becomes progressively weaker with the establishment of definiteness 
and precision in form and behavior." 

"So far as I can see there is no half way ground between the assumption that 
the chromosomes are definite, self-perpetuating organic structures and the other 
which presents them as mere incidental products of cellular action. According 
to one view individual chromosomes are descendents of like elements and possess 
certain qualities and behavior because of their material descent, the visible 
mechanism for which is the process of mitosis : according to the other any similari- 
ties that may exist in the complexes are the result of chance aggregations of non- 
specific materials. It is a choice between organization arid non-organization in 
the last analysis, at least in terms of cellular structures. To attempt the sub- 
stitution of a conception of molecular organization, which is beyond the ex- 
perience of the biologist and which exceeds the present powers of the chemist to 
analyse, is to cast aside all hope of solving the problem of cellular action, because 
it is necessary to understand, not only the physical and chemical phenomena 
involved, but also their different forms in the various parts of the cell." 

"That the chromosomes do not maintain a compact and easily recognizable 
form in the interval between mitoses is accepted by many . . . biologists as proof 
that they no longer exist as entities. All the other manifold indications of char- 
acter and continuity do not weigh against this apparent loss of identity. Doubt- 
less it would be more satisfying if we could at all times perceive the chromosomes 
in unchanging form in all stages of cellular activity, but why we should demand 
this condition as a test of individuality in the chromosomes when we unhesitat- 
ingly admit the unity of the organism in all the varied changes of its develop- 
ment from a single cell, through such complexities of change and metamorphosis 
as to give rise to doubts of even the phyletic position of some stages, it is difficult 
to see. Being organic, the chromosomes must change their form, they must suffer 
division of their substance and they are obliged to restore this loss through meta- 
bolic changes. Since these changes of substance take place at surface contacts 
there is an obvious advantage in increased superficies and, in common with other, 
larger structural elements, the chromosomes become extended and their sub- 
stances are diffused. In this state their boundaries may not be well defined and 
this circumstance has been seized upon as a disproof of their continuity." 

"Since it is not possible to observe directly the action of the chromosome we 
are obliged to make use of indirect evidence, seeking parallels between elements 
of structure and action in the chromosomes, and the mass effect of cellular action 
as exhibited in the so-called body characters. Such a method is justified by all 
other experience in tracing relations between structure and function in organisms, 
and while it apparently resolves the organism into parts of greater or less in- 
dependence, has given us our best conceptions of it as a whole." 

"What is postulated ... is that the chromosomes are self -perpetuating 
entities with individual peculiarities of form and function to identify them. 
Characteristics of form and behavior we see; certain very definite parallels be- 
tween these and the manifestations of somatic characters exist beyond question; 
provision for the perpetuation of the organic unity of the individual chromosomes 
is found in the process of mitosis; the actual direct result of its operation appears 
in 'the uniform conditions of the complex in the individual animal; the extension 


of this beyond the organism to the group and the means for it in the phenomena 
of maturation and fertilization are easily established by observation; the age 
old existence of all these circumstances is revealed by the near approach to 
uniformity in the chromosome complex of the multitude of species of unnumbered 
individuals constituting a family. And yet, in the face of this overwhelming 
mass of evidence indicative of order, system and specific chromosome organiza- 
tion, some conceive only the action of ordinary chemical forces, or the chance 
association of indifferent substances, while others, over impressed with the 
thought of a general coordinating force in the organism, deny significance to the 
orderly play of its cellular parts." 

"It is my belief that the observed act of reproduction, by which the organiza- 
tion of the chromosomes is materially transmitted in each mitosis, together 
with all facts indicating extensive distribution of given conditions, definiteness 
of organization, uniformity of behavior and consistence of deviation from the 
normal, are so many clear indications of the individual character of the chromo- 
somes. Transmutation of form, even to an extreme degree, can not be held as a 
valid argument against a persistent individuality. A consideration of the criteria 
applied to larger organic aggregates well supports this view. Such objects are 
said to possess individuality when they exhibit a more or less definite unity which 
is persistent and characterized by peculiarities of form and function. Most 
clearly defined is this individuality when it may be perpetuated through some 
form of reproduction to find expression in new units of similar character. The 
term does not connote unchangeability, and there may be fusions with more or 
less loss of physical delimitations, followed by separation, even after exchange 
of substances. The test of individuality is material continuity, but it does not 
necessarily involve complete or entirely persistent contiguity. 1 An organism may 
bud off new individuals similar to itself, the substance of its body differs from 
time to time, movements of parts take place, fragmentation occurs, extreme 
attenuation or extension of substance is found, even separation and recombina- 
tion of parts may happen and yet the individual maintains itself. What it may 
have been in the past, what its possibilities of future development are, what 
potentialities of multiplied individuality it suppresses do not affect the reality of 
its individuality. It is, as Huxley says, 'a single thing of a given kind/ If 
*one such thing divides into two, there are two individuals; if two unite into one 
indistinguishably there is a single individual; if a fusion of two things occurs in 
part, without loss of physical configuration, there are still two individuals in 
existence. Only when the substance of one thing disappears or becomes in- 
corporated integrally into the organization of another does its individuality 

If all these variations of physical state may occur in the history of an organism 
without sacrifice of individuality, there can be no reason for urging them against 
a conception of the individuality of the self -perpetuating chromosomes." 

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1883. Das Ei und seine Befruchtung. Breslau. 

SHARP, L. W. 1913. Somatic chromosomes in Vicia La Cellule 29: 297-331. 

pis. 2. 

1914. Maturation in Vicia. (Prelim, note.) Bot. Gaz. 67: 531. 
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DE SMET, E 1914. Chromosomes, prochromosomes, et nuc!6ole dans quelques 
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SMITH, B, G. 1919. The individuality of the germ nuclei during the cleavage 
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STOMPS, T. J. 1910. Kerndeeling en synapsis bij Spinacea oteracea. (German 
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The spindle fibers and asters about the centrosomes (when these arc 
present) are collectively termed the achromatic figure, in contradistinction 
to the chromatic figure, or chromosomes. Compared with the chromo- 
somes the achromatic figure is relatively little understood, which makes 
it a very unsatisfactory subject for discussion. We shall first describe 
the achromatic figure in its more common forms, and after mentioning 
certain theories which have been propounded to explain its origin and 
nature we shall briefly review a few of the suggestions which have been 
made on the subject of the mechanism of mitosis. 

In Higher Plants. In somatic mitosis in higher plants the achromatic 
figure is devoid of centrosomes and asters. Ordinarily it arises and be- 
haves as follows: While the prophasic changes are taking place within 
the nucleus the first indications of spindle formation appear in the cyto- 
plasm in the immediate vicinity of the nucleus. At the two sides of the 
latter, in the general position of the future spindle poles, there are de- 
veloped two masses of more or less hyaline material, usually called "kino- 
plasmic caps." In these two polar caps delicate fibrils soon appear, as 
if by a process of condensation (Fig. 58, A, B). The nucleus commonly 
shrinks at this time, while the fibrous areas increase in size and together 
form a more definitely spindle-shaped figure. After the nuclear mem- 
brane has shrunken more closely about the chromosomes it goes into 
solution and the ingrowing fibers attach themselves to the longitudinally 
split chromosomes. In many cases the membrane disappears without 
shrinking, the fibers growing considerably in length to reach the chromo- 
somes. The latter quickly become regularly arranged in the equatorial 
plane preparatory to their separation (Chapter VIII). The mitotic 
figure is now established (Fig. 48). The many fibers composing the 
spindle may focus at a single sharp point at each pole, or they may end 
indefinitely without converging to a point, forming in the latter case a 
broad-poled figure which in extreme cases may be as wide at the poles 
as at the equator (Fig. 74, D). Some of the fibers extend from the poles 
to- the chromosomes, to which they are attached, while others pass 
through from one pole to the other without being so attached: these 




two sets of fibers are known respectively as mantle fibers and connecting 
fibers. The latter are also collectively termed the central spindle. 

It is during the anaphases and telophases that the connecting fibers 
become most evident; in mitotic figures with many chromosomes it may 
be impossible to see them at metaphase. At the beginning of the telo- 
phase they may form a bundle no greater in diameter than the daughter 
chromosome groups, but as the daughter nuclei reorganize the fibers 
commonly bend outward at the middle, forming a barrel-shaped phrag- 
moplast (Fig. 58, C) which in plants usually continues* to widen by the 
addition of new fibers until it comes in contact with the lateral walls of 
the cell. 

FIG. 58. 

A, spindle beginning to differentiate in kinoplasmio caps at poles of nucleus in Ncphro- 
dium. (After Yamanouchi, 1908.) /?, same in Marsilia. (After Berghs, 1909.) (7, />, 
the origin of the cell wall in Pinus: C, connecting fibers between daughter nuclei at telo- 
phase; D, thickenings appearing on fibers. E, the continued extension of the cell wall 
after the completion of mitosis in the endosperm of Physostegia virginiana. X 215. (After 
Sharp, 1911.) F, multipolar stage of spindle development in microsporocyte of Acer 
Negundo. X 1125. (After Taylor, 1920.) 

While the above changes are occurring the new cell wall which is to 
be formed between the daughter nuclei begins to differentiate. As the 
central spindle widens the fibers become fainter near the nuclei and more 
prominent at the equatorial region: this appearance seems to be due to 
the flow of the material composing the fibers toward the latter region. 
On the thickened fibers there now appear small swellings (Fig. 58, D) 
which increase in size until they fuse to form a continuous plate across 
the equator of the mother cell, thus dividing the latter into two daughter 
cells. As this cell plate undergoes further changes (see p. 190) the fibers 
disappear completely, first near the two nuclei and ultimately at the 
equatorial region near the new wall. If the cell undergoing division 
is very broad it often happens that wall formation begins near the center 
of the phragmoplast while the latter is still extending laterally. In 


extreme cases wall formation may still be seen in progress at the periphery 
after the fibers have completely disappeared at the central region (Fig. 
58, E). Such is notably the case in the tangential divisions of elongated 
cambium cells (Bailey 1919, 1920). 

The spindle in many cases has an origin somewhat different from that 
described above. The first indication of its differentiation is here the 
appearance of a weft of fine fibrils in the cytoplasm all around the nucleus 
(Fig. 84, E). As these fibrils increase in size and number they may 
form several distinct groups extending in various directions, thus giving 
a multipolar spindle (Fig. 58, F). Some of the groups then gradually 
disappear, while others alter their positions and coalesce, so that a bipolar 
spindle eventually results. This, in general, is the manner in which the 
spindle arises in the microsporocytes of angiosperms. For example, 
Lawson (1898, 1900, 1903) finds that in Cobcea, Gladiolus, and Iris a 
zone of granular "perikaryoplasm" collects about the nucleus during 
the prophases of mitosis. When the nuclear membrane dissolves, this 
substance together with the linin of the nucleus forms a fibrous network 
which grows out into several cones of fibers, and these later become 
arranged in two opposed groups. 

In Animals. In the majority of animal cells, and in certain cells of 
lower plants also, the achromatic figure is a much more elaborate struc- 
ture than that of the higher plants described above. This is due to the 
presence of centrosornes, which with their asters are very conspicuous at 
the time of mitosis. Commonly the aster is not present during the resting 
stages of the cell, but cases are known in which both centrosome and 
aster are visible, forming with other materials an " attraction sphere" in 
the cytoplasm. As the process of mitosis begins (Fig. 59), an aster, if 
not already present, develops about the centrosome. The centrosome 
divides, and as the daughter centrosornes move apart each is seen to be 
surrounded by its own aster, and a small group of fibers ("central spin- 
dle ") extends between them. The achromatic figure, made up of the 
asters and the spindle connecting them, is known both at this stage and 
later as the amphiaster. As the daughter centrosomes continue to sepa- 
rate the astral rays increase in prominence. Some of the rays grow into 
the nucleus when its membrane disappears and become attached as 
mantle fibers to the chromosomes, while the lengthening central spindle 
between the asters becomes the central spindle portion (connecting fibers) 
of the completed mitotic figure (Fig. 49). All the fibers focus upon the 

During the anaphase the asters remain very conspicuous, but as the 
telophases progress they gradually fade from view, except in those forms 
which have a more or less permanent attraction sphere. Aside from the 
presence of centrosomes and asters the achromatic figure in animal cells 
differs most conspicuously from that of higher plant cells in its behavior 



I ^-ss 


FIG. 59. Mitosis in the spermatocyte of Salamandra. 

/, prophase, centrosomes in astrosphere substance; latter spread out on. nucleus. I/, 
prophase; bivalent chromosomes formed; centrosomes beginning to diverge; central spin- 
dle and asters developed. ///, late prophase: nuclear membrane dissolved; spindle 
fibers attaching to chromosomes, centrosomes moving apart. IV, anaphase: connecting 
fibers prominent. V, telophase: constriction of cell nearly complete; mid-body forming 
pn central spindle or interzonal fibers. (After Meves, 1907.) 

FIG. 00. Elaborate achromatic figure in oocyto of Pisciola. X 1000. 
( After JorQcnsen , 1 9 1 .'J.) 


during the telophases. Instead of forming thickenings which become an 
equatorial cell plate, the connecting fibers play relatively little part in 
cytokinesis. One or more granules may be differentiated on the fibers 
at the equatorial region, forming the so-called " mid-body," but the 
actual division of the cell is brought about by the development of a 
cleavage furrow, as will be described in the section on cytokinesis. 

Intranuclear Figures. In the above described cases of mitosis in 
plants and animals the achromatic figure is derived mainly from the cyto- 
plasmic region of the cell, the nuclear materials playing a relatively 
minor part. In a number of forms, both among animals and plants (fungi, 
for example), the spindle arises entirely in the nuclear region, forming 
an intranuclear figure which may be completely established before the 

FIG. 61. 

A, B, anaphase and telophase of mitosis in ascus of Laboulbenia chastophora. X 135O. 
(After Fault, 1912.) (See also Fig. 22.) C, intranuclear mitotic figure in oogonium of 
Fucus. (After Yamanouchi, 1909.) 

nuclear membrane disappears. Cases are known in which the centro- 
somes themselves are also intranuclear, but usually these bodies lie in 
the cytoplasm against the nuclear membrane, so that although the spindle 
portion of the figure is within the nucleus the asters lie in the cytoplasm. 

In the division of the nucleus in the ascus of an ascomycete, 1 to take 
a single example, the process is as follows (Figs. 22; 61 A, B): The 
centrosome, which in ascomycetes is often discoid in shape, lies against 
the nuclear membrane. As mitosis begins an aster develops in the cyto- 
plasm 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 
where the chromosomes are being formed from the reticulum. The 
centrosomes finally reach opposite sides of the nucleus, and their two 

1 For references to the literature of mitosis in ascomycetes see page 290. 


groups of fibers become arranged in the form of a sharp poled spindle 
extending through the nucleus with the chromosomes at the equator. 
The nuclear membrane commonly remains intact until the chromosomes 
approach the poles at anaphase; it then disappears, allowing the 
nucleolus, which has remained unchanged, to escape into the cytoplasm 
nearby. Between the two densely packed daughter chromosome groups 
there extends a long strand of chromatic material: this soon disappears 
and the two daughter chromosome groups reorganize two daughter 
nuclei not separated by a wall. In those cases in which the division of the 
fungus nucleus is followed by the development of a separating wall the 
latter is formed by a cleavage furrow independently of the achromatic 

Origin of the Figure. Having before us the above examples of the 
achromatic figure, we may now refer very briefly to some of the ideas 
which have been advanced regarding the details of its origin in the cell. 1 
Early observers looked upon the whole rnitotic figure chromosomes, 
spindle, and all as a transformed nucleus, all the structures being formed 
from the nuclear material at each mitosis. Strasburger, who first held 
this view, later (1888), with Hermann (1891), believed the spindle to arise 
wholly from the cytoplasm, whereas 0. Hertwig pointed out cases in 
which the astral rays arise from the cytoplasm and the spindle from the 
linin reticulum of the nucleus. Flemming (1891) derived the fibers from 
the linin and the nuclear membrane. It soon became evident that the 
spindle, although in some cases arising entirely within the nucleus or 
wholly from the cytoplasm, is commonly made up of materials derived 
from both regions, as is evident from the examples described in the fore- 
going paragraphs. 

When van Beneden and Boveri announced their view that the centro- 
some is a permanent cell organ, transmitted by division to daughter cells 
and directly concerned in the formation of the asters, the theory was 
adopted that the figure arises from the cytoplasm as a result of the 
influence of the centrosome. The centrosome therefore came to be 
known as "the dynamic center of the cell." Although this organ does 
play a conspicuous role when present, its importance in connection with 
the achromatic figure was somewhat diminished when it became evi- 
dent that many centrosomes do not persist from one cell generation 
to the next, and that such bodies are entirely absent from the cells of 
higher plants*, 

Rearrangement Theories. Many attempts have been made to account 
for the formation of the achromatic fibrils in the cytoplasm. According 
to some the fibers and astral rays arise as the result of a morphological 
rearrangement of -the preexistent protoplasmic structure, chiefly under 

1 Extensive reviews of the early theories are given by Wilson (1900, pp. 72-86 and 


the influence of the centrosome. Blitschli (1876), who looked upon 
protoplasm as alveolar in nature, held that the rays are not really fibers, 
but only the lamellae between radially elongated alveolae about the cen- 
trosome. It was the opinion of Wilson (1899) on the other hand, that 
the rays are actual fibers, though their material is derived from the 
alveolar walls. Klein (1878) and others who believed protoplasm to be 
ultimately fibrillar or reticular in structure, regarded the rays as radially 
arranged fibrillae. Van Beneden (1883) supposed these fibrillse to be 
derived partly from the intranuclear reticulum, and Rabl (1889) 
pointed out that they are continuous with the unaltered cytoplasmic 
meshwork and arise by a direct transformation of the latter. In Passi- 
fiora Williams (1899) found that the nuclear membrane forms a meshwork 
connecting the linin reticulum with the cytoplasmic reticulum, all three 
together organizing the spindle. 

Special Substance Theories. According to another group of theories 
the spindle and asters are not formed merely by the rearrangement of a 
structure already present, but arise from a special substance in the cell. 
This substance was held by some to be a constantly present constituent 
of the cell, forming the achromatic figure at the time of mitosis and re- 
maining in reserve through the resting stages. Boveri's archoplasm 
hypothesis in its earlier form (1888) was a prominent development of 
this idea. According to this hypothesis the attraction sphere is composed 
of a distinct substance called archoplasnij which consists in turn of fine 
granules or microsomes aggregated about the centrosome as a result of 
the centrosome's attractive force. The entire achromatic figure was 
held to arise from this mass of archoplasm, the fibers and astral rays 
growing out from it like roots, to be withdrawn again into the daughter 
masses of archoplasm at the two poles during the closing phases of mitosis. 
In this way each daughter cell was thought to receive half of the archo- 
plasm. Although other workers (Watase 1894) also held that the fibers 
are outgrowths of the centrosome or centrosphere substance, it was made 
evident later that the material composing the fiber comes from the cyto- 
plasm, being added to the growing fiber at its end. This was the view of 
Druner (1894, 1895). Boveri later (1895) modified his archoplasm hypo- 
thesis, adopting the view that the fiber is formed from the substance of 
the cytoplasm and not necessarily from a constantly present archoplasm. 

Another theory based on the idea of a special substance in the cell 
was that of Strasburger (1892, 1897, 1898). Strasburger l&ld that the 
cell has two kinds of protoplasm : an active fibrillar kinoplastfi and a less 
active alveolar trophoplasm. The former constitutes the ectoplast, centro- 
somes, the mitotic fibers, and the contractile substance of cilia and 
allied structures. The kinoplasm is thus concerned with the motor 
work of the cell, whereas the trophoplasm has to do chiefly with 


The nucleolus has been thought by some observers to furnish material 
for the formation of the spindle, because of the fact that it very commonly 
disappears from view at about the time the spindle begins to differentiate. 
It is possible that in some cases there may be a connection of this sort 
between nucleolus and spindle, but it is clear that this cannot serve as a 
general interpretation of spindle origin. 

That the achromatic figure may arise from a special substance not 
constantly present in the cell, but formed anew at each mitosis, is a 
theory which several workers have advanced. The researches of Devise 
(1914) and Miss Nothnagel (1916) may be cited for illustration. Devise*, 
as the result of a careful study of the development of the spindle in the 
microsporocytes of Larix t concluded that the spindle is not formed by the 
rearrangement of any preexistent nuclear or cytoplasrnic structures, but 
arises from a substance which develops in the nuclear region during the 
late prophases (after diakinesis). He was not able to decide whether this 
substance is of purely nuclear origin or is formed when the karyolymph 
comes in contact with the cytoplasm. The interaction of karyolymph and 
cytoplasm is emphasized by Miss Nothnagel in her work on Allium. 
She points out that the contact of newly formed karyolymph with the 
cytoplasm at telophase brings about the precipitation of the nuclear 
membrane, and that in an analogous manner an exosmosis of karyo- 
lymph through the nuclear membrane into the cytoplasm during prophavse 
causes the precipitation of fine fibrils around the nucleus, these fibrils then 
developing into the spindle. The achromatic figure therefore arises 
from a special substance, but this substance, as in the case of Larix, 
is newly formed at each mitosis. 

. Conclusion. In general it may be said that although the spindle 
fibers and the motor and contractile elements of the cell appear to have 
a substantial relationship with one another, the substance common to 
them is probably "jiot to be regarded as being necessarily a permanent 
constituent of the cell, but only as a phase, more or less persistent, in 
the general metabolic transformation of the cell substance" (Wilson). 
Indeed the conspicuous tendency on the part of cytologists at present 
is to regard the achromatic figure neither as a mere rearrangement of a 
structure previously present, nor as a form assumed by a special spindle 
substance, but rather as the result of streaming, gelation, and other 
temporary alterations in the colloidal substratum. This interpretation 
is strongly supported by the microdissection studies to be cited in a 
subsequent paragraph. 

The Mechanism of Mitosis. Since the phenomenon of mitosis was 
first described there have been put forward a number of theories to ac- 
count for the operation of the achromatic structures in bringing about the 
separation of the daughter chromosomes and for the division of the cell. 
Many of the suggestions undoubtedly contain elements of truth, but it 


must be admitted that there is no immediate prospect of a satisfactory 
solution of these problems. 

^Contractility. One of the simplest and most widely accepted theories 
was that of fibrillar contractility suggested by Klein (1878) and van 
Beneden (1883, 1887), according to which the chromosomes are simply 
dragged apart by the contraction of two opposed groups of spindle fibers. 
This theory and its modifications are fully reviewed by Wilson: it will 
be sufficient here to point out that, whereas many facts were cited in its 
favor, and elastic models made which simulated the supposed contraction 
and its results (Heidenhain), the further evidence brought forward by 
Hermann (1891), Drtiner (1894, 1895), Calkins (1898), and others led to 
the general restriction of the role of contractility, until it became appa- 
rent that this factor, although it may contribute to the general result, 
must be of minor importance. The contractility factor appeared again 
in the more elaborate theory proposed by Rhumbler, which may be 
briefly stated as follows: The ccntrosome arises as a local solidification 
of the walls of the alveolae; the denser constituents of the protoplasm 
collect at this point and form an attraction sphere, driving the less dense 
constituents to the other parts of the cell where the pressure is lower; this 
migration of fluid affects particularly those strands of the protoplasmic 
reticulum which radiate more directly from the centrosomes; these 
strands or rays, in giving up their fluid, shbrten, and thus exert a trac- 
tive force which draws the daughter chromosomes apart. In this theory, 
there^Jre, the main factors are streaming and contractility. 

^Streaming. The phenomena of streaming and surface tension have 
been prominent factors in several attempts to explain both karyokinesis 
and cytokinesis. The role of streaming in karyokinesis has been held to 
be especially important since Butschli, Hertwig, and Fol showed many 
years ago that currents exist in the protoplasm. Rhumbler (1896, 1899), 
Morgan (1899), Wilson (1901), and Conklin (1902) all held that the 
astral rays are due at least in part to centripetal currents. This inter- 
pretation has recently been confirmed by Chambers (1917) in his micro- 
dissection studies on the living cell. With regard to the aster Chambers 
says: "The formation of the aster consists in the gelation of the hyalo- 
plasm which comes under the influence of the astral center. A hyaline 
liquid separates out during the gelation and flows in innumerable centri- 
petal paths toward the center where it accumulates to form a sphere. 
This centripetal flow brings about an arrangement of the gelled hyalo- 
plasm containing the cell-granules into radial strands separated by the 
hyaline-liquid paths. This produces the astral figure. The strands of 
gelatinized cytoplasm merge peripherally into the surrounding liquid 
cytoplasm or reach and anchor themselves in the substance of the gelled 
surface when the aster is fully formed. The liquid rays merge centrally 
into the substance of the sphere, the liquid of the rays and of the sphere 
being thus identical." 


Sakamura (1920), although holding the fibers to be important agents 
in the normal separation of the daughter chromosomes, observes that in 
abnormal nuclear divisions where no fibers are present the chromosomes 
still show movements which are probably due to streaming of the cyto- 
plasm and to surface tension phenomena. 

The relation of streaming and surface tension to cytokinesis will be 
discj/ssed in the section dealing more particularly with cytokinesis. 

^/Osmosis. In a theory of the mechanics of karyokinesis proposed by 
Lawson (1911) the principal factor involved is osmosis. Lawson's ex- 
planation is essentially as follows. During the late prophase karyolymph 
passes outward through the nuclear membrane by osmosis, this loss of 
fluid resulting in a contraction of the nucleus. Owing to the fact that 
the cytoplasmic reticulum is continuous with the nuclear membrane this 
contraction sets up radial lines of tension in this reticulum on all sides of 
the nucleus. As the process continues these lines or "fibers" gradually 
become arranged in two opposed groups, while the nuclear membrane to 
which they are attached continues to contract until it actually enwraps 
each double chromosome. To each double chromosome there are thus 
attached fibers which represent stretched and distorted regions of the 
cytoplasmic reticulum extending to the two sides of the cell. When the 
chromosomes become properly arranged at the equatorial plane the 
fibers, which are under considerable tension, are able to pull the daughter 
chromosomes apart and draw them to the poles. As the fibers relax they 
resume their true reticular state. Although the chromosomes are thus 
drawn apart by the shortening of "fibers" attached to them, Lawson 
points out that this is not to be regarded as a case of true active contrac- 
tility, but only as a release of tension set up in the passive but elastic 
cytoplasmic reticulum as the result of the exosmosis of karyolymph from 
the nucleus. This theory has been severely criticized by a number of 
writers, chiefly on the grounds that such an enwrapping of the chromo- 
somes by the nuclear membrane as Lawson describes cannot be demon- 
strated in many objects subsequently examined, and that the membrane 
frequently goes into solution when both it and the growing fibers are 
stily some distance from the chromosomes. 

\J Electrical Theories. The striking resemblance between the achromatic 
figure and the lines of force in an electromagnetic field early led to at- 
tempts to account for mitosis on the basis of electrical principles. Several 
investigators, working with various chemical substances, succeeded in 
modelling fields of force that illustrated graphically the changes supposed 
to take place in the dividing cell. 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 
Lillie (1903) (see p. 62) on the behavior of nucleus and cytoplasm in 


the electromagnetic field, he concluded that the chromosomes and the 
cytoplasm carry charges of unlike sign: the daughter centrosomes repel 
each other and move apart because of their like sign, the spindle poles 
being of like sign also. The movement of the chromosomes to the poles 
he held to be due to the combined action of two forces: the mutual repul- 
sion of the similarly charged daughter chromosomes, and the attraction 
between the oppositely charged centrosomes and chromosomes. 

The fact that the two centrosomes and hence the two spindle poles 
are electrically homopolar (Lillie) and alike osmotically at once makes it 
apparent that the mitotic figure does not represent an ordinary electro- 
magnetic field, for in the latter the poles are of unlike sign the field is 
heteropolar. It has consequently been suggested by Prenant (1910) and 
Hartog (1905, 1914) that the mitotic figure is the seat of a special force, 
analogous to electrostatic force but not identical with it, which is peculiar 
to living organisms. This new force they call "mitokinetism." 

A large amount of discussion has centered about the possible r61e of 
electrical forces in mitosis, and many kinds of normal and abnormal 
mitotic phenomena have been cited as evidence for various views. So 
far as conclusive statements are concerned, there is disappointingly little 
of a definite nature that can be said. Meek (1913) asserts that the only 
generalization which is at present possible is the negative one that 
"the mitotic spindle is not a figure formed entirely by the action of 
forces at its poles/ 7 

Conclusion. In conclusion we may emphasize the fact that the 
achromatic figure depends for its operation upon a variety of interacting 
factors. Certain investigators have doubtless done good service in em- 
phasizing the importance of one or another of these factors streaming, 
surface tension, contractility, gelation, electrical phenomena, and the 
like but it has become increasingly evident that in no one of them alone 
is the key to the problem of mitosis to be found. In spite of the confi- 
dence that some progress has been made, at least in the elucidation of 
certain phenomena which must have a part in any ultimate explanation, 
it is nevertheless true that the statements made twenty years ago by 
Wilson (1900, p. Ill) may be taken as an essentially accurate expression 
of the condition of the subject: "When all is said, we must admit that 
the mechanism of mitosis in every phase still awaits adequate physio- 
logical analysis. The suggestive experiments of Butschli and Heidenhain 
lead us to hope that a partial solution of the problem may be reached 
along the lines of physical and chemical experiment. At present we can 
only admit that none of the conclusions thus far reached, whether by 
observation or by experiment, are more than the first naive attempts to 
analyse a group of most complex phenomena of which we have little real 
understanding. " 




In the foregoing pages discussion has been limited largely to karyo- 
kinesis. In the present section attention will be directed to cytokinesis, 
or the division of the extra-nuclear portion of the cell. 

In plants the wall separating the two daughter cells is formed by 
two general methods: cell plate formation and furrowing. The first and 
more common of these methods, by which a wall is formed in close 
association with the spindle fibers at the close of mitosis, has been briefly 
described in the foregoing section on the achromatic figure (p. 176) and 
will be taken up in greater detail in the following section on the cell wall 
(p. 190). At this point we shall therefore describe the second method, 
that of furrowing, which in plants is seen most conspicuously in the 
thallophytes and in the microsporocytes of the higher plants. The 
review of the subject given by Farr (1916) will be followed. 

Thallophytes. In Spirogyra Strasburger (1875) showed that the 
wall between the two daughter cells appears as a "girdle" or ring-like 
ingrowth from the side wall of the parent cell. This wall continues to 


FIG. 62. FIG. 63. 

Fio. 62. Cytokinesis by furrowing in Clostcrium. Only the central part of the cell 
is shown. X 700. (After Lutman, 1911.) 

FIG. 6,3. 

A, Cleavage furrows beginning to form at periphery of sporangium of Rhizopus nigricans. 
X 1500. B t Cleavage in the sporangium of Phycomyces nitens: intersporal substance in the 
angular furrows. X 500. (Both after D. B. Swingle, 1903.) 

grow centripetally by the addition of new material at its inner edge while 
the protoplast develops a deep cleavage furrow, the process continuing 
until the separating wall is completed at the center of the cell. A 
somewhat similar process occurs in Closterium (Lutman 1911) (Fig. 62). 
In the brown algse Sphacelaria (Strasburger 1892; W. T. Swingle 1897) 
and Dictyota (Mottier 1900) the wall develops uniformly across the 


whole equatorial plane at the same time, and not as a progressive in- 
growth from the periphery. 

In the fungi Harper and others showed that the two daughter cells are 
separated by the development of a cleavage furrow in which the new wall 
is laid down. In large multinucleate masses that become broken up into 
spores this progressive cleavage is a very complicated process. The 
manner in which the furrows develop is shown in the studies of Timberlake 
(1902) on Hydrodictyon, D. B. Swingle (1903) and Moreau (1913) on 
Rhizopus and Phycomyces, Davis (1903) on Saprolegnia, Rytz (1907) 
on Synchytrium, and Harper (1899, 1900, 1914) on Synchytrium, Pilobolus, 
Sporodinia, Fuligo, and Didymium. In Rhizopus (Fig. 63, A) the 
cleavage furrows begin to form both at the peripheral membrane of the 
sporangium and at the columella and work gradually into the multi- 
nucleate protoplasm, eventually cutting out multinucleate blocks which 
become the spores. In Phycomyces (Fig. 63, B) small vacuoles appear in 
the midst of the multinucleate protoplasm, enlarge and become stellate, 
and cut out spore masses with from 1 to 12 nuclei 
each. In the myxomycete, Fuligo, the cleavage 
is from the surface inward, and the multinucleate 
blocks are subdivided by further furrowing into 
uninucleate spores. In Didymium the spores are 
delimited in a similar way by furrows which 
begin to form along the young capillitium fila- 
ments in the interior of the multinucleate mass 
as well as at its periphery. 

Microsporocytes. In the microsporocytes of 
the higher plants it has been shown with great 
clearness by Farr (1916, 1918) that the quadri- 
partition to form spore tetrads of the tetrahedral 
type is brought about by furrowing, previous ac- 
counts having generally stated that the walls 
are formed by the cell plate method. Farr finds 
that after the four microspore nuclei are formed 
they all become connected by a series of six 
spindles, or sets of connecting fibers. The two 
spindles of the second maturation mitosis may 
persist, four new ones being added, or the two 
may disappear, six new ones being developed. 
Although some sporadic thickenings may ap- 
pear on these fibers they have nothing to do with the formation of the 
separating walls, there being no centrifugally growing cell plates such as 
are seen in cells dividing by the cell plate method. Constriction fur- 
rows appear at the periphery of the cell (Fig. 64) and grow inward until 
they meet at the center, dividing the protoplast simultaneously into four 

FIG. 64. Cytokinesis by 
furrowing in the micro- 
sporocyte of Nicotiana. 
X 1400. (After Farr, 1916.) 


spores. Any fibers which these furrows encounter as they grow inward 
are probably incorporated in the new wall, but they play no prominent 
part in wall formation: the development of the furrows appears to be 
entirely independent of the fibers present. 

In his first paper (1916) Farr states that the microspore tetrads of 
the bilateral type are usually formed by the cell plate method, a wall 
being formed across the diameter of the microsporocyte on the connecting 
fibers after the first maturation mitosis, and the two daughter cells 
being divided in a similar way after the second mitosis. In his second 
contribution (1918) he shows that in Magnolia such tetrads also are 
formed by furrowing. 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 toward the center and forms a wall across the 
diameter of the spherical protoplast. At the same time other new 
furrows subdivide each hemisphere, so that four uninucleate microspores 
result. Farr states that no case of bipartition by furrowing is known in 
the higher plants; bipartition begins in Magnolia, but the furrow ceases to 
grow until other furrows are formed after the second mitosis, the eventual 
division occurring by quadripartition. In the lower plants, however, 
bilateral tetrads may be formed by the cell plate method. It is the opinion 
of Farr that furrowing in microsporocytes is due to conditions similar to 
those which bring it about in animal eggs (see below), since both float 
freely in a liquid. 

Animals. In animals there is found nothing corresponding to the 
formation of a cell plate on the spindle fibers and its development into a 
thick wall such as is seen in plants. As noted in the section on the 
achromatic figure, there is often a slight differentiation at this region 
(the "mid-body"), but it has nothing to do with cytokinesis, which is 
brought about by simple constriction or furrowing. This process is 
most easily followed in the segmenting egg. In small eggs, such as those 
of worms, the daughter cells (blastomeres) round up and become more or 
less spherical, whereas in larger eggs, such as that of the frog, a cleavage 
furrow appears at one pole and develops through the egg without altering 
the shape of the latter, so that the first two blastomeres have the form of 
hemispheres. It is with animal eggs that most of "the researches on the 
mechanism of cytokinesis by furrowing have been carried out. 

Mechanism of Furrowing. Attempts to explain furrowing and the 
separation of the daughter cells on physico-chemical grounds have been 
rather numerous. Many years ago Biitschli (1876) advanced the view 
that as a result of a specific activity on the part of the centrosomes cyto- 
plasmic currents are set up which flow toward the centrosomes and 
produce a higher surface tension at the equator of the cell, this in turn 
bringing about furrowing and cell-division. McClendon (1910, 1913) 
also reported an increase in surface tension at the region of furrowing. 


On the contrary, Robertson (1911, 1913) and others attribute furrowing 
rather to a decrease in the equatorial surface tension, this decrease being 
due to a diffusion of materials toward that region from the daughter 
nuclei. Evidence favoring Rutschli's interpretation has been afforded 
by the studies of Spek (1918). 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 relatively higher surface 
tension at the equatorial region could be made to bring about the con- 
striction and fission of the droplet. In both droplet and dividing egg 
he found streamings such as Erlangen (1897) had described in the nema- 
tode egg: an axial movement polewards to the regions of low surface 
tension and a superficial streaming toward the equatorial region of higher 
surface tension, the streams turning inward at the furrow (Fig. 65). 

FIG. 65. Diagram showing streaming and furrowing in the egg of Rhabditis 
(A) und an oil droplet (B). (After Spek, 1918.) 

Although the causes of the initial changes in surface tension in the case 
of the cell are relatively obscure, these experiments of Spek show beyond 
question that alteration in surface tension and streaming are very im- 
portant factors in cell-division of this type. 

The relation of periodic changes in the viscosity of the egg substance 
to cytokinesis by furrowing has recently been discussed by Chambers 
(1919). Immediately after the entrance of the spermatozoon into the 
echinoderm egg the sperm aster begins to differentiate as a semi-solid 
region near the sperm head. (See p. 279.) When the aster is most fully 
developed the egg has its maximum viscosity (Heilbrunn 1915). As 
the aster disappears the egg again becomes more fluid. Then a second 
solidification begins at two centers forming the amphiaster, or bipqjar 
figure. The growth of these two semi-solid masses results in the elonga- 
tion of the egg, and eventually in the development of a cleavage furrow 
in the more fluid portion of the egg substance separating them. After 
cleavage is complete the semi-solid masses (asters) revert to a more fluid 
state. The formation of the cleavage furrow, moreover, may be pre- 
vented by mechanical means. At the second mitosis in eggs so treated 
(binucleate eggs) there are four centers of semi-solidification rather than 
two, and the egg cleaves simultaneously into four blastomeres. An egg 
cut into two pieces during the amphiaster stage will, provided it does not 


return to the fluid state, continue to cleave along the normal plane 
through the equator of the cell as if nothing unusual had happened. All 
of these observations indicate a close dependence of cytokinesis upon the 
temporary differentiation of semi-solid masses in the egg cytoplasm, and 
throw much light upon the question of the true nature of the achromatic 


Probably the most striking difference which meets the eye in a com- 
parison of animal and plant tissues lies in the relative degree of dis- 
tinctness with which the limits of the individual cells may be made out. 
Animal cells as a rule are separated only by very thin limiting 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. 

The Primary Wall Layer. Since the time when mitotic cell-division 
was first carefully studied with the aid of modern methods it has been 
known that in the cell wall of plants the primary layer, or middle lamella 
(the "intercellular substance " and "cement" of early writers), is formed 
in most cases in close connection with the spindle fibers at the close of 
mitosis. 1 The exact manner of its origin, however, has proved to be a 
very difficult point to determine, and has formed the subject of a long 
continued controversy. (See papers of Timberlake and Allen, 1900 
and 1901.) During the telophases of mitosis the spindle fibers con- 
necting the two daughter nuclei develop thickenings (Fig. 58, D), enlarge 
until they come in contact with one another and fuse to form a cell plate, 
or partition, between the daughter cells. For some time it was thought 
(Strasburger 1875, 1882, 1884) that the cell plate so formed became at 
once the middle lamella, upon which secondary and frequently tertiary 
layers were subsequently deposited by the protoplasts on either side. 
Strasburger here found support for his theory that the cell wall is essen- 
tially a transformed layer of the protoplast, in opposition to Nageli and 
von Mohl, who regarded it as primarily a secretion product. As a 
result of further researches, however, he later (1898) abandoned this 
view and adopted an interpretation that had been suggested by Treub 
(1878), namely, that the cell plate formed by the consolidation of the 
swellings ("microsomes") on the spindle fibers very soon splits to form 
the plasma membranes of the two daughter cells, and that there is then 
secreted between these membranes by the protoplasts a substance 
which becomes the primary layer, or middle lamella. The correctness 
of this view was confirmed by the careful researches of Timberlake 
(1900) and Allen (1901). Timberlake pointed out that in the micro- 

1 Discussion is here limited to the walls of higher plant tissues. The ectoplast of 
naked cells has been dealt with in Chapter III. 


sporocytes of Larix and the root cells of Allium the connecting Qbers 
first thicken near the nuclei, then become uniform throughout their 
length, and finally become swollen at the equatorial region, indicating a 
transfer toward that region of the material that is to compose the cell 
plate. Allen was able to show not only that the middle lamella itself 
may increase in thickness by the addition of new material before the 
secondary layers begin to be laid down, but also 
that it consists in reality of two layers representing 
the secretions contributed by the two daughter 
protoplasts. Where these two masses of secreted 
material meet there is developed a median plane of 
weakness which is ordinarily invisible but along 
which the lamella invariably splits when inter- 
cellular spaces are developed by the rounding up 
of the cells. By the use of proper staining methods 
it has been found possible to differentiate this 
u primary cleavage plane." The continuity of the 
middle lamella is interrupted, if at all, only by 
the fine pores through which pass the protoplasmic 
strands connecting adjacent cells. (See p. 46.) 

Secondary and Tertiary Wall Layers (Fig. 66). 
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 ap- 
parently certain exceptions. The secondary layer, 
which seems to be formed with considerable 
rapidity, differs from the primary layer not only 
chemically (see below) but also in structure, being 
interrupted by 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 lamella extending 
across the pit being termed the closing membrane. 
The central portion of this membrane sometimes 
(vascular cells of gynmosperms chiefly) has 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 meshwork (Fig. 67), while extreme cases are known in which it is 
held in place only by a few strands. In bordered pits (Fig. 68) the second- 
ary wall overarches the margins of the closing membrane. In this type 
of pit, characteristic chiefly of water-conducting cells of the gymnosperms, 
the closing membrane is of such a nature that its position in the center of 

FIG. 66. Longitudinal 
and transverse sections 
of a gymnosperm tra- 
cheid; p, primary wall 
or middle lamella; s, 
secondary layer; t, spiral 
tertiary thickening. 



the pit is readily altered. Probably because of ch^iges 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 latter may even be forced tightly into the pit 

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 
protoxylern cells, in which the secondary layer is deposited in the form of 
rings and spirals (Fig. 4). This form of thickening, together with the 

FIG. 67. FIG. 68. 

FIG. 67. Pits in the wood of Larix, showing perforations in pit membrane. X 800. 
(After Bailey.) 

FIG. 68. Diagram of bordered pit of coniferous wood. 

A, section of pit showing closing membrane supporting the torus, and secondary layers 
on each side of middle lamella. B, face view of same. C, section showing torus forced 
against mouth of pit. (After Bailey.) 

peculiarly extensible character of their primary walls, allows for 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 angio- 
sperms, a tertiary layer is deposited upon the secondary wall. This ter- 
tiary layer takes the form of slender spirals, rings, and other figures 
resembling the secondary thickenings of protoxylern cells. 

The Physical Nature of the Cell Wall. Hugo von Mohl (1853, 1858) 
first expressed the idea that the cell wall grows by apposition, i.e., by the 
deposition of material in successive laminae. Although certain other 
workers (Wigand 1856) supported this view, it became over-shadowed for 
a time by the theory of Nageli. This investigator, as a result of his classic 
researches on the wall and on starch grains (1858, 1862, 1863), concluded 


that the wall is made up of ultramicroscopic crystalline micellae sur- 
rounded by water fihns. Growth of the wall in thickness and in area he 
believed to be due to the intercalation of new micellae between the old ones, 
a process termed intussusception. Contrasted with this was Strasburger's 
development of the apposition theory (1882, 1889). Although Stras- 
burger agreed that the wall had both solid and liquid constituents, he 
held that the latter were not complex micellae, but only molecules linked 
together in the form of a reticular framework by their chemical affinities. 
Growth in area he thought was merely a matter of stretching without the 
intercalation of additional particles, while increase in thickness was 
supposed to be accomplished by apposition, or the deposition of layers 
of new material in the form of small particles, or microsomes. The 
striations which both he and von Mohl observed in the wall substance 
were regarded by Strasburger as due to the linear arrangement of these 

That the cell wall is not merely a lifeless secretion of the protoplast, 
but contains protoplasm in some form, is a view which has often been 
upheld, and involves problems which are still far from being solved. 
Prominence was given to the view by Wiesner (1886), who looked upon 
the growing cell membrane as a living part of the cell. Following Stras- 
burger's early view, he held the primary layer to be wholly protoplasmic, 
and supposed the growing wall to be made up of regularly arranged 
particles, which he called dermatosomes f connected by fine fibrils of 
protoplasm. Growth was accomplished by the intussusception of new 
dermatosomes. Evidence in support of Wiesner's interpretation was 
brought forward by Molisch (1888), who showed that when tyloses come 
into contact pits are formed exactly opposite each other in the two 
abutting walls, a phenomenon which it would be difficult to explain were 
the walls without living substance. 

The new intussusception theory of Wiesner was accepted by a number 
of workers including Haberlandt and Zacharias (1891). The apposition, 
or lamination, theory of Strasburger also had many supporters, among 
them being Noll (1887), Klebs (1886), Zimmermann (1887), and Askenasy 
(1890). According to Pfeffer (1892) both processes, the intussusception 
of new particles or molecules and the apposition of new material in layers, 
are concerned in the development of the wall. This view was later 
adopted by Strasburger (1898), and has received general acceptance. 
But much work must be done before any final conclusion can be drawn re- 
garding many points. Especially obscure is the exact relationship of 
the protoplasm and the wall. The solution of this difficult problem 
must await the results of further inquiries by both the cytologist and the 

The Chemical Nature of the Cell Wall. Through^the researches of 
Payen (1842), Fr&ny (1859), Kabsch (1863), Wiesner (1864, 1878), and 



particularly Mangin (1888-1893) it has been found that the chief constitu- 
ents of the newly formed cell walls of plants are pectose and cellulose 
that the primary wall or middle lamella consists of pectose, the secondary 
layer of pectose and cellulose, and the tertiary layer of cellulose. These 
substances however, rarely exist in the wall in pure and unmodified form. 
The pectose of the primary layer changes later to insoluble pectates, 
especially the pectate of calcium, while the secondary and tertiary layers 
very soon become greatly changed in composition, not alone through the 
addition of a variety of new substances, but also through an actual trans- 
formation which in some cases appears to be complete. For example, the 
secondary and tertiary layers of xylem cells, although at first containing 
much cellulose, may later become so completely transformed into or re- 
placed by lignin that they show no reaction whatever to cellulose stains. 
In some cases the primary wall may undergo a certain amount of lignifi- 
cation also. The walls of many cells become heavily impregnated with 
cutin or suberin, the latter substance being responsible for the peculiar 
character of corky tissues. Infiltration by cutin, or "cutiriization," is 
to be distinguished from "cuticularization," by which is meant the secre- 
tion of a layer of cutin (cuticle) on the outside of the cell. A variety of 
mineral substances, such as silica, calcium oxalate, and calcium carbonate, 
as well as more complex organic compounds, such as tannin, oils, and 
resins, are often deposited in the walls of old cells. The heartwoods 
of trees owe their qualities largely to the presence of these additional 

In spite of these modifications, however, it is still true that cellulose 
is the substance chiefly characteristic of plant cell walls in general. Al- 
though cellulose has been identified in certain animals, the membranes of 
practically all animal cells are composed of other substances, such as 
keratin, elastin, gelatin, and chitin. In the fungi also the r61e of cellulose 
appears to be played in part by chitin. 

The Walls of Spores. Special attention has been given to the develop- 
ment of the elaborate walls, or coats, of the spores of various plants in a 
number of investigations. Strasburger (1882, 1889, 1898, 1907) con- 
cluded that such coats arise by two general methods: (1) by the growth in 
thickness (by apposition) of the original wall of the spore cell through the 
activity of the protoplast, as in the pollen grains of Malva and other angio- 
sperms, and (2) by a deposition of material upon the original wall by the 
t apetal fluid in which the young spores lie, as in the case of the megaspore 
of Marsilia. 

The highly specialized coats of the megaspore of Selaginella have been 
most intensively studied, particularly by Fitting (1900, 1906) and Miss 
Lyon (1905), whose accounts disagree in several points. At the close of 
the tetrad division there is formed about each young spore a thick gela- 
tinous "special wall/' at the inner surface of which, according to Fitting f 


the spore coats begin to differentiate. The exospore first appears, and 
just outside of it the rough perispore soon begins to develop. Then a 
second layer, the mesospore, is formed within the exospore. Between the 
protoplast, which is at this time very small, and the mesospore, and 
Between the exospore and the mesospore, there are developed two cavities 
filled with a sporangial fluid which furnishes material to the growing 
coats. Emphasis is placed on the fact that the coats are able to increase 
in thickness while they have no immediate contact with the protoplast. 
The protoplast now expands, after which a third coat, the endospore, is 
formed at its surface. The mature spore thus has three coats according 
to Fitting's interpretation, which Denke (1902) and Campbell (1902) 

e x. &m, e n. 

FKJ. 69. The developing megnspore coat of Sclagindla rupestris: 
p, protoplast with nucleus; en, endospore; s.m., undifferentiated portion of "spore 
membrane;" ex, exospore: the outer denser portion is the "perimum." (After Lyon, 1905.) 

Miss Lyon found that the spore coats (S. rupestris) begin to differ- 
entiate in the midst of the "spore membrane" ("special wall:" Fitting), 
rather than at its inner surface as Fitting thought. The exospore 
first appears as a double zone, the outer part of which becomes the per- 
inium (perispore: Fitting) (Fig. 69). The small protoplast gradually 
expands and pushes back the undifferentiated inner portion of the spore 
membrane; and while it does so a second coat is formed at its surface 
and becomes the endospore (mesospore: Fitting) which increases in thick- 
ness by lamination. In another species (S. emiliana) the exospore and 
endospore form simultaneously. Miss Lyon thus finds two coats rather 


than three, but points out that a portion of the spore membrane which 
may remain in an undifferentiated condition until a late stage may easily 
be mistaken for a third coat. The two " spaces " in the immature spore 
wall she holds to be undifferentiated regions in the spore membrane, and 
not cavities filled with a foreign fluid; and further urges that the proto- 
plast is at all times in contact with the gelatinous spore membrane in 
which the coats are differentiating, opposing the view that the latter 
have the power of independent growth in thickness. 

Evidence favoring the view that the spore coats can grow while not 
in contact with the protoplast has been brought forward by Beer (1905, 
1911) and Tischler (1908). Beer asserts that although both the primary 
wall and the secondary thickening layer of the pollen grain (in certain 
members of the Onagracese) originate in intimate connection with the 
plasma membrane, most of their subsequent growth occurs by intussus- 
ception while they are completely separated from the protoplast, which 
secretes the material used. The development of the pollen wall in 
Ipomoea purpurea has been described in great detail by Beer. Around 
each young spore immediately after its formation there appears a tem- 
porary gelatinous " special wall/' upon the inner surface of which the 
protoplast deposits the exine, or outer spore coat. This is at first homo- 
geneous, but soon differentiates into a thin outer lamella and an inner 
zone made up of a network of thickenings with the rudiments of spines 
at its nodes. Both the spines and the small rodlets, which develop in a 
clear space appearing between the outer lamella and the network of 
thickenings (mesospore), undergo most of their development after they 
are separated from the protoplast. Tischler (1908) reports that the 
exine of the pollen of sterile Mirabilis hybrids may continue to increase 
in thickness after the protoplast begins to degenerate. 

As an example of the formation of spore coats through the activity 
of a tapetal plasmodium may be taken the case of Equisetum, described 
by Beer (1909) and Hannig (1911). The spores of this form have three 
coats: an endospore, an exospore, and a perispore consisting of several 
layers including the one which splits to form the "elaters." The young 
spore cell at first has a simple membrane, the rudiment of the exospore. 
The walls of the tapetal cells dissolve, allowing the cell contents to flow 
freely among the spores as a tapetal plasmodium. Upon the spore 
membrane the plasmodium deposits successively (1) an inner gelatinous 
layer, (2) the "middle coat/ 1 (3) an outer gelatinous layer, and (4) the 
elater layer. The exospore develops from the original membrane after the 
middle coat is formed, and the endospore, or innermost coat, is developed 
last of all. 

From this brief review, to which other examples might be added, it is 
evident that spore coats may develop in a variety of ways, but too little 
is known to warrant any statement as to which method may be the most 


general one. Although cytological interest centers chiefly in other 
problems, further studies on spore coats would not only contribute to 
our understanding of cell wall formation, but would also aid in solving the 
problem of the possible existence of protoplasm in the wall. 

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nebst allgemeinen Bemerkungen liber Centrosomen und Verwandtes. Verh. 

Phys.-Med. Ges. Wurzburg, N. F. 29. 
BUTSCHLI, O. 1876. Studien iiber die ersten Entwicklungsvorgange der Eizelle, die 

Zelltheilung, und die Kunjugation der Infusorien. Senckenb. Naturforsch. 

Ges. 10. 
CALKINS, G. N. 1898. Mitosis in Noctiluca miliaris and its bearing on the nuclear 

relations of the Protozoa and Metazoa. Jour. Morph. 15: 711-770. pis. 40-42. 
CAMPBELL, D. H. 1902. Studies in the gametophyte of Selaginella. Ann. Bot. 16: 

419-428. pi. 19. 
CHAMBERS, R. 1917. Microdissection Studies. II. The Cell aster. A reversible 

gelation phenomenon. Jour. Exp. Zool. 23: 483-504. 
1919. Changes of protoplasmic permeability and their relation to cell division. 

Jour. Gen. Physiol. 2 : 49-68. figs. 14. 
CONKLIN, E. G. 1902. Karyokinesis and cytokinesis in the maturation, fertilization 

and cleavage of Crepidula and other Gasteropoda. Jour. Acad. Nat. Sci. Phila. 

12:5-121. pis. 1-6. figs. 33. 
DAVIS, B. M. Oogenesis in Saprolegnia. Bot. Gaz. 35 : 233-249, 320-349. pis. 9, 

DENKE, P. 1902. Sporenentwicklung bei Selaginella. Beih. Bot. Centr. 12: 182- 

199. pi. 5. 


DEVISED R. 1914. Le fuseau dans les microsporocytes du Larix. (Note prelim.) 

Comptes. Rend. Acad. Sci. Paris 158: 1028-1030. 
DRtfNER, L. 1894. Zur Morphologic der Centralspindel. Jen. Zeitschr. 28: 469- 

1895. Studien tiber den Mechanismus der Zelltheilung. Ibid. 29: 271-344. 

pis. 4-8. 

VON ERLANGEN, R. 1897. Beobachtungen liber die Befruchtung und ersten Teil- 
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FARR ; C. H. 1916. Cytokinesis of the pollen-mother-cells of certain Dicotyledons 

Mem. N. Y. Bot. Gard. 6: 253-317. pis. 27-29. 
1918. Cell-division by furrowing in Magnolia. Am. Jour. Bot. 6: 379-395. 

pis. 30-32. 
FAULL, J. H. 1912. The cytology of Laboulbenia chcetophora and L. Gyrinidarum. 

Ann. Bot. 26: 325-355. pis. 37-40. 

FITTING, H. 1900. Bau und Entwicklungsgeschichte der Makrosporen von Isoetes 
und Selaginella und ihre Bedeutung fur die Kenntniss des Wachsthums pflanz- 
lichen Zeilenmembranen. Bot. Zeit. 68 1 :107-164. pis. 5, 6. 
1906. (Review of paper by Lyon, 1905). Ibid. 64: 42-43. 
FLEMMING, W. 1891. Neue Beitrage zur Kenntniss der Zelle. II. Arch. Mikr. 

Anat. 37: 685-751. pis. 38-40. 
FR^MY, E. 1859a. Recherches chimiques sur la composition des cellules ve"ge* tales. 

Comptes Rend. Acad. Sci. Paris 48: 202-212. 
18596. Recherches chimiqies sur la cuticle. Ibid. 667-673. 
1859c. Recherches sur la composition chimique du bois. Ibid. 862-868. 
GALLARDO, A. 1896a. La carioquinesis. Ann. Soc. Cientif. Argentina 42. 
1896&. Essai d 'interpretation des figures karyokine*tiques. Ann. Mus. Nac. d. 

Buenos Aires. 
1901. Les croisments des radiations polaires et Pinterprdtation dynamique des 

figures de karyokinese. Soc. de Biol. 63. 
1906. L'interpr6tation bipolaire de la division karyokine*tique. Ann. Mus. Nac. 

d. Buenos Aires 13 : 259. 
1909. La division de la cellule ph6nomene bipolaire de caractere e*lectro-colloidal. 

Arch. Entw. 28: 125-154. Figs. 9. 

HANNIG, E. 1911. Ueber die Bedeutung der Periplasmodien. I. Die Bildung des 
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HARPER, R. A. 1899. Cell division in sporangia and asci. Ann. Bot. 13: 467-525. 

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1900. Cell and nuclear division in Fuligo varians. Bot. Gaz. 30 : 217-251. pi. 14. 
1914. Cleavage in Didymium melanospermum (Pers.) Macbr. Am. Jour. Bot. 1: 

127-144. pis. 11, 12. 

HARTOG, M. 1905. The dual force of the dividing cell. I. The achromatic spindle 
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1914. The true mechanism of mitosis. Arch. Entw. 40: 33-64. figs. 16. 
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HERMANN, J. 1891. Beitrage zur Lehre von der Entstehung der karyokinetischen 

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J6RGEN8EN, M. 1913. Zellenstudien, II. Die Ei- und Nahrzellen von Piscicola. 
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KABSCH, W. 1863. Untersuchungen iiber die chemische Beschaffenheit der Pflan- 
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LAWSON, A. A. 1898. Some observations on the development of the karyokinetic 
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1900. Origin of the cones of the multipolar spindle in Gladiolus. Bot. Gaz. 30: 

145-153. pi. 12. 

1903. Studies in spindle formation. Ibid. 36: 81-100. pis. 15, 16. 
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LILLIE, R. S. 1903. On differences in the direction of the electrical connection of 

certain free cells and nuclei. Am. Jour. Physiol. 8: 273-283. 
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401-430. pl&. 22, 23. 

LYON, F. 1905. The spore coats of Seiaginella. Bot. Gaz. 40 : 285-295. pis. 10, 1 1. 
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1889. Sur la.presence des composers pectiques dans les v6ge" taux. Ibid. 109 : 579. 
1890a, Sur la substance intercellulaire. Ibid. 110 : 295. 
18906. Sur les r6actifs colorants des substances fondamentales de la membrane. 

Ibid. Ill: 120. 

1891. Observations sur la membrane cellulosique. Ibid. 113: 1069. 
1893. Sur 1'emploi du rouge de ruthenium en anatomic ve"g6tale. Ibid. 116. 653. 
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19106. On the dynamics of cell-division. II. Changes in permeability in develop- 
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division. Arch. Entw. 37: 233-247. figs. 10. 

MEEK, C. F. U. 1913. The problem of mitosis. Quar. Jour. Micr. Sci. 58 : 567-592. 
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VON MOHL, H. 1853. Ueber die Zusammensetzung der Zellmembran aus Fasern. 

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1858. Die Untersuchungen des Pflanzengewebes mit Htiife des polarisierten 

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MOLISCH, H. 1888. Zur Kenntniss der Thyllen, nebst Beobachtungen uber Wund- 
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MORGAN, T. H. 1899. The action of salt solutions on the unfertilized and fertilized 
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RABL, C. 1889. Ueber Zellteilung. Anat. Anz. 4: 21-30. figs. 2. 
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1897. Stemmen die Strahlen der Astrosphare oder ziehen sie? Ibid. 4: 659-730. 
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1898. Die Mechanik der Zelldurchschnurung nach M eves' und nach meiner 
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1899. Furchung des Ctenophoreneies nach Ziegler und deren Mechanik: usw. 
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1903. Mechanische Erklarung der Aehlichkeit zwischen magnetischen Kraftlinien- 

system und Zellteilungsfiguren. Ibid. 16 : 476-535. figs. 36. 
ROBERTSON, T. B. 1909. Note on the chemical mechanics of cell-division. Arch. 

Entw. 27:29-34. 
1911. Further remarks onjthe chemical mechanics of cell-division. Ibid. 32 : 308- 

1913. Further explanatory remarks concerning the chemical mechanics of cell 

division. Ibid. 36 : 692-707. figs. 3. 
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19186. Die amoboiden Bewegungen und Stromungen in den Eizellen einiger 
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STRASBURGER, E. 1875. Ueber Zellbildung und Zelltheilung. Jena. 
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1888. Ueber Kern- und Zellteilung im Pflanzenreich, nebst einem Anhang tiber 
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1889. Ueber das Wachstum vegetabilischer Zellhaute. Ibid. 2. 


1892. Schwarmsporen, Gameten, pflanzliche Spermatozoiden und das Wesen der 
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1897. Ueber Cytoplasmastrukturen, Kern- und Zellteilung. Jahrb. Wiss. Bot. 
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1898. Die pflanzlichen Zellhaute. Ibid. 31: 534-598. pis. 15, 16. 
1907. Apogamie bei Marsilia. Flora 97: 123-191. pis. 3-8. 

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11 50: 442-453. 
1886. Untersuchungen uber die Organization der vegetabilischen Zellhaut. Ibid. 

193:17-80. figs. 5. 
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some other animals. Jour. Morph. 16 : Suppl. 1-23. 

1900. The Cell in Development and Inheritance. 

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ZACHARIAS, E. 1888. Ueber Kern und Zellteilung. Bot. Zeit. 46: 33-40, 51-62. 

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pis. 16, 17. 
ZIMMERMANN, A. 1887. Die Pflanzenzelle. 

1893. Sammel-Referate. 6. Beih. Bot. Centr. 3: 342-354 


In accordance with the well established principle which states that 
only through the simpler organisms can an adequate understanding of 
those higher in the scale of complexity be approached, search has been 
made for primitive modes of nuclear division with the hope that light 
may thereby be thrown upon the origin and significance of the elaborate 
karyokinetic process which is so universally found in the cells of higher 
animals and plants. It is to be acknowledged that such a phylogenetic 
explanation of mitosis is very far from being reached, but many of the 
observations recorded are nevertheless of a very suggestive nature. To 
botanists the most interesting of these have been made upon the Cyano- 
phycese, which have long been a subject of controversy in this connection. 

Cyanophycese. For many years the nature of the " central body" 
of the cells of such blue-green algse as Oscillatoria remained very obscure. 
Butschli (1890), Dangeard (1892), Scott (1888), and others believed it 
to be a nucleus of a somewhat primitive type, whereas other investigators, 
among them Zacharias (1892) and Chodat (1894), denied its nuclear 
nature. Zukal (1892) held that the peripheral portion of the cell repre- 
sents a chromatophore, the central body consisting of cytoplasm with a 
number of minute nuclei imbedded in it. 

One of the first critical accounts based partly on the study of sections 
was that of Fischer in 1897. Fischer concluded that the central body, 
in which he found no chromatin, is the main portion of the cytoplasm, 
and not to be regarded as the forerunner of the nucleus or indeed as an 
independent organ at all. He also investigated the nature of the periph- 
eral portion of the protoplast. By treating the plants with 10 per 
cent hydrofluoric acid he dissolved away the other parts of the cell, leav- 
ing this portion intact; and as the result of comparative studies on other 
plants he concluded, in harmony with Zukal, that it is a single large 

Since Fischer's work the most important contributions are those of 
Hegler, Kohl, Olive, Phillips, Gardner, and Miss Acton. Contrary to 
the view of Fischer, all of these cytologists interpret the central body 
as a nucleus, and the first three regard its division as essentially mitotic. 
The opinions of these workers with respect to the organization of the cell 
of the Cyanophyeese and the behavior of its nucleus are summarized 




According to Hegler (1901) the nucleus contains granules of chromatin 
but no nucleolus or nuclear membrane, division occurring by a simple 
form of mitosis. The coloring matter exists in the form of minute 
granules or cyanoplasts. Two other kinds of bodies are also present: 
albuminous slime globules and albuminous crystals (cyanophycin granules) 
representing reserve food. 

Kohl's (1904) description of the cell of Tolypothrix (Fig. 70) is one of 
the most detailed which has been given in this group of researches. Kohl 
shows that the nucleus of this form has extensions reaching outward 

FIG. 70. Structure and division of the cell of Tolypothrix lanata. 
A, cell in the vegetative state: c, cytoplasm; n, nucleus; /, fat droplets; p, phycocyanin 
and chlorophyll granules; s, slime globules; g, granules of cyanophycin. B, four stages of 
cell-division in Tolypothrix, showing transverse division of chromosomes. C, diagram 
showing 6 stages of cell-division. (After Kohl, 1903.) 

toward the cell wall, and that they are withdrawn at the time of nuclear 
division. The nucleus, which contains chromatin, also includes a num- 
ber of large Zentralkorner, or slime globules, while in the cytoplasm are 
fat droplets, cyanophycin granules of reserve albumen, and granules of 
chlorophyll and phycocyanin. The nucleus, which is very rarely in the 
resting state, divides as follows: the chromatic material forms a spireme 
which segments into a definite number of chromosomes; these lie in the 
direction of the long axis of the cell 'and break transversely as the separat- 
ing wall grows inward from the periphery. Their halves are thus in- 
cluded in the two daughter cells, where they form daughter nuclei without 



FIG. 71. Nuclear division 
in Oscillatoria Froelichia. 1, 2, 
3, 4, four successive stages. 
(After Olive, 1904.)j 

Olive (1904) * finds that the nucleus of Oscillatoria (Fig. 71) consists 
of a fibrous achromatic framework with a number of very small chroma- 
tin granules, and is nearly always in some stage of division. A spireme 
is formed carrying 16 chromatin granules (8 in Glceocapsa and 32 in one 
species of Oscillatoria), each representing a chromosome. The spireme 
and its chromatin granules are split longitudinally, and the daughter 
spiremes with the daughter granules separate, a distinct central spindle 
extending between them. The dividing wall is formed as a centripetally 

growing partition. In Glceocapsa the cell di- 
vides by simple constriction. The vegetative 
nuclei of Oscillatoria very rarely approach 
the resting condition, but in spores and 
heterocysts they soon pass into this state, a 
nuclear membrane and vacuole being de- 
veloped. In the heterocyst the protoplast 
disorganizes. Olive regards the central body 
of the Cyanophycese as not essentially different 
from the nucleus of the higher plants, although 
it is relatively primitive in several features. 
In the cytoplasm he finds both cyanophycin 
granules and slime globules, but no cyano- 
plasts, the coloring matters being diffused in the peripheral portion 
of the protoplast. 

Fischer (1905), in reply to the claims of Kohl and Olive, reasserted 
his view that the central body is not a nucleus, but rather an accumulation 
of carbohydrate materials. The glycogen formed as a result of assimila- 
tory activity gathers in the central body where it is transformed into 
another carbohydrate, anabcenin, which assumes the form of sausage- 
shaped structures. At the time of cell-division these masses of reserve 
material are distributed by a process of " pseudomitosis " to the daughter 
cells. Fischer therefore regards the mitotic figures observed by others 
as significant in connection with nutrition rather than with the functions 
usually attributed to nuclei. 

Gardner (1906), investigating a number of species, found nuclei of 
three kinds, which he called the diffuse type, the net karyosome type, 
and the primitive mitosis type respectively. The "diffuse type" of 
nucleus, which has no very definite delimitation from the peripheral 
portion of the protoplast, contains an indefinite number of chromatin 
masses. As the cell divides this central aggregation of chromatic material 
divides into approximately equal portions. In the "net karyosome" 
type, found in Dermocarpa, the distinction between the nucleus and the 
surrounding cytoplasm is much clearer. The nucleus has an achromatic 

1 A very convenient tabulation of the results of researches on cell structure in the 
Cyanophycese up to 1904 is given by Olive. 



network with chromatin granules at its nodes, and constricts simultane- 
ously into a large number of daughter nuclei which pass to the conidia. 
In Synochocystis aquatilis occurs the "primitive mitosis " type: here 
Gardner found the only case of anything approaching mitotic behavior. 
A spireme develops and segments into three pieces which arrange them- 
selves parallel to the long axis of the cell and divide transversely; the 
daughter pieces then separate and a centripetally growing cell wall 
completes the division of the cell. Gardner thus finds in the Cyano- 
phycese "a series of nuclear structures, beginning with a very simple 



FIG. 72. The nuclei of various members of the Chroococcace. 
A, cell of Chroococcus turgidus with scattered metachromatin granules (m) and plasma- 
tic microsomes (p) ; division beginning. X 2500. /?, cell of Gloeocapsa with chromatic 
granules. C, Merismopedia elegans, showing two stages of nuclear division. X 1500. 
D. Chroococcus macrococcus: n, nucleus; m, metachromatin; v, vacuole. X 2500. E, 
dividing nucleus of Chroococcus macrococcus. X 2500. (After Acton, 1914.) 

form of nucleus scarcely differentiated from the surrounding cytoplasm 
and dividing by simple direct division" and passing "by very gradual 
steps to a highly differentiated form of nucleus which in dividing shows 
a primitive type of mitosis, and in structure approximates the nucleus of 
the Chlorophycese and the higher plants." 

In a more recent investigation of the Chroococcaceae Miss Acton 
(1914) finds that the nucleus is in general much simpler than that of the 
higher plants. Like Gardner, however, she points out a series beginning 
with a form in which definite organization is almost entirely lacking and 
ending with one in which the structure of the higher plant nucleus is 
closely approached (Fig. 72). In Chroococcus turgidus the protoplast is 

206 rpTrrnprrrrnrr 

made up of a ground substance with a reticulum bearing bodies of two 
sorts: granules of metachromatin closely similar to chromatin in reaction, 
and cyanophycin granules, or plasmatic microsomes. Although there is 
no definitely delimited central region in the cell the metachromatin is 
found mostly at the center and the cyanophycin mostly nearer the pe- 
riphery. When the metachromatin granules become numerous division 
sets in, a centripetally growing wall cleaving the protoplast into two 
daughter cells. In Gl&ocapsa the central region is somewhat more definite 
and may often show a spireme-like appearance such as Olive describes; 
but this may possibly be an artifact. In Merismopedia elegans there is a 
definitely delimited nucleus, not like that of the higher plants but merely 
an accumulation of chromatin or chromatin-like material which divides 
just before the cell constricts into two portions. In Chroococcus macro- 
coccus, finally, the nucleus and cytoplasm are sharply distinct, the former 
having a reticulum with chromatin granules at its nodes and dividing 
by a sort of constriction at the time of cell-division. 

As a result of these observations Miss Acton advances a theory of the 
evolution of nucleus and cytoplasm, which is briefly as follows. The 
excess food elaborated by the protoplast with its pigments was first 
stored as plasmatic microsomes composed of a carbohydrate, cyanophy- 
cin. As the reserve material became more complex in nature the nucleo- 
protein metachromatin was elaborated; this became aggregated at the 
center of the cell, insuring its equal distribution in cell-division, as in 
Merismopedia. There thus arose in the cell a physiological and mor- 
phological differentiation, the nucleo-protein with its portion of the 
supporting reticulum becoming a stable nucleus, as in Chroococcus 
macrococcus, and the ground substance remaining as the cytoplasm. 

Summary. In the Cyanophycese, therefore, although these forms in 
all probability had nothing directly to do with the evolution of the higher 
plants, we see a series of stages such as may well have occurred in the 
evolution of the nucleus and its complicated mitotic division. In the 
simplest forms the material concerned with those cell activities which 
in higher organisms are associated with the nucleus, is scattered through- 
out the cell without the morphological distinctness characteristic of an 
organ in the strict sense. It is passively distributed to the daughter 
cells when the cleavage wall is formed at the time of cell-division. In 
other cases this material reacts more strongly like true chromatin and 
may form a more or less definite aggregation separating into two masses 
as the cell divides. This metachromatin, which is a nucleic acid com- 
pound, has also been observed in other algae, in Protozoa, and in fungi, 
including the yeasts. It appears to represent a reserve material, though 
it may also have other functions. Finally, definite and well organized 
nuclei are present in certain of the forms described in the foregoing 
pages, and although these nuclei may lack some of the features exhibited 


The two kinds of chromatin now separate, ^Jife^tik^oclmiirffittn placing 
itself in the center and the generative or idiochroin^rtnlying like a thin 
equatorial plate around it." As the nucleus' elongates the tropho- 
chromatin body becomes dumbbell-shaped and breaks into two, while 
the idiochromatin plate splits^into daughter plates which apparently 
move to the poles and cooperate with the trophochromatin in the forma- 
tion of the daughter nuclei. 

FIG. 74. 

A, two stages of mitosis in Sorodiscus. (After Winge, 1912.) B, anaphase of nuclear 
division in Euglena. Chromosomes grouped about dividing "nucleolo-centrosomo." 
(After Keuten, 1895.) C, chromosomes developing from nucleolus in Spirogyra. X 1335. 
(After Berghs, 1906.) D, Mitosis in Spirogyra crassa. (After Merriman, 1913.) 

A process with much the same appearance at certain stages is seen in 
the flagellate, Euglena (Keuten 1895) (Fig. 74, B). Here the chromo- 
somes group themselves about the large nucleolus which soon takes the 
form of a dumbbell-shaped " central spindle " or "centrodesmose." 
The nucleolus completes its division, the chromosomes meanwhile 
separating into two groups which pass to the poles and reorganize the 
daughter nuclei. In certain other flagellates Kofoid (1915) reports a 
split spireme and a definite number of chromosomes which differ markedly 
in size and shape. 

In Cladophora (Carter 1919) nearly all the chromatin is contained in 
one or more large chromatin nucleoli, or karyosomes. After the numer- 
ous chromosomes have arrived at the two poles at the close of the ana- 
phase the spindle connecting the two groups constricts and completes 
the division of the nucleus. 

Another unusual condition is found in Spirogyra (Fig. 74, C, D). 
In this form nearly all of the chromatic material is lodged in the large 
nucleolus, the nuclear reticulum being very delicate and almost invisible 
in many preparations. According to Berghs (1906), Karsten (1908), 
and Trondle (1912) all the chromosomes wliich appear in the prophase 
and split as usual are derived from this nucleolus, most of its material 



being used in their formation. In the opinion of Miss Merriman(1913) 
the chromatic bodies observed by the above workers are not true chromo- 
somes, but are rather more indefinite chromatic aggregations which are 
variable in number and appearance, and which are irregularly pulled 
apart as mitosis proceeds. She finds here "no evidence throughout the 
karyokinesis of an equational division of autonomous bodies." 

In Zygnema both Escoyez (1907) and van Wisselingh (1914) find that 
the reticulum, and not the nucleolus, gives rise to all the- chromosomes. 
Although the nucleolus furnishes no morphological element, chromatic 
material may flow from it to the chromosomes as they develop from the 
reticulum. Much the same condition is found in Marsilia (Strasburger 
1907; Berghs 1909). Strasburger points out that in the somatic nuclei 
(in the cells of the root and the young prothallium) most of the chromatic 
substance is held in the nucleolus during the resting stages (Fig. 17, E), 
and that the material of the reticular framework, which is very delicate, 
is to be regarded as the substance of importance in heredity. Berghs 
shows that the nucleolus consists of an achromatic substratum which 
appears independently of the reticulum in the telophase and soon becomes 
impregnated with chromatic material transferred to it from the chromo- 
somes. In the next prophase the chromatic material flows back to the 
delicate reticulum, from which the chromosomes gradually develop. As 
the chromosomes increase in distinctness the nucleolus becomes paler, 
and when the nuclear membrane breaks down the nucleolus dissolves in 
the protoplasmic liquid. It is therefore clear that in Marsilia the nu- 
cleolus is not a mere aggregation of the chromosomes of the telophase, as 
might at first be supposed. The chromosomes arise from the reticulum 
as usual, and not from the nucleolus as reported for Spirogyra. In these 
observations we have additional evidence favoring the view of Haecker, 
Boveri, Marshal, and others (see Chapter VIII) that it is the achromatic 
substratum of the chromosome, and not the chromatic substance which 
it carries, that should be regarded as the persistent structural unity 
representing the basis of inheritance. 

Amitosis. In amitotic or direct nuclear division the nucleus simply 
constricts and separates into two portions while in the "resting" condi- 
tion, no condensed chromosomes, centrosomes, spindle, or asters being 
formed. As a general rule such a division of the nucleus is not followed 
by a division of the cell; cells with two or more nuclei therefore commonly 
result. As examples may be cited the tapetal cells in the anthers of 
angiosperms, the internodal cells of Chara (Fig. 75) (Johow 1881), and 
certain glandular cells of animals. The presence of more than one 
nucleus cannot by itself be regarded as evidence that amitosis has 
occurred, however. Amitosis appears to be of rather frequent occurrence 
among the lower organisms, some of which show other methods of divi- 
sion also. For example, amitosis occurs regularly in budding yeasts, 



though the divisions giving rise to the ascospore nuclei have been shown 
to be mitotic in certain cases. (See Guilliermond 1920.) Amitosis 
was once believed to be the normal mode of nuclear division, mitosis 
being looked upon as very exceptional. The true condition, so far as 
higher organisms are concerned, has turned out to be quite the reverse: 
it is evident that amitosis occurs frequently in certain kinds of cells, but 
the mitotic method of division has been found to be 
almost universal. 

What the physiological significance of amitosis 
may be is not well known. It was once suggested 
(Chun 1890) that it aids the processes of metabolism 
by increasing the nuclear surface in the cell, since 
it is of such frequent occurrence in cells with a dis- 
tinctively nutritive function. This view has recently 
been restated by Nakahara (1917) as a result of his 
work on the larva of Pieris. 1 The most generally held 
opinion regarding amitosis in the higher organisms 
was for many years that expressed by Flemming 
(1891), namely, that it represents a degeneration 
phenomenon or aberration of some kind, which would 
explain why it is so often found in degenerating and 
pathological tissues. In the words of vom Rath 
(1891), "when once a cell has undergone amitotic 
division it has received its death-warrant; it may indeed continue to 
divide for a time by amitosis, but inevitably perishes in the end." 

That the view of vom Rath must be modified has been indicated by 
the results of a number of investigations. For instance, Pfeffer (1899) 
and Nathansohn (1900) found that if Spirogyra filaments are placed in a 
% to 1 per cent solution of ether the nuclei divide by amitosis only, and 
that when the filaments are returned to pure water the mitotic method 
of division is resumed, with no evidence of degeneration. Haecker, how- 
ever, working on the eggs of Cyclops, came to view such artificially in- 
duced behavior not as true amitosis but rather as a much modified 
mitotic division, which he termed "pseudoamitosis." Other cytologists 
observed nuclear divisions that seemed intermediate in character between 
mitosis and amitosis (Dixon in the endosperm of Fritillaria, 1895; Sargant 
in the embryo sac of Lilium, 1896; R. Hertwig in Actinosphcerium, 1898; 
Buscalioni in the endosperm of Corydalis, 1898; and Wasielewski in the 
roots of Vicia faba, 1902, 1903). Hertwig accordingly concluded that 
mitosis and amitosis are separated by no sharp boundary line, but are 
connected by an unbroken series of transition stages. 

1 In a second paper (1918) Nakahara gives a convenient review of the literature 
of the subject. 

FIG. 75. Amitosis 
in internodal cell of 
Chara. X 413. 



As a result of his recent researches on chloralized cells (Fig. 76) 
Sakamura (1920) interprets all such unusual types of nuclear division as 
those described by Hertwig and Wasielewski as the effect of disturbed 
mitotic division, but denies the claim of those authors that such types 
of division represent actual transition stages between amitosis and 
mitosis. True amitosis he regards as a fundamentally different process, 
and as essentially a degeneration phenomenon. 

FIG. 76. Abnormal mitosis in chloralized root cells of Vicia. 

A, chromosomes distributed irregularly in cell. B, scattered chromosomes beginning to 
assume nuclear form. C, nucleus reconstructed by scattered chromosomes. D, scattered 
chromosomes reconstructing 3 separate nuclei. E, chromosomes reconstructing 2 nuclei 
connected by bridge. F, amitosis-like appearance resulting from condition shown in E. 
(After Sakamura, 1920.) 

On the contrary, Des Cilleuls (1914) reports that in the rabbit 
periods of amitosis and mitosis succeed each other regularly in the same 
cell lineage without affecting the vitality of the cells. In his opinion, 
therefore, amitosis does not necessarily place the stigma of senescence 
upon the cell. A similar conclusion is reached by Arber (1914), who finds 
amitosis supplementing mitosis in the early growth stages of the leaves 
and adventitious roots of Stratiotes aloides; and by McLean (1914), who 
asserts that it is the sole method of nuclear division in the cortical 
parenchyma of several aquatic angiosperms. Saguchi (1917) likewise 
states that the nuclei in the ciliated cells of vertebrates divide by amitosis 

Amitosis and Heredity. One of the most important theoretical ques- 
tions raised by the phenomenon of amitosis is that of the effect which 
the process may have upon the hereditary mechanism of the cell. Ac- 
cording to the chromosome theory of heredity and development in its 
usual form it has been thought that, although amitosis may occur in 
connection with an altered metabolism in cells not to undergo further 
differentiation, mitosis must occur exclusively in the gerjn cell lineage, 
in order that the chromosomes and the hereditary elements they con- 


tain shall be properly distributed to the reproductive cells; and also in 
developing tissues and organs, so that differentiation may proceed nor- 
mally. On the other hand, several workers (Meves; Flemming in his 
later papers) admit that amitosis may not affect any hereditary powers 
which the nuclei concerned may possess. Child (1907, 1911), who re- 
ports amitosis in both the somatic and germ cells of certain animals, 
where it appears to play an important role in the developmental cycle, 
strongly urges that such facts render the hypothesis of chromosome in- 
dividuality highly improbable, and that our conceptions of the r&le of 
the cell organs in heredity must be greatly altered. 

The hopelessly unsettled state of opinion on this question may be 
illustrated by the list of authors and their views cited by Conklin (1917). 
That amitosis frequently occurs in the process of normal cell differ- 
entiation, and therefore constitutes evidence against the chromosome 
theory, has been held by Nathansohn (1900), Wasielewski (1902, 1903), 
Gurwitsch (1905), Hargitt (1904, 1911), Child (1907, 1911), Patterson 
(1908), Glaser (1908), Jordan (1908), Jorgensen (1908), Maximow (1908), 
Moroff (1909), Knoche (1910), Nowikoff (1910), and Foot and Strobell 
(1911). Several of these investigators, together with R. Hertwig (1898), 
Lang (1901), Calkins (1901), Herbst (1909), Godlewski (1909), and 
Konopacki (1911), see no principal distinction between amitosis and 
mitosis, believing that both may occur without interfering with normal 

Haecker (1900), Nemec (1903), and Schiller (1909) dissented from the 
above view, which was also strongly contested by Boveri (1907) and 
Strasburger (1908). Richards (1909, 1911) and Harman (1913) failed to 
confirm the results of Child on amitosis in cestodes, but Child (1911) 
reasserted his view, which was supported by Young (1913). Schurhoff 
(1919), working on Podocarpus, emphatically states that a nucleus which 
has once undergone true amitosis is incapable of dividing mitotically. 
Sakamura (1920) is of the same opinion. 

In a careful study of maturation and cleavage in Crepidula plana 
Conklin (1917) finds that the nuclei divide only by mitosis. There are 
many apparent cases of amitosis, but upon careful examination they all 
prove to be only various modifications of the regular mitotic process. 
Such modifications are these : the scattering of the chromosomes and their 
failure to unite into a single nucleus; mitosis without cytokinesis, giving 
cells with two or more nuclei; the failure of certain daughter chromosomes 
to pull apart, leaving a chromatic bridge between the daughter nuclei; 
the persistence of the nuclear membrane, with a division of the chromo- 
somes by mitosis and of the nuclear vesicle by constriction. Conklin 
concludes as a result of his many observations and an examination of 
the evidence offered by others, that there is not known a single conclusive 
case of true amitosis in a normally differentiating cell, and that all attacks 


upon the chromosome theory on the ground of amitosis have signally 
failed. The results obtained by Sakamura (1920) in his study of modi- 
fied mitosis in chloral ized plant cells are strikingly similar to those of 
Conklin, and his conclusions regarding the chromosome theory are es- 
sentially the same. 

From the foregoing it is evident that the problem of the effect of 
amitosis upon the differentiation of the tissues in which it occurs and 
upon the hereditary powers of the nucleus is by no means easy of solution, 
and that much care must be used in interpreting supposed amitotic phe- 
nomena in fixed preparations. The work of Conklin and Sakamura has 
shown clearly that many of the phenomena reported as amitosis. are in 
reality aberrations of the mitotic process, and that the opinions of many 
writers are undoubtedly due to a failure to recognize this fact. Should it 
be proved, however, that true amitosis may occur in the lineage of 
normally functioning germ cells a serious obstacle would be placed in the 
way of the chromosome theory of inheritance in its current form, for this 
theory requires that, no matter what happens in cells not in the direct line 
of the germ cells, nuclear division in this line must be exclusively mitotic 
in order that the hereditary mechanism in the nucleus shall be preserved. 
This mechanism, as we shall see in later chapters, is supposed to be of 
such a nature that amitosis would seriously derange its organization. 
In each daughter nucleus of an amitotic division some of the elements 
necessary for normal functional activity would presumably be lacking, 
owing to the simple mass division of the chromatin. With reference to 
this point it has been contended by Child that the nucleus is a dynamic 
system capable of regenerating its lost parts and "producing a whole " 
after amitosis. But it is a well established fact that when chromosomes 
are lost in abnormal mitotic division they arc not regenerated by the 
daughter nuclei (non-disjunction; Chapter XVII). 

In this connection an experiment performed by Chambers (1917) is 
of interest. This investigator succeeded in pinching the nucleus of an 
animal egg into two pieces. The two "amitotic" nuclei so produced 
reunited upon touching, after which the egg was fertilized and passed 
through the early cleavage stages in the normal manner. It is known 
that the character of these early stages is largely independent of the 
nuclei present, being the outgrowth of an organization already present 
in the egg cytoplasm. (See Chapter XIV.) The later stages, in which 
the effects of the hereditary constitution of the nucleus appear, were not 
reached in the present experiment. Moreover, the entire chromatin 
outfit was present in the reunited nucleus, which is not supposed to be 
true of a daughter nucleus of an amitotic division. From this experiment, 
therefore, it can only be concluded that whatever disturbance of the 
spatial arrangement of the nuclear elements may have .been caused by 
the temporary separation of the nucleus into two parts, it had no serious 


effect on the nutritive functions performed by the nucleus during the 
early cleavage stages. Development did not proceed far enough to 
warrant any conclusion regarding the effect upon the r61e of the nucleus 
in differentiation and inheritance. 

Although what probably represents amitosis has been observed in 
young germ cells, it has not been shown with certainty in any case that 
descendants of these amitotically dividing nuclei become the nuclei of 
normally functioning gametes. To gain conclusive evidence for such an 
occurrence it would be necessary to trace the descendants of the amitotic- 
ally dividing nuclei through to particular gametes or spores and then to 
note the effect upon the individuals produced by them. This would be a 
matter of extreme experimental difficulty, and not at all possible in 
most organisms. If it were successfully accomplished and the individuals 
were found to be normal in every respect, not only in the cleavage stages 
but throughout development, the revision of the chromosome theory 
which various workers have advised would at once become necessary. 

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Roy. Soc. London 72: 401-408. figs. 3. 
VON WASIELEWSKI, W., 1902, 1903. Theoretische u. Experimentelle Beitrage zur 

Kenntniss der Amitose, I, II. Jahrb. W. Bot. 38: 377-420, pi. 7; 39: 581, 60& 

figs. 10. 
WINQE, 0. 1912. Cytological studies in the Plasmodiophoraceae. Arkiv. for 

Botanik 12: 1-39. pis. 3. 
VAN WISSELINGH, C., 1914. On the nucleolus and karyokinesis in Zygnema. Rec. 

Trav. Bot. Neer. 11: 1-13. 
YOUNG, R. T. 1913. The histogenesis of the reproductive organs of Tcenia pisifor- 

mis. Zool. Jahrb. 35: 355-418. pis. 18-21. 
ZACHARIAS, E. 1887. Beitrage zur Kenntniss des Zellkerns und der Sexualzellen. 

Bot. Zeit. 46 : 297-304. pi. 4. * 

1890; Ueber die Zellen der Cyanophyceen. Ibid. 48: 1-. pi. 1. 
1892. Ueber die Zellen der Cyanophyceen. Ibid. 50: 617-624. 
1903. Jahrb. Hamb. Wiss. Anst. 21. 

1907. Ueber die neuere Cyanophyceen-Literatur. Bot. Zeit. 65 : 264-287. 
ZUKAL, H. 1892. Ueber den Zellinhalt der Schizophyten. (Vorl. Mitt.) Ber. 

Deu. Bot. Ges. 10: 51-55. 


The subject of chromosome reduction is one of the most important to 
be met with in the study of cytology. Many of the problems, both theo- 
retical and practical, upon which biological investigators are expending 
their most intense efforts seem to be bound up directly or indirectly with 
the reduction of the chromosomes. The essential feature of reduction is 
relatively simple in nature, and must be thoroughly grasped in order that 
the discussions in the following chapters may be intelligible. The entire 
process by which reduction is accomplished, on the other hand, is very 
complicated and extremely difficult to observe and interpret with any 
degree of confidence. In spite of the enormous amount of work already 
done there still exists much difference of opinion regarding some of the 
significant steps in the series of changes undergone by the miclear material. 
In the present chapter a number of these opinions will be reviewed, but 
our main purpose will be to make clear the fundamental feature of chro- 
mosome reduction. 

We have seen that all the cells of the body in a given species are char- 
acterized by the presence of a certain number of chromosomes in their 
nuclei, and that this number is held constant throughout development by 
an equational division of every chromosome at every somatic mitosis. 
When we speak of "reduction" we ordinarily refer to the fact that at a 
certain stage in the life history of the organism the number of chromosomes 
is reduced one-half. This mere change in the number of chromosomes, 
though very important, is not in itself the essential feature of the reducing 
process, as will be seen further on. The whole number is restored at the 
time of fertilization, when two nuclei, each with the reduced number, 
unite. In all organisms reproducing sexually reduction and fertilization 
thus represent the two most critical stages in the life cycle so far as the 
chromosomes are concerned; hence the exhaustive researches on these two 

Discovery. The discovery of reduction was made by van Beneden, 
who in 1883 announced that the nuclei of the egg and spermatozoon of 
Ascaris each contain one-half the number of chromosomes found in the 
body cells. Although van Beneden and other early workers believed that 
the change in number was brought about by the simple casting out of half 
the chromosomes during the growth of the germ cells, it was soon shown 
that this view was incorrect, and that "reduction is effected by a rearrange- 



ment and redistribution of the nuclear substance without loss of any of its 
essential constituents " (Wilson 1900, p. 233). 

In plants the discovery of reduction came somewhat later. Stras- 
burger in 1888 showed that in angiosperms the number of chromosomes in 
the egg and male nuclei is fixed by a reduction occurring in the mother- 
cells of the embryo sac and pollen respectively. This was at once con- 
firmed by Guignard (1889, 1891). E. Overton (1893) found that the 
female gametophyte cells in the cycad, Ceratozamia, have half the number 
of chromosomes found in the cells of the sporophyte. He further sug- 
gested that reduction probably occurs in the sporocytes in mosses and ferns. 
In the liverwort, Pallavicinia, Farmer (1894) found the gametophyte cells 
to have four chromosomes and the sporophyte cells eight. That Overton's 
theory of a reduction in the sporocytes of bryophytes and pteridophytes 
was correct was demonstrated by Strasburger (1894), who postulated 
the occurrence of a periodic reduction of the chromosomes in all organ- 
isms reproducing sexually. 

The Stage in the Life Cycle at which Reduction Occurs. The reduc- 
tion of the chromosomes is accomplished during the course of two nuclear 
divisions which, since in animals they have to do with the maturing of the 
gametes, early came to be known as the maturation divisions. Because 
of its peculiar character the first of these divisions was termed the hetero- 
typic by Flemming (1887), while the second, which is essentially like a 
somatic division, was called the homceotypic (sometimes written homo- 
typic). Although the essential act of reduction usually occurs at the first 
division, the entire process, to which the name meiosis has been applied, 
is of such a nature that the second division is normally necessary for its 
completion. As a result of the two divisions the " reduced " nuclei or cells 
are formed in groups of four, or tetrads, though all members of a tetrad may 
not function. The point in the life cycle at which these divisions take 
place in various organisms will now be noted. 

In animals, almost without exception, reduction occurs at gameto- 
genesis (Fig. 77). In the male those cells (spermatogonia) in the testes 
whose ultimate descendants are to become spermatozoa multiply by 
divisions of the ordinary equational type until a certain number are 
produced. These cells, now called primary spermatocytes, enlarge a little 
and quickly undergo two successive divisions: the first division in each 
is heterotypic and results in two cells called secondary spermatocytes; the 
second is homoeotypic and divides the two secondary spermatocytes into 
four spermatids, each of which becomes transformed into a spermatozoon. 
The four spermatozoa are therefore the immediate result of the two 
maturation divisions. In the female the situation is somewhat different: 
here nearly all of the differentiation of the gamete is accomplished before 
the nuclear divisions bringing about reduction actually occur. The 
primary odcytes (ovocytes) are the descendants of a number of generations 



of oogonia (ovogonia). The oocyte, usually while its nucleus is in the 
prophases of the first maturation division, enlarges greatly ("growth 
period ")> becomes filled with stored food, and develops the general fea-. 
tures characterizing the egg. The oocyte is now called the " ovarian egg,"i 
and it actually is an egg in all respects save one of much importance: its! 
nucleus still has the full number of chromosomes. At a comparatively 
late stage, in many cases even after the spermatozoon has entered the egg 
at fertilization, the oocyte nucleus (germinal vesicle), having passed 
through some of the prophasic changes characteristic of the heterotypic 



FIG. 77. Diagram showing the history of the chromosomes in the ordinary 
life cyclers of animals and plants. 

mitosis before and during the growth period, gives rise to a mitotic figure 
which is often surprisingly small for the volume of the nucleus. The 
spindle takes up a position perpendicular to the surface of the cell, and at 
telophase the chromosomes passing to the outer pole are included in the 
first polar body, a small cell budded off at this point. (See Fig. 106.) A 
second spindle is rapidly formed about the chromosomes remaining in 
the egg (called at this stage the secondary oocyte) and the second matura- 
tion mitosis occurs, one daughter nucleus being included in the second 
polar body. In the course of these two divisions chromosome reduction 
is accomplished. The first polar body may divide to form two, thus 
completing the tetrad of cells corresponding to the tetrad of spermatozoa 
in the male. Although the polar bodies are normally f unctionless they are 


generally looked upon as eggs historically: the maturation divisions 
probably resulted formerly in a tetrad of eggs, whereas now only one 
relatively large and highly differentiated egg is produced at the expense 
of the other three cells, which remain small and functionless. 

Among the protozoa (see Minchin 1912) it has been found that in 
those forms which appear to have their chromatin aggregated into no 
definite number of chromosomes, there often occur two successive nuclear 
divisions suggestive in certain respects of maturation divisions, a part of 
the products then degenerating. Some have regarded this as a " casting 
out of effete vegetative chromatin/' an interpretation which was at one 
time placed upon the maturation process generally. In many cases this 
" reduction" of the chromatin occurs immediately prior to syngamy 
(sexual union), 1 and so agrees with reduction in higher forms in taking 
place at gametogenesis; but in other cases it immediately follows syngamy, 
as in certain algae mentioned below. Other protozoa have been shown to 
have a definite chromosome number which is regularly reduced in a man- 
ner essentially comparable to that in the metazoa. 

In plants it is among the members of the lower groups (thallophytes) 
that a striking diversity is shown in the stage of the life cycle at which 
reduction takes place : in the groups above the thallophytes it is regularly 
accomplished at sporogenesis. In the myxomycete, Ceratiomyxa, it 
has been shown by Olive (1907) and Jahn (1908) that spore formation is 
accompanied by a chromosome reduction. In the green algae it is in the 
first two divisions of the zygote (either a zygospore or a fertilized egg) 
that reduction occurs: this has been definitely established in Spirogyra 
(Karsten 1908; Trondle 1911), Zygnema (Kurssanow 1911), Coleochcete 
(Allen 1905c), and Chara (Oelkers 1916). In a number of other forms, 
such as Ulothrix, (Edogonium, Sphceroplea, and Closterium, in which the 
chromosomes are not well known, it is probable that the same condition 
holds, since the zygote upon germination gives rise with considerable 
regularity to four cells; in some cases ((Edogonium) these four cells are 

In the BROWN ALG^B Cutleria (Yamanouchi 1912), Zanardinia (Yama- 
nouchi), and Ectocarpus (Kylin 1918a) reduction occurs in connection 
with zoospore formation. In Fucus, however, an exceptional condition 
is found: here reduction takes place in the antheridium and oogonium 
initials, in the first two divisions following the one delimiting the stalk 
cell (Fig. 78, JS). Since there are only three divisions in the oogonium, 
which thus produces eight eggs, the eggs are but one division removed 
from the four products of the maturation mitoses, a condition closely 
approaching that in animals. That reduction in Fucus is associated 
with gametogenesis was inferred by Strasburger (1897) and Farmer and 
Williams (1898) and demonstrated by Yamanouchi (1909). 

1 See the cases of Actinophrys sol and Amoeba albida, Chapter XII. 



In the BED ALG^E reduction occurs in the two divisions differentiating 
the nuclei of the tetraspores when the latter are present in the life history. 
Such is the case in Polysiphonia (Yamanouchi 1906) (Fig. 78, A), Gri- 
ffithsia (Lewis 1909), and Corallina (Yamanouchi). The brown algse 
Dictyota (Williams 1904) and Padina (Wolfe 1918) also conform to this 
scheme. In Nemalion, which has no tetraspores, it was long supposed 
(Wolfe 1904) that reduction occurs in connection with carpospore forma- 
tion, but Cleland (1919) has recently shown that 
it takes place at the time the zygote germinates, as 
in so many green algse. 1 

In the ASCOMYCETES reduction occurs in the 
course of the first two of the three mitoses initiated 
by the primary ascus nucleus (Figs. 22, 61) and re- 
sulting in the eight ascospore nuclei. It was for a 
long time generally thought that there were two 
nuclear fusions in the life history one in the archicarp 
and one in the ascus (see p. 290), and the three di- 
visions in the ascus were accordingly regarded as a 
process whose function was to reduce the " quadri- 
valent" chromosomes to the univalent condition 
(Harper 1905; Overton 1906). Such a double reduc- 
tion was described by Miss Fraser (1907, 1908) for 
Humaria rutilans: the first mitosis she found to be 
heterotypic, the second homceotypic, and the third 
"brachymeiotic," the last bringing about a further 
reduction by the separation of the chromosomes heterotypic division 
into two smaller groups. This was also reported S Poij/sTpTonTa. 
for Otidea aurantia and Peziza vesiculosa (Fraser and (After Yamanouchi, 
Welsford 1908), Lachnea stercorea, Ascobolus furfura- O f heterotjrpi^nStosls 
ceus, and Humaria granulata (Fraser and Brooks 1909), in oogonium of Fucus. 
and HctoeZfampa(Carruthers 1911). Harper (1900, [&'" Yamanouchi > 
1905), although he thought two fusions occurred, found 
no double reduction, holding rather that the fusion of the two ascus 
nuclei and their chromsomes is so complete as to render the quadrivalent 
character of the latter entirely invisible. Other investigators also find 
no double reduction in the ascus. They show rather that the first two 
mitoses correspond to the heterotypic and homceotypic mitoses of other 
organisms, and that the third division is purely vegetative or equational 
in character. As instances may be cited the work of Faull (1905, 1912) 

1 For a review of sexual reproduction and alternation of generations in the algae 
see Bonnet (1914). Davis (1916) gives a convenient summary of the life histories 
of the red algse. Dodge (1914) summarizes and compares the life histories of red 
algse and ascomycetes. See Atkinson (1915) for a complete review of researches on 
ascomycetes. For the cytology of the yeasts see Guilliermond 1920, 

FIG. 78. 
A, prophase of 



on Hydnobolites, Neotiella, and Laboulbenia, and that of Claussen (1912) 
on Pyronema. Furthermore, it is becoming increasingly apparent (see p. 
291) that there is but one fusion in the life cycle that in the ascus, so 
that the necessity for a second reduction is removed. 

In the BASIDIOMYCETES it has been shown by the researches of Juel 
(1898), Maire (1905), Guilliermond (1910), Kniep (1911, 1913), Levine 
(1913), and others on the hymenomycetes, and by those of V. H. Black- 
man (1904), Dietel (1911), Fitzpatrick (1918), and others on the rusts, 1 
that reduction occurs in the two mitoses giving rise to the four basidio- 

FIG. 79. Sexual fusion and maturation divisions in the basidium of 

Nidularia pisiformis. 

a, two sexual nuclei about to unite. b, prophase of heterotypic division in fusion 
nucleus, c, heterotypic mitosis, d, homceotypic mitosis, e, the four basidiospore 
nuclei. X 1800. (After Fries, 1911.) 

spore nuclei (Fig. 79). As in the ascomycetes, it thus follows immediately 
upon the nuclear fusion: in the basidium in hymenomycetes and in the 
teleutospore in rusts. An exception is reported in the case of Hygro- 
phorus conicus, in which Fries (1911) finds in the basidium neither a 
nuclear fusion nor a reduction. 

In the BRYOPHYTES reduction, so far as known, is universally brought 
about by the two mitoses which differentiate the four nuclei of each spore 
tetrad. It was at one time reported (van Leeuwen-Reijnvaan 1907) 
that in Polytrichum there is a second reduction at spermatogenesis and 
oogenesis: the sporophyte was said to have 12 chromosomes, the spore 
and gametophyte six, and the gametes three. This double reduction 
was thought to be compensated for by the fusion of the ventral canal 
cell with the egg, raising the number in the latter to six, in combination 
with the entrance of two sperms into the egg at fertilization, making the 
sporophytic number 12. This interpretation has been shown to be 
false by both Vandendries (1913) and Walker (1913), who find the life 
cycle normal in every respect: a reduction from 12 to 6 occurs at sporo- 
genesis but no second reduction follows at gametogenesis. 

1 A summary of researches on rusts is given by Maire (1911). 
nuclei in the cells of basidiomycetes is given by Levine (1913). 

A list of numbers of 



In VASCULAR PLANTS reduction in all normal life cycles in both homo- 
sporous and heterosporous forms occurs uniformly in the divisions differ- 
entiating the spore tetrads (Fig. 77). .The sporocytes, particularly the 
microsporocytes ("pollen mother-cells "), of the higher plants have long 
been favorite objects for the study of reduction. Since the gametophyte 
generation in the higher plants is so abbreviated, reduction closely pre- 
cedes fertilization in these forms. In the ordinary angiosperm embryo 
sac in which the eight nuclei are derived from a single megaspore of the 
tetrad, the egg nucleus is removed from the product of reduction (mega- 
spore nucleus) by only three mitoses. In some cases, of which Lilium 
is the best known example, walls fail to form be- 
tween the four megaspore nuclei (Fig. 80, J3), 
leaving them in a common cavity (embryo sac) 
where they undergo but one further division to 
produce the eight nuclei of the female gameto- 
phyte. The egg here is consequently removed 
from the product of reduction by a single 
mitosis. In one known case, Plumbagella 
(Dahlgren 1915), the foUr reduced nuclei, 
formed as in Lilium, divide no further, one of 
them functioning directly as the egg nucleus. 
Here, therefore, the condition characteristic of 
animals has been reached : the gamete nucleus is 
itself the direct product of reduction, and the 
haploid generation usually produced by the 
spore is eliminated. The male gametophyte 
also has undergone much abbreviation in higher 

plants, but the mal nucleus is still removed from the reduction product 
(microspore nucleus) by two mitoses. In no known case does the micro- 
spore nucleus function directly as a gamete nucleus. 

The term gonotokont was introduced by Lotsy (1904) to designate 
any cell, whatever its origin or position in the life cycle, in which the 
reduction process is initiated. In animals the gonotokonts are therefore 
the primary spermatocyte and the primary oocyte. In most green algse 
the gonotokont is the zygote; in the red algse it is usually the tetrasporo- 
cyte; in the ascomycetes it is the ascus; in the basidiomycetes it is the 
basidium; and in the bryophytes and vascular plants it is the sporocyte 
the microsporocyte and megasporocyte in the case of heterosporous forms. 

The Meaning of Reduction. In order that the true meaning of reduc- 
tion may be appreciated it will be necessary to indicate the main points 
of a theory first suggested by Roux (1883) and later developed particu- 
larly by Weismann (1887, 1891, 1892). It had been believed by the earlier 
workers that reduction was merely a process whose function was "to 
prevent a summation through fertilization of the nuclear mass and of 


FIG. 80 Megaspore 

tetrads in Angiosperms. 

A, tetrad of walled cells 

in Physostegia virginiana; 

formation of two upper 

ones just being completed. 

X462. (After Sharp, 1911.) 

B, tetrad of megaspore 

nuclei in Lilium canadense. 


the chromatic elements" (Hertwig 1890). But the chromatic mass is 
actually quartered at reduction, whereas the number of chromo'somes is 
halved. Moreover, great changes in nuclear volume occur with no 
change in the number of chromosomes. This careful guarding, so to 
speak, of the chromosome number was siezed upon as a most significant 
fact by Roux, who " argued that the facts of mitosis are only explicable 
under the assumption that the chromatin is not a homogeneous substance, 
but differs qualitatively in different regions of the nucleus; that the 
collection of the chromatin into a thread and its accurate division into 
two halves is meaningless unless the chromatin in different regions of the 
thread represents different qualities which are to be divided and dis- 
tributed to the daughter cells according to some definite law. He urged 
that if the chromatin were qualitatively the same throughout the nucleus, 
direct division would be as efficacious as indirect, and the complicated 
apparatus of mitosis would be superfluous." 1 Upon this conception 
Weismann based his remarkable theory, the starting point of which was 
"the hypothesis of De Vries that the chromatin is a congeries or colony of 
invisible self -propagating vital units or biophores, somewhat like Darwin's 
'gemmules/ each of which has the power of determining the development 
of a particular quality. Weismann conceives these units as aggregated 
to form units of a higher order known as 'determinants/ which in turn are 
grouped to form 'ids/ each of which ... is assumed to possess the 
complete architecture of the germ-plasm characteristic of the species. 
The 'ids' finally, which are identified with the visible chromatin-granules, 
are arranged in linear series to form 'idants' or chromosomes. It is 
assumed further that the 'ids' differ slightly in a manner corresponding 
with the individual variations of the species, each chromosome therefore 
being a particular group of slightly different germ-plasms and differing 
qualitatively from all the others. 

"We come now to the essence of Weismann's interpretation. 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 
chromosomes 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 having been 
divided into halves.' This form of division, which he called equal 
division (Aequationstheilung), was then a known fact. The second 
'This and the following quotations are from Wilson (1900, pp. 245-246). 


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 reducing division (Reduktionstheilung), and suggested 
that this might be effected either by a transverse division of the chromo- 
somes, or by the elimination of entire chromosomes without division. By 
either method the number of 'ids' would be reduced; and Weismann 
argued that such reducing divisions must be involved in the formation 
of the polar bodies, and in the parallel phenomena of spermatogenesis." 

Reduction in Weismann's sense, then, is a reduction of the number of 
kinds of germ-plasm or ancestral hereditary qualities present, this 
reduction being brought about by means of a redistribution, half of the 
qualities to one daughter nucleus and the remainder to the other daughter 
nucleus. The change in the number of chromosomes is a consequence of 
the manner in which this redistribution is accomplished, as we shall see. 

Interpretations Based on Weismann's Theory. As would be ex- 
pected, there were announced certain interpretations of chromosome be- 
havior based on Weismann's idea. Several cytologists thought that 
they found the chromsomes actually dividing transversely at one or the 
other of the two maturation mitoses. This interpretation, however, 
proved to be incorrect. Much light was thrown on the problem when 
Henking (1891), Rtickert (1891, etc.), Haecker (1890-9), vom Rath 
(1892-3), and others showed that the double chromosomes appearing in 
the reduced number on the spindle at the first maturation mitosis are not 
split chromosomes like those seen in somatic divisions, but are pairs of 
chromosomes, or bivalent chromosomes, each arising by an end-to-end 
conjugation (synapsis) of two somatic chromosomes. The two parts of 
each bivalent then separate at the first or second maturation division, 
the entire chromosomes thus being segregated into two groups, each 
with the reduced number. Thus it appeared unnecessary that a single 
chromosome, representing a linear series of different qualities, should be 
transversely divided in order for Weismannian reduction to occur: it 
was only necessary to assume that the whole chromosomes differ qualita- 
tively from one another, so that when the two members of a bivalent 
pair separate there would be a Segregation of different qualities. It is in 
the light of this bivalent chromosome conception that we are to interpret 
the many early reports of a transverse division of the chromosome during 
maturation. What was called a transverse division was merely the 
separation of two entire chromsomes placed end-to-end. 

A number of workers soon found that in many cases there is nothing 
even simulating a transverse division, either of single chromosomes or of 
bivalent pairs, but that both maturation divisions are apparently longi- 
tudinal (Flemming, Brauer 1893, Moore 1896, Meves 1896, Gr^goire, 
etc.). How, then, is there any Weismannian reduction if there is neither 



a transverse division of the chromosome nor a transverse separation of 
bivalents? Montgomery (1901), von Winiwarter (1900), Sutton (1902), 
Boveri (1904), and a number of others showed that here the chromo- 
somes conjugate side-by-side rather than end-to-end. Thus when they 
separate there is an appearance of a longitudinal division, but reduction 
is nevertheless accomplished, since entire somatic chromosomes suppos- 
edly qualitatively different, and not the longitudinal halves of split 
chromosomes, are separating. The appearance of a longitudinal division 
may also be present after an end-to-end conjugation, for the two members 
may bend around to a side-by-side position before finally separating. 


FIG. 81. Diagram showing essential difference between somatic and heterotypic 



As a matter of fact, the maturation divisions in nearly all cases, especially 
those studied by botanists, are both longitudinal in appearance. End- 
to-end conjugation later came to be called telosynapsis or m&tasynd&se, 
and side-by-side conjugation parasynapsis or parasyndese. 

Somatic and Heterotypic Mitoses Compared. Before taking up a 
more detailed account of the process of reduction as it has been described 
by various investigators it is of the utmost importance to fix clearly in 
mind the essential difference between somatic and heterotypic mitosis 
in order to realize what constitutes the cardinal feature of reduction, and 
thereby to detect the significant points of the various theories. This 
essential difference is illustrated in Figs. 81 and 82. In a somatic or 
vegetative mitosis every chromosome is split into two exactly similar longi- 
tudinal halves which are distributed to the two daughter nuclei. The daughter 
nuclei are therefore like each other and like the mother nucleus in the quality 



of their substance. In the heterotypic mitosis, the first of the two matura- 
tion mitoses, the chromosomes conjugate two by two during the prophase to 
form the reduced number of bivalent chromosomes, which take their place 
on the spindle. The members of each pair, which are supposed to differ 
qualitatively from each other, separate and pass to the two daughter nuclei. 
These nuclei are therefore qualitatively unlike each other, having different 
members of the full chromosome group; and also unlike the mother nucleus, 
since each of them has only half as many chromosomes as the latter. The 
second maturation mitosis (not shown in the diagrams) is essentially a 
vegetative mitosis in most cases: each chromosome splits longitudinally 


FIG. 82. Diagram showing essential difference between somatic and hetero- 
typic mitoses. 

and the halves arc distributed to the daughter nuclei. The four nuclei, 
and consequently the four cells, resulting from the two maturation divi- 
sions are therefore of two kinds: two of them have half of the chromosomes 
of the original nucleus and the other two have the remaining ones. 

Assuming, then, that the chromatin of the nucleus represents the 
principal physical basis of inheritance (see Chapter XIV), reduction is 
essentially this: a reduction in the number of kinds of hereditary units by 
the separation and distribution of qualitatively different masses of chromatin 
to different cells and eventually into different hereditary lines, rather than an 
equational division and distribution of all the qualities as in somatic mitosis. 
As has already been stated, the change in the number of chromosomes 
("numerical reduction ") is a consequence of the method by which this 
qualitative reduction is brought about, this method being the distribution 
of entire chromosomes, each representing one or more particular qualities, 
to different cells. 


Another important feature of the reduction process should be noted 
before proceeding further. In many cases, chiefly among animals, the 
chromosomes appearing on the spindle of the first maturation mitosis are 
not merely double, but quadruple. This is due to the fact that each of the 
conjugating chromosomes is already longitudinally split, giving the 
bivalent chromosome the form of a chromosome tetrad (not to be confused 
with tetrads of cells or nuclei). The four constituents of the chromosome 
tetrad are known as chromatids, and are distributed by the two matura- 
tion mitoses to the four resulting cells. It is thus seen that in the case of 
chromosome tetrads the lines of separation for both maturation mitoses 
are marked out in the prophase of the first. It should be borne in mind 
that one of these lines represents a plane of chromosome conjugation, 
and the other a plane of true longitudinal splitting. When the chroma- 
tids separate along the conjugation plane reduction occurs, whether this 
be at the first or second mitosis, and when separation along the plane of 
splitting occurs the mitosis is equational, as in somatic division. 

In all cytology there is scarcely a subject upon which there has been 
entertained so great a variety of opinion as upon the question of the 
exact behavior of the chromosomes during the meiotic phases. Entirely 
aside from the theoretical interpretations placed upon the process of 
maturation, cytologists have yet failed to arrive at any universally 
accepted conclusion regarding all the structural changes which occur. 
This diversity of opinion is due in part to the complexity of the process 
and the difficulty of interpreting its various stages, some of which fail 
to stand out clearly in preparations made by our available methods. 
On the other hand, a great variety of organisms have been studied, and 
these undoubtedly differ considerably in the details of the reduction 
process, so that agreement in all particulars is not to be expected. The 
attempt has too often been made to apply universally an interpretation 
founded upon a study of one or two organisms. Certain essential fea- 
tures of meiosis may be expected to show close agreement in all organisms 
reproducing sexually, as Strasburger pointed out, but it is evident that 
there is no full correspondence as regards, the exact manner in which the 
essential changes are accomplished. In the following pages are given 
brief descriptions of a few representative interpretations advanced by 
various cytologists. 1 

The two interpretations of reduction which have been most conspicu- 
ous in the literature of recent years are diagrammed in Figs. 83 and 89. 

1 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 maturation 
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 Gre*goire's two invaluable works (1905, 1910). A useful list of works on somatic 
and heterotypic mitosis in angiosperms is given by Picard (1913). 



Nearly all of the accounts of reduction now appearing, especially those 
given by botanists, conform in general to one or the other of these two 
schemes, though they vary greatly in detail. Both theories have been 
upheld by competent observers, and it may be possible that both modes 
of reduction actually occur; but the same objects have been so differently 
described by the two opposing schools that it seems very probable that 
interpretation is chiefly responsible for the persistent diversity of opinion. 
For convenience the two theories will be referred to as Scheme A and 
Scheme B. 


trie niT*i 

FIG. 83. The method of chromosome reduction according to Scheme A. 
Explanation in text. 

Scheme A. The first of the two main interpretations of reduction 
came into prominence in 1900 and shortly after, when von Winiwarter 
(1900), Gr^goire (1904, 1907, 1909), A. and K. E. Schreiner (1904-1908), 
and Berghs (1904, 1905) applied it to the phenomena observed by them 
in several animals and plants. Its essential points are as follows (Figs. 

At the beginning of the heterotypic prophase the nuclear reticulum, 
without breaking down into such distinct elementary nets or alveolar 
units as are seen in the somatic prophase, takes the form of long slender 
threads (leptotene or leptonema stage). 1 During the very early prophase 

1 The terms leplotene, synaptene, pachylene, and diplotene were proposed by von 
Winiwarter (1900); leptonema, zygotkne, pachynema, and strepsinema by Gre"goire 
(1907); amphitene by Janssens (1905); strepsitene by Dixon (1900); diakinesis by 
Haecker (1897); synapsis by Moore (1896); synizesis by McClung (1905); and meiosis 
by Farmer and Moore (1905). The terms ending in -t&ne are ordinarily used as 



these threads conjugate in pairs side-by-side (parasynaptically ; para- 
syndetically). The association does not take place at all regions of the 
threads at once: it begins at one or two points, commonly at one end, 

FIG. 84. Reduction in sporocyte of Nephrodium. 

A, leptonema. B t recovery from synizesis; parallel conjugation consummated during 
synizesis. C, pachynema. D, second contraction of bivalent spireme. E, diakinesis. 
F t anaphase of heterotypic mitosis. G, interkinesis. H, homoeotypic mitosis. /, two 
of the four spore cells. (After Yamanouchi, 1908.) 

and gradually involves all portions, so that at stages when the process is 
yet incomplete the two threads may be closely paired at some points and 
widely divergent at others, giving an appearance very unlike that of the 
halves of a longitudinally split chromosome in a somatic cell. This is 



known as the zygotene, zygonema, synaptene, or amphit&ne stage. Usually 
before the union is complete the nucleus enlarges somewhat and the 
threads contract, forming a tight knot at one side of the nucleus. This 
stage, formerly called synapsis (see p. 255), is now more properly known as 
synizesis. The pairing threads come into very close association during 
synizesis, which, though variable in time, usually ensues at about this 
stage. When the closely paired threads recover from the synizesis con- 
traction they extend more uniformly throughout the nucleus ("open 
spireme")> and are now seen to be much thicker (pachytene; pachynema). 
In many cases they may again contract into a 
loose knot with loops extending from it ("second 
contraction"). As they continue to decrease in 
length and increase in diameter the members of 
each pair twist more or less tightly about each 
other for a short time (strepsitene; strepsinema; 
diplotene). Eventually they become very short 
and thick, and the various pairs (gemini; 
bivalent chromosomes), present in the haploid 
or reduced number, lie scattered throughout 
the nucleus (diakinesis) . The two components 
of each geminus may now separate slightly at 
one or both ends or at the middle, which gives 
them the form of Ys, Vs, Xs, and Os. The 
bivalent chromosomes are now fully formed and 
ready to take their places on the spindle, which 
soon forms. 

In the case of the animal egg the "growth 
period " introduces a complication. In the 
sporocytes of plants and the sperm atocytes of 
animals there is some enlargement of the cell 
and nucleus during the stages just described, 
but the chromosomes pass directly from the 
strepsinema stage to diakinesis. During the 
relatively enormous growth of the oocyte on the other hand, 
the chromosomes, which have usually reached the strepsinema stage 
when the enlargement begins, become greatly modified in form. 
Their achromatic framework takes the form of fine threads extending 
out in all directions, giving the chromosome an irregular brush- 
like form (Fig. 86, C, D), while the chromatic substance either may 
flow into the nucleolus, leaving the chromosome framework uncolored and 
very difficult to observe, or by loss of its staining capacity through chem- 
ical change it may disappear from view completely. As the growth 
period comes to an end, however, the original staining capacity returns 
and the chromosomes again assume the compact form and pass into the 
diakinesis stage. 

FIG. 85. Parasynapsis in 
Phrynotettix magnus. 
A, leptonema; x, sex- 
chromosome. B, conjuga- 
tion of "chromosome A." 
Portions of other uncon- 
jugated threads and one 
other bivalent also present 
in section. X 2000. 
(After Wenrich, 1916.) 



In the case of most animals, and apparently in certain plants also, 
the split which is to function in the homoeotypic mitosis may develop dur- 
ing diakinesis or even much earlier, the result being the formation of 
chromosome tetrads. This introduces another element of complication 
which will be touched upon later (p. 243). 



j ***""*-* r ; {J^P t^T *'./' 

|\ <''**~~XX I ' "' J f&. y . 

FIQ. 86. 

A, parasynapsis in Allium fistulosum. B,paTa,synapsiaiiiOsmundaregalis. C, nucleus 
of oocyte of Scyllium canicula (Selachian) in "growth stage." D, single chromosome in 
growth stage, showing the fine subdivision of its substance. (A and B after Grtgoire, 1907, 
C and D after Marshal 1907.) 

The diakinesis stage is terminated by the dissolution of the nuclear 
membrane and the formation of the spindle, upon which the bivalent 
chromosomes, whether secondarily split or not, now become arranged. 
Because of the peculiar form and consistency of the heterotype chromo- 
somes the mitotic figure presents a striking contrast in appearance to the 
ordinary figure of somatic cells. This is especially true as the chromo- 
somes are drawn into various curious shapes as their anaphasic separation 
begins. The two univalent components of each bivalent chromosome 
eventually become free from each other and pass to the -two daughter 
nuclei, bringing about reduction. During the anaphase the separating 



FIG. 87. Nuclei from microsporocytes of Vicia faba, showing parasynapsis. 
Synigesis beginning in No. 6. X 1900. 

. FIG. 88. Heterotypic prophases in spermatocyte of Tomopteris onisciformis. 

A, pairing of leptotene threads beginning. B, pairing complete in some threads and 
only beginning in others. C, conjugation complete; pachynema stage. D, resplitting 
of pachytene threads (separation of conjugated chromosomes.) (After A. and K. E. 
Schreiner, 1905.) 


univalents, if not already double, rapidly develop a longitudinal split, in 
some cases even .before they are entirely free from each other. The 
resulting halves tend to open out along this split; chromosomes being 
drawn endwise to the poles thus take the form of simple Vs, while those 
to which the fibers are attached at the middle appear as double Vs. After 
reaching the poles the split chromosomes begin the reconstruction of the 
daughter nuclei. As a rule this does not proceed very far, since the 
homceotypic mitosis follows very quickly upon the heterotypic. Well 
organized daughter nuclei are often formed, whereas in the animal egg 
there may be no reconstruction whatever, the daughter chromosomes of 
the first mitosis at once taking their places on a newly formed spindle for 
the second mitosis. 

In the homoeotypic mitosis the chromosomes, if there has been an inter- 
vening interkinesis of any length, usually appear much longer and thin- 
ner than in the heterotypic mitosis, and separate along the longitudinal 
line of fission seen in the preceding anaphase. The homoeotypic mitosis 
is therefore equational in character, and differs from an ordinary somatic 
mitosis only in the number of its chromosomes and the precocity of their 
splitting. In each of the four nuclei resulting from the two maturation 
mitoses there is now the haploid number of univalent chromosomes, and 
meiosis is complete. 

The foregoing interpretation of reduction has been widely accepted 
from the first by both botanists and zoologists. The following is a partial 
list of works in which it has been described. 


Gre"goire 1904, '07 Lilium, Allium, Osmunda 

Berghs 1904, '05 Allium, Drosera, HeUeborus, etc. 

Rosenberg 1905, '07, '08, '09 Drosera, Composite 

Allen 1905&C Lilium, Coleochcete 

J. B. Overton 1905, '09 Thalictrum, Calycanthus, Richardia 

Strasburger 1905, '07, '08, '09 Lilium, Galtonia, etc. 

Miyake 1905 Lilium, Funkia, Iris, Allium, Trades- 

cantia, Galtonia 

Tischler 1906 Ribes 

Cardiff 1906 Acer, Salomonia, Botrychium, Ginkga 

Lagerberg 1906, '09 Adoxa 

Yamanouchi 1906, '08, '10 Polysiphonia, Nephrodium, Osmunda 

Martins Mano 1909 Funkia 

Lundegardh 1909, '14 Trollius 

Frisendahl 1912 Myricaria 

McAllister 1913 Smilacina 

Schneider 1913, '14 Thelygonium 

Weinzieher 1914 Xyris 

Sakamura 1914 Vida 

de Litardiere 1917 Poly podium 




von Winiwarter 


1904, '05, '07 

A. and K. E. Schreiner 1906, '07, '08 

Lerat 1905 

Deton 1908 

GrSgoire 1909 

Janssens ' 1905, '09 
Janssens et Willems 1909 

Schleip 1906, '07 

Debaisieux 1909 

Montgomery 1911 

Kornhauser 1914, '15 

Wenrich 1916, '17 

Fasten 1914, '18 

Malone 1918 

Pratt and Long 1917 

Robertson 1916 

Rabbit, Man 

Tunicates, Selachians, Teleosts, Amphi- 

Tomopteris, Ophryotrocha, Zodgonus, 

Enteroxenos, Myxine, Salamandra, 

Hersilia, Enchenopa 
Phrynotettix, Chorthippus 
Cambarus, Cancer 


FIG. 89. The method of chromosome reduction according to Scheme B. 
Explanation in text. 

Scheme B. The second of the two conspicuous interpretations was 
advanced by Farmer and Moore (1903, 1905), and is essentially as 
follows (Figs. 89-92) : In the early heterotypic prophase the reticulum 
becomes more thready in structure and contracts into a tight knot 
(synizesis). When this knot loosens up the chromatic material has 



assumed the form of a continuous spireme which is double. This double- 
ness is believed to represent a true longitudinal split, and although it 
usually disappears from view during the later prophases it is thought to 

FIG. 90. The heterotypic prophases in Lilium, according to Mottier (1907.) 
A, synizesis knot loosening up; threads splitting; note chromomeres. #, hollow spireme. 
C, second contraction. D, diakinesis. X 900. 

FIG. 91. Maturation mitoses in microsporocyte of Vicia faba. 
A, anaphase of heterotypic mitosis; split for second mitosis evident in separating 
daughter chromosomes. B, one daughter nucleus in early telophase of heterotypic mitosis. 
C, later telophase. D, metaphase of homoeotypic mitosis. E, anaphase of same, showing 
portions of both spindles. F, three of the four microspore nuclei. X 1335. (After 
Fraser, 1914.) 

persist and reappear at a much later stage. After extending loosely 
throughout the nucleus ("open spireme")> the double spireme, now con- 
siderably thickened and twisted (strepsinemd) , contracts again and is 



thrown into loops ("second contraction "). These loops then break 
apart from one another through a segmentation of the spireme; each of 
them is composed of two split chromosomes arranged end-to-end. Chro- 
mosome conjugation has thus occurred telosynaptically (metasyndetic- 
ally) either while the spireme was being formed or when the daughter 
spiremes were formed in the preceding telophase. The two members of 
each pair are brought around to a side-by-side position by the looping 
at the second contraction, usually but not always remaining closely 
connected at the original point of conjugation. The resulting bivalent 
chromosomes, with their split obscured, become much shortened and 
thickened (diakinesis) and take up their positions on the first maturation 
spindle. In case the original split, instead of being wholly obscured, is 
visible at this time or earlier, chromosome tetrads are evident. In the 
heterotypic anaphase the bivalents are separated into their component 
univalents, bringing about reduction. During the anaphase the uni- 
valents often widen out along the line of fission which had been tempo- 
rarily obscured, giving them the form of simple or double Vs as described 
for Scheme A. They remain through interkinesis in the double condi- 
tion, and in the homceotypic mitosis separate along this line of fission. 

The following is a list of the principal works in which this theory of 
eduction has been advocated. 

Farmer and Moore 
Farmer and Digby 
Farmer and Shove 











Farmer and Moore 

Moore and Embleton 



H. S. Davis 



1903, '05 Lilium, Osmunda, Psilotum, Aneura 

1910 Galtonia 

1905 Tradescantia 

1907, '09, '14 Lilium, Acer, Allium, Podophyllum, 
Tradescantia, Staphylea 

1904 Ferns 

1908 Finns, Thuja 

1906, '09 Agave 

1910, '12, '14, '19 Galtonia, Primula, Crepis, Osmunda 

1914 Vicia 
1912 Smilacina 
1912 Fuchsia 

1912, ; 13 Equisetum, Crepis t Tragopogon 

1915 Smilacina 

1916 Allium 


1905 Periplanelaj Elasmobranchs 
1903, '04, '05, '06, Hemiptera, Amphibia 


1906 Amphibia 

1906 Ascaris 

1907 Forficula 

1908 Insects 
1920 Perl" 



Some of the above named investigators, notably Miss Digby (1910, 
1912, 1914, 1919), Miss Fraser (1914), and Miss Nothnagel (1916), 
have laid emphasis upon the view that the split seen in the early hetero- 
typic prophase has its origin in the telophase of the last premeiotic divi- 
sion, each chromosome persisting through the intervening resting stage 
in the double condition. It is consequently held, as fully stated by Miss 
Digby (1919) in her account of the archesporial and meiotic phases of 
Osmunda (see Fig. 92), that the lateral pairing of thin threads in the 


FIG. 92. Diagram showing behavior of chromosomes in premeiotic and 

meiotic phases in Osmunda, according to Digby (1919). 

a, split which originates in telophase of premeiotic mitosis, persists (though obscured at 
times) through heterotypic prophases, reappears in heterotypic anaphase, and becomes 
effective in homceotypic mitosis, b, split which originates in heterotypic telophase, 
persists obscured through homceotypic prophases, reappears in homceotypic anaphase, 
and becomes effective in post-homceotypic division, x, plane of conjugation. 

heterotypic prophase which the advocates of Scheme A have regarded 
as a conjugation of entire chromosomes is in reality only the reassocia- 
tion of the two halves of one chromosome which had been split in the 
preceding telophase. Such a reassociation is thought to occur in every 
prophase, somatic and heterotypic, since these workers regard chromo- 
some splitting as regularly a thlophasic phenomenon. The split which 
forms in the last premeiotic telophase functions in the homceotypic 
mitosis: the homceotypic division is therefore looked upon as the continua- 
tion of the premeiotic division, the heterotypic mitosis being an inter- 
polated process bringing about numerical reduction. Not only does this 
premeiotic split reappear in the anaphase of the heterotypic mitosis to 
function in the homceotypic, but a new split develops in the heterotypic 



telophase, and after being temporarily obscured functions in the post- 
homoeotypic division. 1 

A variation of Scheme B has been observed in (Enothera (Gates 1908, 
1909, 1911; Geerts 1908; B. M. Davis 1909, 1910, 1911); in Fucus and 
Cutleria (Yamanouchi 1909, 1912); in Bufo (King 1907); and in a few 
other forms. Here the spireme in the heterotypic prophase does not 
become double, the split for the second division appearing first in the 
heterotypic anaphase. 

Comparison of Schemes A and B. According to both of the fore- 
going prominent theories of reduction the conjugated chromosomes 
separate at the first maturation mitosis, thus causing reduction, and 





FIG. 93. Diagram showing distinction between Schemes A and B. See text. 

divide longitudinally (equationally) at the second mitosis, so that the 
final result is essentially the same: two of the resulting four nuclei differ 
qualitatively from the other two in their chromatin content (Fig. 93). 
The distinction between the two interpretations is nevertheless an im- 
portant one, and may be emphasized in the following summary. 

According to Scheme A the double character of the chromatin spiremes 
of the early heterotypic prophase is due to a lateral pairing of simple 
threads each representing an entire somatic chromosome, the second con- 
traction not being significant as regards pairing. The bivalent chromo- 
somes so formed, after much shortening and thickening, are separated in 
the heterotypic mitosis, during the anaphase of which (or earlier in the 

1 A more detailed summary of this view may be found in a review of Miss Digby's 
paper on Osmunda by the present author (1920a). 


case of chromosome tetrads) the split that is to function in the homceoty pic 
mitosis makes its appearance. The doubleness in the heterotypic pro- 
phase is therefore not homologous with that in the somatic prophase: 
in the former it is due to a conjugation and in the latter to a split. 

According to Scheme B the doubleness of the heterotypic prophase is 
due to a true splitting as in the case of somatic division. In both cases, 
moreover, the split may have its origin in the preceding telophase. The 
bivalent chromosome is formed by the association in pairs (often at first 
end-to-end in the spireme but later side-by-side) of segments of this split 
spireme at the time of the second contraction. The two split univalents 
composing the bivalent are separated in the heterotypic mitosis, while 
in the homoeotypic mitosis the separation is along the line of the split 
originating in the last premeiotic telophase and seen in the spireme of the 
early heterotypic prophase. The doubleness of the early heterotypic 
prophase is therefore regarded as homologous with that of the somatic 
prophase: in both cases it represents a true split. 

It cannot yet be said what the outcome of this controversy is to be. 
The advocates of Scheme A believe that those of Scheme B have mis- 
interpreted the changes occurring in the early heterotypic prophase and 
in all telophases, while the latter charge the former with a neglect of the 
second contraction stage. Scheme B as fully elaborated by Miss Digby 
has certain advantages: it allows one interpretation to be placed upon 
the double spireme in both somatic and heterotypic prophases, irrespective 
of the exact time at which the split originates, and it also helps to explain 
the sudden appearance of the split for the second maturation mitosis in 
the anaphase of the first. Scheme A, on the other hand, is preferred by 
geneticists because of the earlier and much longer continued association 
of the conjugating chromosomes, which allows a greater opportunity for 
"crossing-over" to occur. The significance of this point will be brought 
out in Chapter XVII. 

This question, however, must be settled primarily by direct evidence. 
It is obvious that its solution depends upon the exact manner in which the 
telophasic transformation of the chromosomes and the derivation of the 
latter from the reticulum in the prophase are accomplished. It is granted 
by both schools that the alveolar or reticulate condition in which the 
chromosomes are found in late telophase is continuous with the similar 
condition seen in the succeeding prophase. If, then, it is true (1) that 
the telophasic transformation (alveolation) represents a true splitting, 
and (2) that the early prophasic reticulate condition passes directly 
into the double spireme, it follows that this doubleness in every prophase 
is due to the split originating in the preceding telophase. But workers on 
mitosis are not at all agreed that the evolution of the chromosomes is 
that stated in (1) and (2). It has been shown in Viciafaba (Sharp 1913), 
Tradescantia (Sharp 19206), and a number of other instances (see Chapter 


VIII) not only that the telophasic alveolation is too irregular to bfe 
regarded as a splitting, but also that the reticulate condition of the pro- 
phase, instea^ of developing directly into the definitive split, gives rise 
to simple thin threads in which a new split is developed. From this it 
cannot be concluded that in no form does the split develop directly from 
the early reticulate condition, or that the telophasic alveolation, though 
irregular, may not later become so equalized as to constitute the first 
stages of the split; but it does follow that it is quite unsafe to use the 
principle of telophasic splitting as a premise from which to draw the 
conclusion that the approximation of thin threads in the early heterotypic 
prophase represents the reassociation of the halves of a single split 
chromosome. It is well to emphasize the possible importance of the 
premeiotic telophase, but any ultimate solution of this perplexing prob- 
lem must be reached mainly through a more refined analysis of those 

FIG. 94. Chromosome pair "B" in Phrunotettix maynus, showing condensation of 
bivalent pair during the heterotypic prophases to form the compact chromosomes appearing 
on the spindle at metaphase. X 1734. (After W enrich, 1916.) 

prophasic changes which have led a long list of investigators to the con- 
clusion that the early heterotypic association of slender threads represents 
a conjugation of entire chromosomes which separate in the first matura- 
tion mitosis. 

One of the most convincing pieces of direct evidence favoring Scheme 
A is found in Wenrich's recent work on Phrynotettix (1916). Wenrich is 
able to trace a single pair of chromosomes, distinguishable by their 
peculiar form and the arrangement of their chromatic accumulations or 
chromomeres, through every stage from the spermatogonia to the sperma- 
tids. During the heterotypic prophase the two members of the- pair 
conjugate parasynaptically while in the form of slender filaments. Simi- 
larly strong arguments are advanced by Robertson (1916) as the result 
of his detailed analysis of the chromosome groups in other Tettigidse 
and Acrididae, in which the homologous members can be followed with 
much certainty because of their frequent inequality in size. 

Reduction With Chromosome Tetrads. As already pointed out, the 
marking out of the lines of separation for both maturation divisions 
during the heterotypic prophase, with the resulting formation of chromo- 
some tetrads, increases in no inconsiderable manner the difficulty of 
interpreting the essential changes at these stages. The four chromatids 
composing the tetrad represent two conjugated chromosomes each of 
which is longitudinally split. Because of the variety of ways in which 



these may arrange themselves with reference to one another in the form 
of simple or compound rods, crosses, and rings their distribution to the 
daughter nuclei, as well as the manner of their origin, is very difficult to 
follow with certainty. The accompanying diagrams will serve to illus- 
trate the more common modes of behavior described for chromosome 
tetrads, which are found chiefly in the cells of animals. 

Figure 95, D represents an exceptional method of tetrad formation 
described by Henking (1891) f or Pyrrochoris and by Korschelt (1895) for 
Ophryotrocha. The continuous spireme segments to form the diploid 
number of chromosomes, 1 which then split longitudinally and shorten. 

FIG. 95. Reduction with chromosome tetrads. 

Z>, in Pyrrochoris (Henking) and Ophryotrocha (Korschelt.) E, in certain copepods 
(Ruckert, Haecker, and vom Rath.) F, in Anasa and Allolobophora (Paulmier; Foot and 

No conjugation occurs until the metaphase, when the split chromosomes 
come together end-to-end, forming tetrads. They at once separate in 
the anaphase, bringing about reduction. In the second mitosis they 
divide along the original split, so that each of the four resulting nuclei 
receives the haploid number of chromosomes, two of the nuclei thus 
differing from the other two as the result of the separation of entire 
(though secondarily split) chromosomes at the first mitosis. According 
to Goldschmidt (1905), the chromosomes of Zoogonus mirus, after thus 
undergoing no prophasic conjugation, divide longitudinally at the first 

1 For the sake of uniformity and clearness the diploid number is represented as 6 
in all of these diagrams. 


mitosis and separate into two haploid groups at the second. To this 
simple form, of reduction Goldschmidt applied the term "Primaertypus." 
Gr6goire (1909a), on the contrary, found parasynapsis and the usual 
mode of reduction in Zoogonus. 

The interpretation at one time given by Riickert (1893, 1894), 
Haecker (1895), and vom Rath (1895) for certain copepods is shown in 
Fig. 95, E. The continuous spireme splits throughout its length and then 
breaks into the haploid number of segments. These again break trans- 
versely, forming chromosome tetrads, each composed of two split chromo- 
somes arranged end-to-end. In some species the chromatids open out to 
form four-parted rings, whereas in others they maintain the rod form. 
A separation occurs along the line of the original split at the first mitosis, 
which is therefore equational, and along the plane of conjugation at the 
second mitosis, which is therefore reductional. In Dicroccelium Gold- 
schmidt (1908) reported that such tetrads divide reductionally at the 
first mitosis. Lerat (1905), moreover, has found that in Cyclops strenuus, 
one of the forms used by the earlier workers, the tetrads arise by a parallel 
conjugation of thin threads which later split. 

A third mode of tetrad behavior is that reported by Paulrnier (1899) 
for Anasa tristis and by Foot and Strobell (1905, 1907) for Anasa and 
Allolobophora foetida (Fig. 95, F). Here the chromosomes conjugate 
cnd-to-end, the bivalents so formed then splitting longitudinally, giving 
tetrads which take on a cross or ring form. At the first mitosis the sepa- 
ration is along the plane of conjugation, effecting reduction, and at the 
second it is along the plane of splitting. According to McClung (1902), 
Sutton (1902, 1905), Robertson (1908), and others, such tetrads separate 
reductionally at the second mitosis (postreduction) rather than at the 
first (prereduction) in certain orthopterans studied by them. 

Figure 96 illustrates the origin of chromosome tetrads of five charac- 
teristic types by the two prominent modes of reduction described in 
detail in foregoing pages. According to Scheme A (Ar~Ci), two chromo- 
somes conjugate parasynaptically while in the form of slender threads. 
Instead of remaining unsplit as in most plants, each member then splits 
longitudinally in a plane at right angles to the conjugation plane, thus 
giving a tetrad composed of four parallel strands (chromatids) (D). 
According to Scheme B (A 2-<7 2 ), the two chromosomes are at first ar- 
ranged telosynaptically in the spireme and the latter splits throughout its 
length. The two conjugating members then take up a side-by-side 
position, and their split, instead of becoming obscured as usually occurs 
in plants, remains open, giving the tetrad of parallel strands (Z>). 

The tetrad, by whichever method it has arisen, may now undergo a 
variety of alterations, some of which are hown at E and F. The chroma- 
tids may simply shorten and thicken, the tetrad at diakinesis maintaining 
the form of parallel rods (Ei, FI). They may open out along the plane of 



conjugation (E t ) and take the form of rod tetrads (Ft) like those described 
by Riickert and Haecker. While opening out in this manner the longi- 

FIG. 96. Diagram showing the origin of the tetrad of chromatids (D) according to 
Scheme A (Ai-Ci) and Scheme B (Az-Cz), and the further transformation of this tetrad into 
tetrads of five types (Fi-Ft) . 

tudinal halves of each chromosome may diverge where the two chromo- 
aptnoes. remain in contact (JS? 8 ), the tetrad eventually taking the form of a 
Qrpss (F 3 ) as in the cases described by Paulmier and by Foot and Strobell. 



If the conjugated chromosomes remain in contact at both ends (#4) a 
complete ring results (F 4 ). In certain orthopterans the four chromatids 
open out along the conjugation plane in some regions and along the plane 
of splitting in other regions; this results in the curious compound rings 
(Fig. 156) found in the cells of these insects. Finally t the chromatids 
may open out from one end along the conjugation plane and from the 
other end along the splitting plane (#5), the tetrad then assuming the 
form of a ring composed of four parts (F 6 ). In all cases the tetrads usu- 
ally condense into compact quadruple bodies by the time they take their 
places on the spindle of the heterotypic mitosis. 

FIG. 97. Reduction with chromosome tetrads in Fasciola hepatica, according 
to Srhellenberg (1911). Explanation in text. 

The four chromatids composing the completed tetrad are in most cases 
exactly similar in appearance, so that it is a matter of much difficulty to 
determine along which plane they are separated at the first maturation 
mitosis. According to the two theories of tetrad origin illustrated in 
the foregoing diagram, however, the chromatids are supposed in almost 
all cases to separate along the plane of conjugation at the first mitosis, 
and this conclusion is supported by the behavior of those bivalent chromo- 
somes which are not divided into tetrads of chromatids. 

A further interpretation of reduction involving chromosome tetrads 
has been given by Schellenberg (1911) for the parasitic flatworm, Fasciola 
hepatica (Fig. 97). The chromatin in the heterotypic prophase takes the 
form of a long slender filament which splits longitudinally soon after 
synizesis. This double thread then segments into the haploid number of 


pieces, each representing two chromosomes end-to-end; these have the 
form of loops with a definite orientation (" first boquet stage")- Each 
segments again, giving the diploid number of split chromosomes, which 
again assume the form of oriented loops (" second boquet stage"). The 
halves twist tightly about each other, shorten to form the double bodies 
seen at diakinesis in the diploid rather than the haploid number, and then 
conjugate to form the haploid number of chromosome tetrads. The 
conjugating members (each split) separate at the first mitosis, bringing 
about reduction; at the second mitosis the separation is along the line of 
the original split. According to this interpretation, therefore, the double- 
ness of the early heterotypic prophase is due to a split, as in Scheme B, 
but the chromosomes arranged end-to-end in the spireme soon become 
separated and do not conjugate again until diakinesis. 

For a number of years it was thought (Carnoy 1886; Boveri 1887; 
Hertwig 1890; Brauer 1893) that the chromosome tetrad in Ascaris 
megalocephala was exceptional in being formed by two longitudinal fis- 
sions of a primary chromatin rod, there being as a consequence no quali- 
tative reduction in the two maturation divisions unless the organization 
of the chromatin were different from that of other organisms. But it has 
since been shown that they arise as in other organisms by the conjugation 
of two split chromosomes (Sabaschnikoff 1897; Tretjakoff 1904; Griggs 
1906). In the oogenesis Griggs reports telosynapsis with prereduction, 
whereas in the spermatogenesis Tretjakoff describes parasynapsis followed 
by postreduction. In Ascaris canis (Marcus 1906; Walton 1918) the 
four chromatids each show a transverse constriction, the chromosomes on 
the first maturation spindle having the form of octads. 

Although the formation of well differentiated chromosome tetrads 
occurs very commonly in animals, it appears to be very rare in plants. 
Farmer (1895) described tetrads in Fossombronia, and they have since 
been reported in at least three other bryophytes: Pallavicinia (Moore 
1905), Sphagnum (Melin 1915), and Chiloscyphus (Florin 1918). They 
have also been described in a few vascular plants: Equisetum (Osterhout 
1897), Pteris (Calkins 1897), Ariscema (Atkinson 1899), Tricyrtis (Ikeda 
1902), Thalictrum, Calycanthus, and Richardia (Overton 1909) (Fig. 98), 
Spinacia (Stomps 1911), Primula (Digby 1912), and Lopezia (Tackholm 

According to Grgoire (1905) such structures in plants are not true 
tetrads, but resemble them because the chromosomes are often bent and 
have their material accumulated largely at their ends. Sakamura 
(1920) interprets them as conjugated constricted chromosomes, and denies 
that the quadripartite condition has anything to do with reduction in 
such cases. He likewise accounts for the metasynaptic rod tetrads (Fig. 
95, E) described by several investigators of maturation in animals, 
holding that they represent two constricted chromosomes conjugated 



parasynaptically rather than two split ones placed end-to-end. In 
support of this contention he cites the following observations: such 
"tetrads" are seen not only .in the oocytes and spermatocytes but also in 
oogonia, spermatogonia, and somatic cells; the supposed telosynaptically 
conjugated members are often very unequal in size; such tetrads are 
sometimes divided in the transverse plane at neither maturation mitosis ; 
not only tetrads, but also octads and hexads are often observed, even in 

o + 


FIG. 98. Chromosome tetrads, 

A, five stages in the development of the tetrad in the spermatocyte of Anasa tristis. 
X 3000. From a preparation by Dr. H. E. Stork. B, tetrads in sporocyte of Chiloscyphus. 
Enlarged; X 2800. (After Florin, 1918.) C, tetrads in Richardia africana. (After 
Overton, 1909.) D, false tetrads in somatic cells of Pisum due to action of chloral hydrate 
on constricted chromosomes. (After Sakamura, 1920.) 

the same cell, and these are plainly due to the presence of additional 
accentuated constrictions. Robertson (1916) also interprets such telo- 
synaptic rod tetrads as those observed by Haecker in the copepods as 
constricted chromosomes. The constrictions, according to this writer, 
represent points of temporary union between non-homologous elements. 
From these considerations it is evident that constrictions have much to 
do with the appearances assumed by chromosomes, and that they should 
be taken into account in interpreting the chromosome tetrad. 

Numerical Reduction Without Qualitative Reduction. Figure 99 
illustrates the behavior of the chromosomes in maturation according to 
three not widely accepted views. A few workers, including Fick (1907, 



1908), Meves (1907, 1908, 1911), Giglio-Tos (1908), and Granata (1910), 
reject the theory of chromosome individuality and specificity, and 
therefore do not regard the chromosomes which are distributed to the 
four cells at maturation as at all identical with those of the divisions im- 
mediately preceding, except in so far as they are composed of the same 
nuclear material. Accordingly they recognize no qualitative reduction, 
but only a numerical one. This reduction in number results from the 
fact that the spireme formed in the hctcrotypic prophase (Fig. 99, A) 
segments into the haploid number of pieces instead of the diploid number, 
these pieces being simply divided longitudinally at both maturation 
divisions, and the four resulting nuclei being qualitatively similar. 

FIG. 99. Diagram showing three reported modes of numerical reduction with- 
out qualitative reduction. 

A, according to Pick et al. B, according to Vejdowsky; complete fusion of conjugating 
members. C, according to Bonnevie; bivalents arranged on spindles in juxtaposition; 
fusion of conjugating members eventually becomes complete. 

According to Vejdowsky (1907) (Fig. 99, B) the chromosomes appear 
in diploid number in the heterotypic prophase and conjugate parasynapti- 
cally. The members of the pair fuse completely and lose their individual 
identity, so that the chromosomes appearing on the first maturation 
spindle in haploid number are new entities, and not merely temporary 
pairs of somatic chromosome individuals. At both divisions these bodies 
split longitudinally, giving equivalence to the four resulting nuclei. 
Here, as in the foregoing example, there is no definite qualitative reduc- 
tion in Weismann's sense, though a numerical reduction is brought about 
by means of a complete fusion at the time of chromosome conjugation. 


An interpretation put forward by Bonne vie (1906, 1908) is shown in 
Fig. 99, C. Here the chromosomes conjugate parasynaptically and 
come into very intimate union: although they appear to undergo a real 
fusion their identity is maintained for a time. Owing to the fact that 
these bivalent chromosomes are inserted upon the spindle with their 
halves in juxtaposition (side-by-side with respect to the poles) rather than 
in superposition (one toward each pole), the members of a conjugated 
pair separate neither at the first division nor at the second. As a result 
each of the four cells receives the haploid number of chromosomes, all 
of which are bivalent, and no qualitative reduction occurs. Bonnevie 
believes that the conjugating members of each pair finally fuse completely 
in the subsequent stages. In this case, therefore, as in the preceding one, 
numerical reduction is supposed to result from a complete fusion of the 
chromosomes in pairs. 

Whether any confidence is to be placed in such interpretations or not 
and according to most cytologists none should be they at least serve 
to show how it is possible that numerical reduction may occur without 
effecting any qualitative reduction, and that the essential feature of the 
reduction of the chromosomes is something other than the mere change 
in their number, as pointed out at the beginning of the chapter. 


The phenomenon of chromosome conjugation, or synapsisj which we 
have seen above is such an important feature of the reduction process, 
must now be somewhat more closely examined. Attention will be 
directed to three points: the relationship of the conjugating members 
(the "synaptic mates"); the stage at which the synaptic union takes 
place, and the exact nature of this union. 

Relationship of the Synaptic Mates. We may first inquire into the 
relationship which may exist between the two chromosomes pairing to 
form a given bivalent chromosome: is any chromosome of the duplex 
group (the two intermingled parental chromosome sets in the individual's 
nuclei) present in the gonotokont free to pair with any other chromosome, 
or does the pairing take place according to more restricting rules? 

It was suggested by Henking (1891) that the two synaptic mates are 
ultimately derived from the two parents at the previous fertilization, 
one from the father and the other from the mother: the chromosomes of 
one parental set pair with those of the other parental set to form the 
haploid number of bivalent chromosomes appearing on the first matura- 
tion spindle. This idea was later emphasized and developed by Mont- 
gomery (1900-4), Sutton (1902), Boveri (1901), and others, who found 
for it much supporting evidence in organisms with chromosomes differ- 
ing in size and shape. An observation made by Rosenberg (1909) on 
Drosera hybrids is significant in this connection. When Drosera rotundi- 


folia (20 chromosomes) is crossed with D. longifolia (40 chromosomes) 
there results a hybrid with 30 chromosomes, of which 10 are contributed 
by rotundifolia and 20 by longifolia. When synapsis occurs preparatory 
to reduction in this hybrid only 10 bivalents are formed, 10 chromosomes 
remaining unpaired. This was taken by Rosenberg to mean that the 10 
rotundifolia chromosomes pair with 10 of the longifolia ones, leaving the 
other 10 of longifolia without synaptic mates. Had any chromosome of 
the duplex group of 30 been free to pair with any other, 15 bivalents 
would have been produced. 

Other instances of this phenomenon may be mentioned. By crossing 
(Enothera Lamarckiana (seven chromosomes in gamete) with (E. gigas (14 
in gamete) individuals with 21 chromosomes are obtained. Geerts 
(1911) found that, preparatory to reduction, the seven Lamarckiana chro- 
mosomes pair with seven of the gigas chromosomes, leaving the other 
seven of gigas unpaired. On the contrary, however, Gates (1909) found 
that the 21 chromosomes in a lata-gigas hybrid simply separate into two 
approximately equal groups, usually of 10 and 11 chromosomes re- 
spectively. Kihara (1919) reports that in some 35-chromosome wheat 
hybrids formed by crossing Triticum polonicum (14 chromosomes in 
gamete) with T. spelta (21 in gamete) there are present in the heterotypic 
prophase 14 bivalents (polonicum conjugated with spelta) and seven 
univalents (spelta). The 14 bivalents are arranged on the spindle and 
separate as usual, whereas the seven unpaired spelta chromosomes split 
longitudinally at the first mitosis and distribute themselves irregularly 
at the second (Fig. 100). An analogous condition is found in Pigcera 
hybrids by Federley (1913). 

A very significant additional suggestion with respect to synapsis was 
made by McClung (1900) and Sutton (1902) : not only are the two chromo- 
somes which conjugate derived from the two parents, but they are hom- 
ologous each chromosome of one parental set pairs with a particular 
chromosome of the other parental set, the two members of the resulting 
bivalent being presumably of corresponding hereditary value, as will be 
shown in Chapter XV. The evidence for this important hypothesis was 
found chiefly in Brachystola (Fig. 101) and a number of other insects 
having chromosome complements made up of members with constant 
characteristic differences in size and shape. Many such cases have been 
subsequently discovered, especially by McClung and his coworkers in 
their extensive researches on insect spermatocytes. As examples among 
plants may be cited Crepis virens, Najas major, N. marina, and Vicia 

Crepis virens (Rosenberg 1909) (Fig. 102) has six chromosomes: two 
long, two medium sized, and two short. When synapsis occurs the like 
chromosomes pair, forming bivalents of three sizes. The members of 
each pair separate and pass to the daughter cells at the first maturation 



mitosis, each microspore (after the second mitosis) having as a result 
three chromosomes: one long, one medium sized, and one short. Since 
the gamete receives such a simplex group of three chromosomes, and the 

FIG. 100. Heterotypic mitosis in Triticum polonicum X T. spelta. 
A, the 21 chromosomes (polar view). B, 14 bivalents separated into component 
univalents; 7 unpaired spelta chromosomes have split and are about to be distributed. 
(After Kihara, 1919.) 

somatic cells of the new individual show six (two of each length), it is 
evident that the other gamete furnishes a similar simplex group of three. 

FIG. 101. The chromosome complement in the spermatocyte of Brachystola 
magna. (After Sutton, 1902.) 

In Najas marina and Najas major (Mliller 1911; Tschernoyarow 
1914) the duplex group of 14 chromosomes is made up of seven visibly 
different pairs (Fig. 56 bis). In the heterotypic prophase these conjugate 
selectively to form seven bivalents, the reduced nuclei therefore receiving 



a set of seven visibly different chromosomes. Sakamura (1920) hplds 
the number here to be six rather than seven. (See p. 160.) 

In Vicia faba (Sharp 1914; Sakamura 1915, 1920) there are in the 
somatic cells 12 chromosomes, two of them being about twice as long as 
the other 10 (Figs. 56 and 102). At synapsis in the microsporocyte there 
are formed six bivalents, one of them having about twice the length of 
the other five. Hence it is clear that the two long chromosomes pair 
with each other. In the heterotypic mitosis the synaptic mates separate 



FIQ. 102.- 

-Chromosome cycles in Vicia faba and Crepis virens, showing 
homologous pairing. 

and pass to the daughter nuclei, bringing about reduction. At the close 
of the homceotypic mitosis the microspore, and hence the male gamete 
to which it later gives rise, receives a simplex group of six chromosomes: 
one long and five short. Since the somatic cells contain each of these in 
duplicate it is evident that a similar set is contributed by the female 

Summing up, we may draw from the above facts certain very impor- 
tant conclusions: (1) Each parent furnishes the offspring with a set of 
chromosomes, the members of the two sets being intermingled in all the 
nuclei of the new individual. This point will receive further attention in 
the following chapter on fertilization. (2) The two members of each 
bivalent chromosome formed at synapsis are derived one from each parental 
set. (3) Each chromosome of the paternal set conjugates with a particular 
chromosome of the maternal set: the two are in some sense homologous. 


It should be pointed out that cytologists and geneticists have generally 
assumed that each synaptic pair is independent of all the others as 
regards the manner in which it is oriented on the heterotypic spindle. 
In some pairs the paternal members are directed toward one pole and in 
other pairs toward the other pole. It is conceivable that in some cases 
all the paternal members might go to one pole and all the maternal 
members to the other. Direct evidence that the assortment of the 
various chromosome pairs is in this respect a random one as originally 
assumed has been furnished by Miss Carothers (1913, 1917). In the 
grasshopper, Trimerotropis, she finds that the components of some of the 
bivalents are visibly different in size, in the mode of attachment to the 
spindle fibers, and in the presence of constrictions; and that these differ- 
ences make it possible to show beyond question that the several pairs are 
entirely independent of one another as regards their orientation on the 
spindle and their consequent distribution to the daughter cells. 

From the precise manner in which the distribution of chromosomes 
at the time of reduction and at other stages of the life cycle parallels the 
distribution of the hereditary characters it is inferred that such hom- 
ologous chromosome pairs represent the material basis for the allelo- 
morphic pairs of Mendclian characters exhibited by the organism. This 
subject is to be taken up in Chapter XV. 

The Stage at Which Conjugation Occurs. In the great majority of 
observed cases chromosome conjugation occurs during the prophase 
of the first maturation division. Since the chromatin threads at some 
time during these prophases usually take the form of a tightly contracted 
knot out of which they emerge in an obviously double condition, it was 
suggested (Moore 1896) that the contraction is an important factor in 
bringing about the conjugation, and the contraction itself came to be 
called " synapsis." But an examination of the various modes of reduction 
shows that the conjugation may begin very early, before the contraction 
(Fig. 83) or, on the other hand, not until the spindle is established 
(Fig. 95, D). The conjugation of the chromosomes is therefore to be 
distinguished from the contraction. It has now become customary to 
refer to the former, at whatever stage it occurs, as synapsis, and to the 
latter as synizesis. 

In an increasing number of reported cases the paired association 
apparently begins even before the heterotypic prophase. The chromo- 
somes have been observed in several instances to undergo pairing during 
the anaphase and telophase of the last premeiotic division. Such is the 
condition in certain Hemiptera (Montgomery 1900, 1901), Oniscus 
(Nichols 1902), Brachystola (Sutton 1902), Scolopendra (Blackman 
1903, 1905), Pedicellina (Dublin 1905), and a number of more recent 
cases. Furthermore, the pairing has been stated to begin in the sperm- 
atogonia several cell generations before maturation in certain Hemiptera 


and Ascaris (Montgomery 1904, 1905, 1908, 1910), Alytes (Janssens 
and Willems 1909), Helix and Sagitta (Stevens 1903; Ancel 1903), certain 
Diptera (Stevens 1908, 1911), and Pediculus (Doncaster 1920). 

More recently it has been shown that the homologous chromosomes 
may begin to show a paired arrangement even earlier in the cycle, in 
some cases directly after the parental groups are brought together at 
fertilization. In the Diptera, for example, Metz (1916a) has shown that 
the association, which at certain stages is so close as to constitute a 
synapsis, begins before the cleavage of the fertilized egg, and that the 
paired condition is maintained in all cells, somatic and germinal, through- 
out the life cycle. Metz examined 80 species and in all of them found 
such a somatic pairing. In Culex (Stevens 1910, 1911; Taylor 1914, 
1917), which has six chromosomes, the association can be seen in the 
nuclei of the segmenting egg, and in the early larval stages there follows 
an actual parasynaptic fusion, so that the somatic cells thereafter show 
three bivalent chromosomes rather than six univalents. In the matura- 
tion divisions the members of each pair separate, the gametes receiving 
three chromosomes each, just as they would had conjugation begun in 
the heterotypic prophasQ as usual. 

A loosely paired arrangement of the chromosomes in the somatic 
cells of plants has been reported by Strasburger (1905, 1907, 1910) for 
Galtonia candicans, Funkia Sieboldiana, Pisum sativum, Melandrium, 
Mercurialis, and Cannabis; by Sykes (1908) for Hydrocharis, Lychnis, 
Begonia, Funkia, and Pisum; by Overton (1909) for Calycanthus; by 
Muller (1909, 1911) for Yucca and other forms; by Stomps (1910, 1911) 
for Spinacia; by Kuwada (1910) for Oryza; by Tahara (1910) for Morus; 
and by Ishikawa (1911) for Dahlia. This is another matter that will be 
considered further in Chapter XII. 

The Nature of the Synaptic Union. Because of the manner in which 
chromosome behavior is at present being applied to the solution of the 
problems of inheritance, no question concerning chromosome conjugation 
is more important than that of the exact nature of the synaptic union. 
In reviewing some of the opinions of this subject it will be convenient 
to list separately the views of the telosynaptists and the parasynaptists. 

In such cases as those described by Henking and by Goldschmidt 
Fig. 95, D) there is only a momentary end-to-end association of the fully 
formed chromosomes on the spindle of the heterotypic mitosis, there 
being no real fusion and almost no opportunity for an "interchange of 
influences/' In the other tetrad chromosomes formed by telosynapsis 
(Fig. 95, E and F; Fig. 90) there is only slightly greater opportunity 
for such interchange. According to Scheme B (Fig. 89) the synaptic 
mates are at first arranged end-to-end, and only later, when partially 
condensed, do they take up a side-by-side position, allowing a more 
intimate and extensive union for a short time. 


Generally speaking, the parasynaptists have given more attention 
to the details of the synaptic union than have the telosynaptists. Al- 
though cases are on record in which there is only a momentary para- 
synaptic association of fully formed chromosomes (von Voss 1914), 
the association usually extends over considerable time. Most para- 
synaptists hold that the conjugation begins with the association of the 
leptotne threads before or during synizesis, continues through the 
remainder of the prophase, and ends with the anaphasic separation 
(Scheme A). The association of the synaptic mates is thus long and 
intimate. Concerning the closeness of the union, however, opinions 
differ widely. 

A few investigators (Vejdowsky 1907; Bonnevie 1906, 1908, 1911; 
Winiwarter and Sainmont 1909; Schneider 1914) have thought that the 
conjugating members fuse completely and lose their individual identity, 
the "mixochromosome" so formed then undergoing two true longitudinal 
splits along new planes at the two maturation divisions. In some cases 
(Bonnevie; see p. 251) the fusion may not be fully consummated until 
during the post-meiotic divisions. Others believe the split for the 
heterotypic mitosis to be along the plane of conjugation (Cardiff 1906, 
Fasten 1914, and others). Probably the most widely advocated view is 
that there is no actual fusion of the synaptic threads, the latter main- 
taining their identity completely. Although their association may at 
times be so intimate that they seem to constitute a single thick thread, 
the doubleness, if thus lost to view, reappears during later stages (Berghs 

1904, 1905; A. and K. E. Schreiner 1905, 1906; Marshal 1907; Overton 

1905, 1909; Robertson 1915, 1916) (Fig. 88). Several careful observers 
have reported that the doubleness can be seen at all stages (Gr6goire 
1907, 1910; Schleip 1906, 1907; Montgomery 1911; Kornhauser 1914, 
1915; Wenrich 1915, 1917). Gr^goire, who has argued strongly for this 
interpretation, has emphasized the ease with which the closely appressed 
threads may be mistaken for a single thick structure. 

One of the most important suggestions which has been made concern- 
ing chromosome conjugation is embodied in the "Chiasmatype Hypo- 
thesis " of Janssens (1909). According to Janssens, the pairing threads, 
though remaining separate throughout the greater part of their length, 
fuse at one or more points as they twist about each other. When they 
again separate a break occurs at each of these fusion points, but along a 
new plane, so that each of the two resulting chromosomes is composed 
of portions of both conjugating members (Fig. 149). This interpreta- 
tion, which has been admitted as possible by several of the investigators 
named in the preceding paragraph, is significant in that it shows how an 
orderly evolution of chromosomes with new constitutions may occur, a 
point of great importance in connection with current conceptions of the 



physical basis of heredity. Soecial attention will be devoted o this 
question in Chapter XVII. * 

Chromomeres. An important r61e has been attributed to the chro- 
rnomeres by many students of synapsis. Allen (1905), for example, 
maintained that the fusion of the leptotSne threads in Lilium involves a 
fusion of their chromomeres, the subsequent division of the fused chro- 
momeres initiating the resplitting of the pachytene thread. Allen found 
the chromomeres to be composed of still smaller chromatic elements, 
and offered various suggestions concerning the manner in which the re- 
splitting of the pachytene thread might be supposed to effect a redistri- 
bution of the "idioplasms." That chromosome conjugation is primarily 
a conjugation of small chromatic elements within the chromosome was 
held by Strasburger (1904, 1905) and the Schreiners (1906). The visible 
chromatin granules, or "pangenosomes," were conceived by Strasburger 
to represent complexes of "pangens" such as were postulated by de Vries, 
conjugation involving an interchange of these latter units. 

The chromomere interpretation has been adversely criticised by 
Gr^goire (1907, 1910) on the basis of further evidence obtained from a 
study of the chromatic structures themselves. This author points out 
several serious objections to the view that the chromomeres are auton- 
omous bodies, and concludes that they are rather to be regarded simply 
as swellings or thicker portions of the chromatin thread, such thick por- 
tions remaining as the thread undergoes a stretching which is not uni- 
formly resisted at all points. Their frequently striking correspondence 
or paired arrangement in the synaptic threads is explained as the result 
of the response of the two closely associated threads to the same stretch- 
ing force. This interpretation is also shown to account for the variability 
in the dimensions of the chromomeres, their tapering form, the often 
reported absence of correspondence between the chromomeres of the 
two threads, and various other aspects. Wenrich (1916, 1917), on the 
other hand, has found that in Phrynotettix (Fig. 155) the chromomeres 
show a remarkable individual constancy in size and position in a given 
member of the chromosome complement, not only in the various cells of 
a given individual, but also in those of different individuals. These 
facts strongly suggest an autonomy of the bodies in question. 

Because of their great theoretical importance (see Chapter XVII) it 
is to be regretted that after such a large amount of research so many 
points regarding the process of synapsis should remain in such an un- 
settled state. It is hoped that further refinements in microtechnique 
may remove some of the obscurity which at present surrounds them. 


Although the phenomena of the heterotypic prophase, particularly 
synizesis and synapsis, are generally looked upon as normal occurrences 


of considerable significance, not all investigators concur in this opinion. 
That synizesis is an artifact due to faulty fixation is an interpretation 
which, though it may be justified for certain cases in which the contrac- 
tion may be very slight or absent, is not of general application. Fixa- 
tion often serves to accentuate the appearance of contraction, but the 
characteristic synizesis figure has been observed widely enough in faith- 
fully preserved, and even in living material to make it evident that we 
are dealing here with a normal feature of the heterotypic prophase. It 
may not, however, be of universal occurrence. 

R. Hertwig (1908) came to the conclusion, as a deduction from his 
theory of the nucleoplasmic relation, that the phenomena of the hetero- 
typic prophase represent an abortive mitosis : the disturbed nucleoplasmic 
balance is restored to the normal by a multiplication of chromatin without 
an actual mitosis, the process taking the form of the changes peculiar to 
the heterotypic prophase. This view of Hertwig, which was denied by 
Gr^goire (19096), is supported by Kingsbury and Hirsch (1912), who 
state : 

" According to this view, on the one hand, synizesis represents 'an attempt 
on the part of the spermatogonia to divide again which fails; while on the other 
hand, the reputed conjugation of chromosomes occurring at about this time is 
but the imperfect fission and subsequent fusion of daughter chromosomes of such 
abortive division. " 

The above quoted authors regard synizesis and synapsis as indications 
of the onset of degeneration. In this conclusion they are supported by 
Kingery (1917), who, in his investigation of the white mouse, finds 
synizesis in the primitive germ cells which degenerate, but not in the 
definitive germ cells. Observations of a similar nature were made by 
Wodsedalek (1916) in the mule. If, as Kingery (1917) and Popoff 
(1908) point out, the "heterotypic" changes are due to degeneration, 
they should be found in abnormal somatic cells. Marcus (1907), in 
fact, had observed a contraction similar to that of synizesis preceding 
degeneration in the cells of the thymus gland. Nemec (1903) and Kemp 
(1910) also found that in the cells of roots treated with chloral hydrate 
the nuclei come to have an abnormally high number of chromosomes 
("syndiploid nuclei"), this number, according to Nemec, being gradually 
restored to the normal during the subsequent mitoses, which show 
phenomena of a heterotypic nature. Strasburger (1911), while agreeing 
with Nemec that the syndiploid condition gradually disappears, denied 
that any truly heterotypic phenomena are concerned. The "hetero- 
typic" changes observed by Nemec he held to be only peculiar vegetative 
mitoses with a superficial resemblance to genuine reduction divisions. 

Nemec's conclusion regarding a reduction in chloralized vegetative 
cells is also contradicted by Sakamura (1920), who has made a particu- 
larly exhaustive study of these phenomena. Sakamura finds that a 


variety of agencies, including chloral hydrate, benzene vapor, ether,, chlo- 
roform, and the gall-producing secretions of Heterodera, may be employed 
to bring about aberrations of the mitotic process. After the chromosomes 
are divided and partially distributed they may be reorganized in a single 
"didiploid" nucleus. In other cases the chromosomes may reorganize 
as two or more nuclei with various chromosome numbers, and these may 
often fuse to form " syndiploid ' ' nuclei. To all the kinds of stimuli applied 
the chromosomes react by becoming shorter and thicker, and thus appear 
like heterotypic chromosomes. Furthermore, latent or obscure constric- 
tions are rendered more conspicuous, so that some of the split chromo- 
somes appear like chromosome tetrads. Sakamura shows that these false 
tetrads do not represent heterotypic phenomena in any true sense: they are 
merely the result of the response of split and constricted chromosomes to 
the abnormal conditions induced in the cell, and have nothing to do with 
any reducing process. No such autoregulative reduction occurs in these 
didiploid cells, their gradual decrease in relative number being due to 
their lowered capacity for, and rate of, division. 

Child (1915) emphasizes the physiological significance of maturation, 
and shows that the heterotypic phenomena are associated with a low 
metabolic rate in the cells, that they may occur occasionally in other cells 
having a low rate, and that they can be induced artificially with narcotics 
as Nemec stated. 

All of these observations are interesting in that they indicate the 
nature of some of the physiological changes occurring at the time of matur- 
ation. The description of the heterotypic phenomena upon which will 
be based our ultimate interpretation of its significance, will not be com- 
plete until the physiological as well as the morphological changes have 
been exhaustively examined and correlated. But because it has been 
found that the onset of the meiotic process is associated with a lowering of 
the rate of metabolism which, if continued, may. result in degeneration; 
or because appearances similar to those of the heterotypic prophase may 
occur in other cells with disturbed metabolism ; it does not at all follow that 
the heterotypic phenomena are at bottom phases of a degeneration 
process, or that they have no other significance in the normal life cycle. 
These phenomena occur almost universally throughout the whole world 
of living organisms at a very critical stage in the life cycle and lead to 
significant results with a high degree of regularity. The lowered rate of 
metabolism accompanying them offers in the vast majority of cases no 
check to the normal functioning of the products of the maturation di- 
visions. It therefore seems more reasonable to regard the observed 
degeneration as a secondary effect that may occasionally set in during the 
normal heterotypic prophases because the metabolic rate is already at a 
relatively low level at that time, than to look upon the heterotypic 
changes as a part of a degeneration process which is only exceptionally 


completed unless, indeed, all changes in the organism which are accom- 
panied by a fall in the metabolic rate be regarded as degenerative in 

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1905. Les resultats acquis sur les cineses de maturation dans les deux regnes. 
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19096. Les phe'nomenes de l'e*tape synaptique represent-ils une caryocinse 

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1911. Chromosomenlangen bei Satamandra, nebst Bemerkungen zur Individ ual- 
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Monokotylen. Jahrb. Wiss. Bot. 42: 83-120. pis. 3-5. 
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1901b. Further studies on the chromosomes of the Hemiptera heteroptera. Proc. 
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1903. The heterotype maturation mitoses in Amphibia and its general significance. 
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1904. Some observations and considerations upon the maturation phenomena 
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1905. The spermatogenesis of Syrbula and Lycosa with general considerations 
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1906. Chromosomes in the spermatogenesis of the Hemiptera heteroptera. 
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1908. On the morphological difference of the chromosomes in Ascaris megalo- 
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1910. On the dimegalous sperm and chromosomal variation in Euschistus, with 
reference to chromosomal continuity. Ibid. 6: 121-145. pis. 9, 10. 1 fig. 

1911. The spermatogenesis of an Hemipteran, Euschistus, Jour. Morph. 22: 
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MOORE, A. C. 1905. Sporogenesis in Pcdlavicinia. Bot. Gaz. 40: 81-96. pis. 

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1905. The development of the heterotypic chromosomes in pollen mother-cells. 
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1907. The development of the heterotypic chromosomes in pollen mother-cells. 

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1905. Ueber die Entwicklung der m an n lie hen Geschlechtszellen von Myxine glu- 
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1906. Neue Studien tiber die Chromatinreifung der Geschlechtszellen. Arch. d. 
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1897. Kerntheilung und Befruchtung bei Fucus. Jahrb. Wiss. Bot. 30: 351-374. 

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1908. Chromosomenzahlen, Plasmastrukturen, Vererbungstrager und* Reduktions- 
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1910. Ueber geschlechtsbestimmende Ursachen. Ibid. 47: 427-520. pis. 9, 10. 

1911. Kernteilungsbilder bei der Erbse. Flora 102: 1-23. pi. 1. 

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1918. Alternation r nd parthenogenesis in Padina. Jour. Elisha Mitchell Sci. Soc. 

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401-449. pis. 19-28. 

1908. Sporogenesis in Nephrodium. Ibid. 45 : 1-30. pis. 1-4. 

1909. Mitosis in Fucus. Ibid. 47: 173-197. pis. 8-11. 

1910. Chromosomes in Osmunda. Ibid. 49 : 1-12. pi. 1. 

1912. The life history of Cutleria. Ibid. 54 : 441-502. pis. 26-35. figs. 15. 
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143-172. pis. 11-14. 


We have already pointed out that reduction and fertilization con- 
stitute the two principal cytological crises in the life cycles of all organisms 
reproducing sexually. Although the first of these processes was not dis- 
covered until 1883, some of the grosser features of fertilization had 
been made out many years previously (Chapter I). But the central 
feature of this process the union of the two parental nuclei was not 
known until 1875, when O. Hertwig discovered it in animals, Strasburger's 
parallel discoveries in plants following in 1877 (Spirogyra) and 1884 
(angiosperms). As the finer details of fertilization and the significance 
of its results become better understood, the aptness of Huxley's (1878) 
often quoted simile, in which he compares the organism to "a web of 
which the warp is derived from the female and the woof from the male," 
becomes increasingly striking. 

We shall first describe the morphology of the fertilization process 
as it is typically shown in many animals, after which attention will be 
given to some of its physiological aspects. The second half of the chapter 
will be devoted to a review of fertilization in the various groups of the 
plant kingdom. 


The Gametes. The spermatozoa of different animals exhibit a 
surprising variety of form and structure (Fig. 103). What may be 
referred to as the "typical" spermatozoon consists of three fairly distinct 
parts: head, middle piece , and tail or flagellum (Fig. 104). The head 
represents the nuclear portion of the sperm cell: it consists almost wholly 
of an extremely compact mass of chromatin. It has an envelope of 
cytoplasm which in few forms is very conspicuous and in many cases is 
scarcely distinguishable. Anterior to the nucleus there may be an 
acrosome, and the end of the head often has the form of a sharp point, 
the perferatorium. Posterior to the head is the middle piece; this is 
made up of cytoplasm in which are located the centrosomal structures, 
together with chondriosomes and other inclusions, such as the "Golgi 
bodies." The flagellum, or tail, consists of a slender axial filament, 

1 In the preparation of this portion of the chapter the author has drawn very freely 
upon Professor F. R. Lillie's admirable and concise presentation of the subject, 
Problems of Fertilization (1919). 

18 273 



which grows out from the centrosome in the middle piece or in some 
cases apparently from the base of the nucleus, and a cytoplasmic sheath 
which usually extends not quite to its end. The sheath sometimes has 
the form of an undulating membrane. The spermatozoa of crustaceans 
and nematodes are non-flagellate, and in other groups various departures 
from the " typical" form and structure are known. A few of the many 
.known types are shown in Fig. 103. 

Fio. 103. Various types of spermatozoa. 

A, Triton (salamander). (After Ballowitz.) B, Nereis (annelid). (After Lillie, 1912.) 
C, guinea pig. (After Meves.) >, Phyllopneuste (bird). (After Ballowitz.) E, sturgeon 
(After Ballowitz.) F, Vesperugo (bat). (After Ballowitz.) G, Castrada hofmanni (turbel- 
larian). (After Luther.) H , Pinnotheres veterum (crustacean) . (After Koltzoff.) I,Homa- 
rus (lobster). (After Herrick). J, Ascaris (nematode) ; a, apical body; n, nucleus; r, "re- 
fractive body." (After Scheben.) 

The ovum undergoes nearly or quite all of its elaborate differentiation 
before the maturation divisions occur. Certain cells in the ovary gradu- 
ally become greatly enlarged (Fig. 105), and during this "growth period" 
the cytoplasm may not only differentiate into visibly distinct regions 
but may also become stored with energy-containing materials ("food")? 
which in the case of some animals, such as birds, is present in relatively 
enormous amounts. The "ovarian egg" or primary oocyte, as the egg 
cell is called before the maturation mitoses take place, may have a definite 
limiting membrane at its surface, but in many forms this cannqf be 
demonstrated. The nucleus of the primary oocyte is known as the 



germinal vesicle: it is very large and contains in addition to its chromatin 
a considerable amount of material which appears to take no part in the 
formation of the chromosomes when division ensues. After the cyto- 
plasmic differentiation is complete and the oocyte has reached its full 
size even after the spermatozoon has entered in many 
cases the oocyte nucleus undergoes two divisions in rapid 
succession at the periphery of the egg, which at this point 
buds off two small nucleated cells, the polar bodies (Fig. 106). 
The first polar body may or may not divide again. The 
details of chromosome behavior in these two mitoses have been 
described in the preceding chapter. The reduced or haploid 
number of chromosomes left in the egg organize the egg 
nucleus (" female pronucleus"), rendering the egg ready for 
the sexual fusion. 

FIG. 104. FIG. 105. 

FIG. 104 .Diagram of typical flagellate spermatozoon. 

P, perferatorium; A, acrosome; N, nucleus; Af, middle piece; F, axial filament; V, 
cytoplasmic sheath; E, end piece. (After Wilson.) 

FIG. 105. The differentiation of the oocyte in Hydra. 

A, very young oocyte lying between ectodermal cells at right. B, oocyte after growth 
period, with yolk globules, X 500. (After Downing, 1909.) 

The time relation of the maturation of the egg and the entrance of the 
spermatozoon varies considerably in different animals. In echinoderms 
and some other forms maturation is completed before the spermatozoon 
penetrates. In some other animals it proceeds as far as the metaphase 
of the heterotypic mitosis (Chcetopterus, Cerebratulus) or the prophase of 
the homoeotypic mitosis (many vertebrates), but does not go further 
unless penetration occurs. In the marine annelid, Nereis, finally, the 



germinal vesicle undergoes no change unless the spermatozoon has 
entered the egg. 

Fio. 106. Maturation and fertilization in Ascaris. 

A, spermatozoftn about to enter egg. B, spermatozoon inside; first maturation mitosis 
in progress. C, first maturation mitosis completed; first polar body budded off. Z>, 
second maturation mitosis, forming second polar body; sperm nucleus below. E, male and 
female pronuclei, each with 2 chromosomes, meeting. F, first cleavage mitosis, showing 2 
paternal and 2 maternal chromosomes. (After Hertwig.) 

FIG. 107. Fertilization in Physa (snail.) Sperm head and amphiaster at right, with 
long flagellum extending toward left. Second maturation mitosis in progress. (After 
Kostanecki and Wierzyski, 1896.) 

The Fusion of the Gametes. In most cases the whole spermatozoon 
enters the egg (Fig. 107). In some sea urchins only the head and middle 
piece enter, while in Nereis the head alone passes in, the middle piece 


and tail being left on the egg surface. The process in Nereis as de- 
scribed by Lillie (1912, 1919) is as folloVs. The egg of this worm has a 
tough 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 alveolae of the cortical layer. This layer now takes the form of 
a zone traversed by radial protoplasmic plates representing the walls of 
the alveolae. A transparent*" fertilization cone" extends from the inner 
part of the egg across this zone and touches the membrane at the point 
where the spermatozoon is beginning to penetrate. The perferatorium 
pierces 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 in Nereis it seems clear 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 

The immediate visible effects of the entrance of the sperm are seen 
chiefly in changes in the appearance of the cortical region of the egg. If 
a vitelline membrane is present, as in vertebrates, a " perivitelline 
space" usually appears between the membrane and the egg; and this 
space may in some cases (frog) be great enough to permit the rotation 
of the egg within the membrane. In the sea urchin a fertilization mem- 
brane is formed as the result of fertilization : it first appears at the point 
where the spermatozoon is attached and spreads over the egg with great 
rapidity. It seems probable that a delicate membrane already present is 
raised and thus made more conspicuous. In Ascaris, which is parasitic 
in the intestine of the horse, this membrane becomes very thick and later 
acts as a protection against the digestive juices of the host. These 
cortical changes do not depend upon the actual entrance of the sperma- 
tozoon into the egg: in Nereis they occur before the slow penetration 
can be completed, or even if the spermatozoon is shaken loose shortly 
after penetration has begun. 

In describing the remarkable transformation undergone by the 
spermatozoon within the egg the behavior of its different organs will for 
the sake of clearness be considered separately. 

The Nucleus. Immediately after gaining entrance to the egg (Fig. 
108) the sperm head begins to enlarge and assumes the usual form and 
structure of a nucleus. Meanwhile it advances toward the egg nucleus. 
As Lillie points out, both male and female pronuclei pass toward a posi- 
tion 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 male pronucleus has usually, but not always, 
become equal in size and appearance to the female pronucleus. The 
union of the two pronuclei to form a fusion nucleus, or synkaryorij usually 

FIG. 108. Diagram of fertilization and cleavage in an animal. It is assumed that 
in this case the egg has undergone maturation before the penetration of the 

FIG. 109. Independence of parental chromatin contributions in the cleavage 

of the egg of Cryptobranchus. 

A, first cleavage mitosis. B, C, prophase and metaphase of fourth cleavage mitosis 
(After Smith, 1919.) 

occurs at once after they meet. In a great many cases there may be no 
actual fusion of the pronuclei at all: 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 on a 
common spindle which organizes when the nuclear membranes dissolve. 
The first cleavage mitosis (first embryonal division) then ensues, and 
the two daughter nuclei receive longitudinal halves of each and every 
chromosome. Thus in the act of fertilization, in both animals and plants, 
each parent furnishes the offspring with a haploid set of chromosomes, 
the two intermingled sets constituting the diploid set of the new individual. 
Since every chromosome divides equationally at every subsequent somatic 
mitosis, every cell of the body receives half of its chromosome complement 
from each parent. The cardinal importance of this fact in connection 
with current theories of heredity will be apparent in subsequent chapters. 

The two groups of chromoosmes, paternal and maternal, can often be 
distinguished not only on the spindle of the first cleavage division, but 
in several divisions thereafter. As examples may be cited Cyclops 
(Rtickert 1895; Hsecker 1895), Crepidula (Conklin 1901), and Crypto- 
branchus (Smith 1919) (Fig. 109). This phenomenon is especially evident 
in hybrids (p. 160). There is much reason to believe that the chro- 
matins of the two parents, although intermingled in the nuclei of the 
offspring, never actually fuse, unless it is at the time of synapsis in the 
next maturation; and it has already been pointed out (Chapter XI) that 
they may not fuse even then. This fact also has an important bearing on 
the chromosome theory of heredity. 

The Centrosome (See Wilson 1900, pp. 208 ff.) Shortly after the 
entrance of the spermatozoon into the egg (Figs. 106-108) an aster devel- 
ops at the base of the sperm head, and in the aster a centrosome appears. 
Since the centrosome thus arises in the position of the middle piece, and 
since the centrosome of the spermatid is included in the middle piece dur- 
ing spermatogenesis, a widely accepted theory has been that the newly 
appearing centrosome is in reality that of the spermatid. Whatever its 
origin, it soon divides to form the two which function in the first cleavage 
mitosis. These facts had much to do with the formulation of a theory of 
fertilization set forth by Boveri (1887, 1891), who was much impressed by 
the conspicuous part played by the centrosomes in cell-division. Accord- 
ing to Boveri's theory 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. This theory has recently been recalled 
by Walton (1918) in his work on Ascaris canis. 

Another early view of the origin of the cleavage centrosomes was that 
of van Beneden (1887) and Wheeler (1895, 1897), who believed them to be 
the centrosomes of the egg cell. 

The theory that the cleavage centrosomes arise from both egg and 
spermatozoon is of some historic interest. It was suggested by Rabl 


(1889) that if the centrosome is a permanent cell organ the conjugation of 
the gametes must involve not only a union of nuclei but also a union of 
centrosomes (Wilson, p. 210). Fol (1891), in his work on echinoderm 
eggs, thought that he observed just such a process, which he termed "The 
Quadrille of the Centers." The egg centrosome and the centrosome 
brought in by the spermatozoon were both supposed to divide, the prod- 
ucts then fusing in pairs to form the two cleavage centrosomes. A simi- 
lar thing was reported by certain other investigators, but none of the cases 
stood the test of later work. Another theory now abandoned was that 
advanced by Carnoy and Lebrun (1897), who also attempted to derive one 
centrosome from each gamete. The cleavage centrosomes were thought 
to arise de novo and separately, one inside each pronucleus, to migrate 
thence into the cytoplasm. 

Much less confidence is now placed in the persistence of the spermatid 
or egg centrosomes through the fertilization stages. Since the middle 
piece, which is thought to contain the centrosome, does not enter the egg 
at all in Nereis, it seems probable that the male nucleus in some way 
induces the formation of asters and centrosomes by the egg cytoplasm. 
Lillie found that even a portion of the sperm head will bring about this 
effect. In Unio (Lillie 1897, 1898) and Crepidula (Conklin 1897) it seems 
not unlikely that each pronucleus causes the formation of one cleavage 
centrosome. In the sea urchin Wilson (1901) concluded that the cleav- 
age centrosomes in all probability arise by the division of one which orig- 
inates de novo at the nuclear membrane. In almost every case there are 
gaps in the known history of the centrosome in fertilization, and it seems 
very doubtful whether the cleavage centrosomes are continuous with 
those of either gamete. This conclusion is supported by the fact that the 
formation of asters with centrosomes in the egg cytoplasm can be arti- 
ficially induced by treating the eggs with certain chemicals, such as weak 
MgCU. It is possible that the spermatozoon carries a substance which 
brings about centrosome formation in a similar way. However this may 
be, the importance of the centrosome undoubtedly lies in its relation to 
cleavage rather than to fertilization. 

Cytoplasm and Chondriosomes. In some cases (Nereis} no cytoplasm 
can be shown to enter the egg with the spermatozoon, whereas in others 
(Ascaris) a relatively large amount is brought in. Its great indefiniteness 
in behavior makes it seem probable that it has no special significance in 
the fertilization process. 

The importance of the chondriosomes in fertilization has been empha- 
sized by Meves (1911, 1915), who finds that many of these bodies are 
present in the large cytoplasmic mass accompanying the sperm nucleus 
in Ascaris, and that they mingle with the chondriosomes of the egg. 
Meves (1908, 1915, 1918), together with other writers, accordingly thinks 
that they are concerned in the transmission of certain hereditary char- 


fatty acid (butyric, propionic, or valerianic;, ana men back into pure 
sea water: the membrane then forms by a cytolysis of the cortical layer 
of the egg. Although in some forms (starfish) this one treatment is 
sufficient to bring about successful development, in most cases (sea 
urchin) the eggs become sickly and die. Loeb found that this sickli- 
ness may be prevented, allowing normal development, by either of two 
second treatments. If, after membrane formation, the eggs are placed 
for 20 minutes in hypertonic sea water or other solution with an osmotic 
pressure 50 per cent above that of ordinary sea water, they will develop 
normally when returned to pure sea water. The same effect may be 
brought about, though not always so successfully, by placing the eggs 
for 3 hours in sea water free from oxygen, or into sea water with a trace 
of KCN. It is therefore concluded by Loeb that the stimulus to such 
parthenogenetic development has two phases: the inducement of mem- 
brane formation by cytolysis, and the subsequent effect of the hyper- 
tonic solution. In rare cases the first treatment alone is sufficient for 
normal development, but in all cases it at least starts the egg into activity. 
As a result of these experiments Loeb has interpreted the action of the 
spermatozoon in normal fertilization on the assumption that it carries 
two substances: first, a lysin which brings about membrane formation 
by cytolysing the cortical layer of the egg, and which can act even if 
the spermatozoon does not enter the egg; and second, a substance which 
produces an effect similar to that of the hypertonic sea water employed 
in the experiments. The quite different explanation offered by Lillie 
will be mentioned further on. 

How it is that cytolysis of the cortical layer of the egg brings about 
activation Loeb attempts to explain in the following manner. A calcium 
lipoid compound forms a continuous layer just beneath the surface of the 
egg, and the solution of this layer would probably result in the destruc- 
tion of the cortical emulsion. It is assumed that in this cortical region 
there is a catalytic agent which increases the metabolism (rate of oxida- 
tion, etc.) of the egg. Following Warburg (1914) Loeb suggests that the 
cytolysis releases the catalyzer by breaking down the cortical emulsion; 
this results in an increase in the rate of oxidation and other reactions, and 
development proceeds. 

That the process of activation is bound up primarily with reactions 
occurring in the cortical region of the egg is shown further by the experi- 
ments of Guyer (1907), Herlant (1913, 1917), McClendon (1912), Loeb 
and Bancroft (1913), and particularly Bataillon (1910), who have shown 
that the egg of the frog may be made to develop by pricking it with a 
needle, especially if some blood enters the egg with it; and also by the 
researches of R. S. Lillie (1908, 1915), who finds that starfish eggs may 
be made to develop parthenogenetically by exposing them to high 
temperatures for definite periods. (See F. R. Lillie, 1919, Chapter VII.) 


Heilbrunn (1920) shows that the egg of Cumingia can be induced to 
undergo maturation by agencies which release the fluid cytoplasm from 
the restraint of the tough vitelline membrane. If the membrane be 
swollen, elevated above the egg surface, ruptured, or removed the 
maturation changes begin at once. 

The sickliness and death of those eggs given only the first treatment 
Loeb thought to be due to the continued action of the cytolytic agent. 
Against this conception it is urged by F. R. Lillie that since any activated 
egg not developing normally cytolyzes sooner or later from internal causes, 
it is more probable that the sickliness and death are due to some internal 
cause resulting from activation, and points out that such a conclusion is 
supported by the cytological phenomena in eggs activated by Loeb's 
method. To these phenomena we may turn for a moment. 

Eggs which have been given the first treatment alone do not begin to 
disorganize for many (12 to 24) hours. During this period Herlant (1917) 
has observed the following events. After the formation of the mem- 
brane and a hyaline zone, alterations cease, and the nucleus becomes the 
seat of a series of conspicuous changes. The nuclear membrane dissolves, 
and around the chromosomes there is formed a monaster (one-poled 
group of achromatic fibers), but no amphiaster develops. The chromo- 
somes divide but do not separate, and although the cytoplasm becomes 
active no cytokinesis ensues. The chromosomes then return to the 
resting 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 
(Loeb's method) in some way gives the egg the capacity to divide regu- 
larly. Morgan (1899) and Wilson had long before shown that such 
treatment with hypertonic sea water causes aster formation in the 
unfertilized sea urchin egg. Herlant shows that one of these asters and a 
second aster formed in connection with the egg nucleus together form an 
amphiaster, normal division then ensuing. 

In the light of these facts it seems evident that the death of the egg 
after the first treatment alone is not due to the continued action of the 
cytolytic agent employed, but rather to irregularities in the activation 
processes aroused by the cortical changes in the absence of a proper 
coordination of nuclear and cell division. The second treatment pro- 
duces a regulatory effect, partly through aster formation, resulting in 
normal development. This recalls Boveri's morphological theory of 
normal fertilization. 

Direct Analysis of the Fertilization Process. In contrast to the theory 
that the spermatozoon contributes organs (Boveri) or substances (Loeb) 
necessary for the activation, Lillie (1919, Chapter VII) regards the egg 
itself as an "independently activable system/' "The egg possesses all 
substances needed for activation; the spermatozoon is an inciting cause 


of those reactions within the egg system upon which development 
depends.". As a result of his direct analysis of the gametes during the 
fertilization period Lillie has identified a substance in the egg which he 
calls fertilizin. This substance is present in the egg for a short time 
only; its formation usually begins at about the time the germinal vesicle 
begins to break down, and immediately after fertilization its production 
ceases, possibly through the neutralizing action of a second substance, 
called "anti-fertilizin." As a rule it is only during the period at which 
fertilizin is present that spermatozoa will enter the egg; the egg re- 
mains fertilizable for but a short time. Hence it seems clear that it is 
not the fertilization membrane that prevents the entrance of other 
spermatozoa, as Fol thought, but rather the physiological state of the egg. 
That the protection is thus a physiological rather than a mechanical 
one is indicated by the fact that membraneless egg fragments without 
fertilizin are not entered by spermatozoa. 

Fertilizin has two effects: it first acts by causing an agglutination 
of the spermatozoa at the surface of the egg, and later causes the activa- 
tion 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 secre- 
tion at a certain period it binds the spermatozoon to the surface of the egg, 
and the spermatozoon, without necessarily penetrating the egg at all, 
by means of a substance which it bears releases tfre activity of the 
fertilizin within the egg, which results 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 sperm- 
atozoon, but by other agencies as well. 

In concluding this sketch of the physiological features of fertiliza- 
tion we may. state briefly the immediate physiological consequences of the 
process as summarized by Lillie (1919, Chapter V). The rate of oxida- 
tion increases in most cases in which it has been investigated. In the sea 
urchin egg (Warburg 1908-1914) this rate increases as much as six- or 
seven-fold; in Strongylocentrotus, four- or five-fold (Loeb and Wasteneys, 
1912, 1913); in the starfish, apparently not at all. The egg membrane 
becomes more permeable to oxygen, C02, pigment, water, alkalis, intra- 
vitam stains, and a number of other substances. The protoplasm be- 
comes less fluid after fertilization (Heilbrunn 1915). This gelation effect 
Chambers (1917) believes to center upon the sperm aster. The volume 
of the egg decreases and its electrical conductivity rises. The most 
conspicuous chemical change is seen in the loss of the fertilizin, and with 
it the loss of capacity for further fertilization reaction. 


Although the central act of the process of fertilization is regularly 
the union of two sexually differentiated nuclei, the morphological 



features associated with this fusion are more varied in plants than in 
animals. This is especially true of the algae and fungi. 

Algae. In Ulothrix fertilization consists in the complete union of 
two, morphologically similar, motile biciliate gametes (Fig. 114, A). 
In Fucus the two gametes are very dissimilar: the male (spermatozoid) is 
small, laterally biciliate, and actively motile (Fig. 114, J5), while the 
female (egg), though discharged from the oogonium, is large and passive, 
as in all higher plants and animals. In (Edogonium (Fig. 114, D, E) the 

FIG. 114. Spermatozoids of plants. 

A, Ulothrix: 1, gamete; 2, gametes fusing (isogamy) ; 3, zygospore. B, Fucus. (After 
Guignard.) C, Zamia. (After Webber.) D, bit of filament of (Edogonium; spermatozoids 
escaping from antheridial cells below; spermatozoid about to enter egg above. (After 
Coulter.) E, spermatozoid of (Edogonium. F, Chara. (After Belajeff.) G, Onoclea. 
(After Steil.) For figures of spermatozoids of Blasia, Potytrichum, Equisetum, and Marsilia, 
see Figs. 28, 29, 30, and 32. 

egg is not shed from the cell which produces it, but is fertilized in situ, 
a condition which is retained in all the higher plant groups. The sperm- 
atozoid in this genus has a crown-like ring of cilia. In Spirogyra (and 
other Conjugate) certain vegetative cells, without further morphological 
differentiation, function as gametes. The entire contents of such ti cell 
pass through a conjugation tube to a similar cell in an adjacent filament, 
where the two unite to form the zygospere. The two nuclei fuse, but the 
chloroplasts furnished by the contributing ("male") gamete may event- 
ually degenerate (Zygnema). In Polysiphonia a non-motile male gamete 



(spermatium) comes in contact with a prolongation (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. In Polysiphonia we 
have one of the few cases among lower plants in which the fusion of the 
sexual nuclei has been minutely described. According to Yamanouchi 
(1906) the male nucleus, by the time it has reached the female nucleus, 
has resolved itself into a group of 20 chromosomes (Fig. 115, A). In this 

Fio. 115. 

A t fertilization in Polysiphonia. Group of male chromosomes about to enter female 
nucleus. (After Yamanouchi, 1906.) B, fertilization in Albugo Candida. Female nucleus 
lying in center of ooplasm near the " ccenocentrum " (larger dark body.) Antheridial tube 
about to discharge a male nucleus; another male nucleus in neck of tube. Additional nuclei 
in periplasm surrounding the ooplasm. (After Davis, 1900.) 

condition it enters the female nucleus while the latter is yet in the reticu- 
late state. Soon the female reticulum becomes transformed into 20 
chromosomes, which arrange themselves with the 20 paternal chromo- 
somes upon the spindle as the fusion nucleus divides. 

Fungi. In the PHYCOMYCETES sexual reproduction occurs in two princi- 
pal forms, which serve to divide the group into two main divisions: 
Oomycetes and Zygomycetes. 

In the Oomycetes the cytological phenomena are best known in the 
Peronosporales and Saprolegniales. In the former there is differentiated 
in the oogonium a single large egg into which the contents of an antheri- 
dium are discharged through a penetrating tube. In Albugo bliti and 
A. portulaccoe (Stevens 1899, 1901) the egg has a large number of nuclei, 



and after the entrance of the antheridial nuclei about 100 sexual fusions 
occur. In t Albugo Candida (Cystopus candidus) (Wager 1896; Davis 
1900), Peronospora parasitica (Wager 1900), Albugo tragopogonis and 
A. ipomceae (Stevens 1901) the mature egg has but one nucleus, which 
fuses with a single male nucleus discharged into the egg by an antheridium 
(Fig. 115, B). In all cases an oospore results. 

In the Saprolegniales, as shown by the researches of Davis (1903, 
1905), Miyake (1901), Trow (1895-1905), and Claussen (1908), there are 
two general conditions. In Saprolegnia (Trow, Davis, Claussen) from 
10 to 15 uninucleate eggs are formed within an oogonium. One or more 
antheridia send in conjugating tubes and deliver a male nucleus to each 
egg, in which a single sexual fusion then occurs. In Pythium (Trow 1901 ; 
Miyake 1901) a single uninucleate egg is produced, the fertilization 
process closely resembling that in Albugo Candida. 

In the Zygomycetes, represented chiefly by the Mucoracese, the sexual 
process consists in the union of the contents of two similar (except oc 
casionally in size) multinucleate gametangia, the result of the fusion 
being a zygospore. As shown by Blakeslee (1904) these two gametangia 
are borne on the same mycelium in some species ("homothallic" species), 
whereas in other species ("heterothallic" species) they are regularly 
borne on different mycelia, no zygospores being formed in the latter spe- 
cies on a mycelium arising from a single spore. Owing to the extremely 
minute size of the nuclei their behavior at these stages is not well known. 
By some investigators (Macormick on Rhizopus nigricans, 1912) it is 
held that only one fusion occurs, the remaining nuclei degenerating. 
Others (Keene on Sporodinia grandis, 1914) think it probable that al- 
though some degeneration occurs, the nuclei nevertheless fuse in pairs 
in considerable numbers. Until further researches have been carried out 
very little of a definite nature can be said concerning the nuclear history 
of the Zygomycetes. 

In the ASCOMYCETES (see Atkinson 1915) the fusion of two nuclei 
in the ascus was first described for several species by Dangeard (1894) 
(Fig. 116, A), who regarded it as a sexual fusion and the ascus as an oogo- 
nium. The matter soon became complicated when a number of cytolo- 
gists, beginning with Harper (1895 etc.), found what they believed to be 
a nuclear fusion at an earlier stage in the life cycle. This fusion was 
described as occurring (a) in the archicarp when fertilized by the contents 
of an antheridium (Harper on Sphcerotheca castagnei, 1895, 1896, Erisiphe 
1896, Pyronema confluens 1900, and Phyllactinia 1905; Blackman and Fra- 
ser on Sphcerotheca 1905; Claussen on Boudiera 1905); (6) in the archicarp 
when the antheridium is functionless or absent (Blackman and Fraser 
on Humaria granulata 1906; Fraser on Lachnea stercorea 1907; Welsford 
on Ascobolus furfuraceus 1907; Dale on Aspergillus repens 1909); or (c) 
in the vegetative cells when the archicarp is functionless or absent (Fraser 



on Humaria rutilans 1907, 1908; Carruthers on Helvetia crispa 1911; 
Blackman and Welsford on Poly stigma rubrum 1912). By the above 
investigators this early fusion was regarded as a sexual one, that in the 
ascus being vegetative in nature; and some described a "double reduc- 
tion " in the ascus to compensate for the two nuclear fusions. (See 
p. 223.) 

In a series of somewhat later researches another group of observers 
found the evidence for an early fusion to be very unsatisfactory, and 
concluded that the only nuclear union in the life cycle is that occurring 
in the ascus : with Dangeard they saw in this union the sexual act. Fur- 
thermore, no " double reduction " was found in the ascus. Among the 
researches supporting this view, which now appears to be the more 
probable, may be cited the following: Claussen on Pyronema confluens 

FIG. 116. 

A, nuclear fusion in the ascus of Peziza vesiculosa. (After Dangeand, 1894.) 
fusion in aeciospore sorus of Phragmidium speciosum. After Christman, 1905.) 

B, cell 

1907, 1912; Schikorra on Monascus 1909; W. H. Brown on Pyronema 
confluens 1909, Lachnea scutellata 1911, and Leotia 1910; Faull on Lab- 
oulbenia 1911, 1912; Blackman on Collema pulposum 1913; Nienburg on 
Poly stigma rubrum 1914; Ramlow on Ascophanus carneus and Ascobolus 
immersus 1914; Brooks on Gnomonia erythrostoma 1910; McCubbin on 
Helvetia elastica 1910; H. B. Brown on Xylaria tentaculata 1913; and Fitz- 
patrick on Rhizina undulata 1918a. 

As the two nuclei fuse in the young ascus Harper (1905) observed in 
the case of Phyllactinia corylea that not only the chromatin systems but 
also the nucle6li and "central bodies" (centrosomes), upon which the 
chromatin strands converge, unite. In the Ascomycetes generally the 
fusion nucleus, or "primary ascus nucleus, " undergoes three successive 
mitoses to form the eight ascospore nuclei, the spore walls in each case 
being formed in association with the curving astral rays which focus upon 
the centrosome. (See p. 80.) 


In certain yeasts it has been shown (see Guilliermond 1920) that the 
production of ascospores is preceded by a copulation of two cells with a 
fusion of their nuclei, the fusion nucleus dividing to form the spore nuclei. 
A somewhat similar copulation of the ascospores themselves has also 
been observed in a few cases. 

Among the BASIDIOMYCETES the nuclear phenomena are best known 
in the case of the rusts, owing to the researches of Blackman (1904), 
Christman (1905), and a number of later writers. In the typical rust 
life cycle there is a fusion of uninucleate cells at the base of the aecial 
sorus (Fig. 116, B). The binucleate cells thus arising produce the binu- 
cleate aeciospores; and these upon germination form a mycelium with 
binucleate cells, the two nuclei dividing in unison ("conjugately") at 
each cell-division. After producing a series of crops of binucleate 
uredospores this mycelium eventually bears 'teliospores which may con- 
sist of one or more cells. In each cell of the teliospore the two nuclei 
delivered to it as the result of the conjugate divisions throughout the 
binucleate mycelium finally unite, initiating the uninucleate phase of 
the life cycle. Here the fusion of sexual cells and the fusion of their 
nnclei two events which in most organisms occur very near each other 
in time are widely separated in the cycle. The two nuclei dividing 
conjugately constitute together a synkaryon in many respects ecjuivaleng 
to a diploid nucleus. Since there is as yet no evidence to show in what 
degree the two effects of fertilization (the stimulus to development and the 
mixing of hereditary lines) are brought about in the rusts by the fusion 
of the sexual cells on the one hand and by the final union of their nuclei 
on the other, it seems best to regard the two fusions as two phases of the 
fertilization process in spite of their wide separation in the life history. 

In the Hymenomycetes it has been known for some time that a fusion 
of two nuclei occurs in the basidium, itself the terminal cell of a binucleate 
hypha, prior to the formation of the four basidiospore nuclei (Fig. 79). 
The origin of the binucleate condition in the mycelium which has ap- 
parently arisen from a uninucleate spore has long been an obscure point. 
It has recently been shown by Miss Bensaude (1918) in the case of 
Coprinus fimetarius that the binucleate hyphse arise as the result of cell 
fusions ("plasmogamy;" "pseudogamy") between uninucleate hyphse 
arising from different spires, and that no carpophores are produced upon 
a uninucleate mycelium arising from a single spore. Thus it appears 
that in at least some hymenomycetes the sexual process is initiated by a 
fusion of two cells of different strains ("plus" and "minus"), as in the 
heterothallic molds. 

Bryophytes and Pteridophytes. In bryophytes and pteridophytes 
the details of the union of the motile spermatozoid with the egg in the 
archegonium have been described in very few cases. In the former 
group may be cited the works of Garber (1904) and Black (1913) on 



Riccia, Meyer (1911) on Comma, Graham (1918) on Preissia, and 
Woodburn (1920) on Reboulia. It appears that in bryophytes the body 
of the biciliate spermatozoid, which consists mainly of nuclear material, 
undergoes in the egg cytoplasm a transformation into a reticulate nucleus 
before fusing with the egg nucleus (Fig. 117). The fate of the non- 
nuclear structures (cytoplasm, blepharoplast, and cilia) is not known 
with certainty, but it is probable that they are absorbed in the egg cyto- 
plasm. In the liverwort, Preissia 
quadrata, Miss Graham has found 
two centrosomes with weakly de- 
veloped asters in the cytoplasm of 
the egg at the time the two pronuclei 
are about to fuse (Fig. 23, A). It is 
not known what relation their ap- 
pearance may have to the entrance 
of the 'spermatozoid. 

The most detailed account of fer- 
tilization in a pteridophyte is that 
given by Yamanouchi. (1908) for 

FIG. 117. FIG. 118. 

FIG. 117. Fertilization in Anthoceros. Male and female pronuclei about to fuse in 
lower part of egg in venter of archegonium; elongated plastid above them. Gametophyte 
cells show one nucleus and one plastid each. X 1050. 

FIG. 118. Fertilization in Nephrodium. 

A, spermatozoid entering egg nucleus. B, spermatozoid becoming reticulate in midst 
of female reticulum. (After Yamanouchi, 1908.) ^ 

Nephrodium (Fig. 118). In Nephrodium tfye multiciliate spermatozoid 
enters bodily into the egg nucleus with no previous alteration into the 
reticulate state. Here it gradually becomes reticulate and irregular in 
shape, until finally its limits are indistinguishable, the chromatic material 
contributed by the two gametes apparently forming a single fine-meshed 

Gymnosperms. Among living gymnosperms the Cycadales and 
Ginkgoales are characterized by the possession of motile spermatozoids. 



These spermatozoids are very much alike in structure and behavior in 
the two groups, and are unusually large, being easily visible to the naked 
eye. The body is made up of a large nucleus surrounded by a thin 
cytoplasmic layer in which is imbedded a long, spirally coiled blepharo- 
plast bearing many cilia (Fig. 114, C). The behavior of the spermatozoid 
in fertilization has been studied in Girikgo by Hirase (1895, 1918) and 
Ikeno (1901); in Cycas revoluta by Ikeno (1898); in Zamiafloridanaby 
Webber (1901); and in Dioon edule, Ceratozamia mexicana, and Stangeria 

paradoxa by Chamberlain (1910, 1912, 1916). 
In all cases the entire spermatozoid penetrates 
into the egg cytoplasm, where the nucleus frees 
itself from the cytoplasmic sheath with its 
blepharoplast and cilia and advances alone to 
the egg nucleus, with which it fuses (Fig. 119). 
The behavior of the chromatin during the fusion 
is not well known in either Ginkgo or the cycads. 
In the Coniferales and Gnetales the male 
cells have no motile apparatus. Each consists 
of a nucleus surrounded by a more or less 
sharply delimited mass of cytoplasm. In most 
cases this cytoplasm remains intact until after 
the male cell has entered the egg, but in other 
forms, such as Pinus, it mingles with the cyto- 
plasm 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 dis- 
charged into the egg. All but the' functioning 
male nucleus usually degenerate at once, but in 
some cases they have been observed to undergo 

When a complete male cell enters the egg the cytoplasm of the former 
shows two general modes of behavior. In some species it may be left 
behind in the peripheral region of the egg as the male nucleus frees itself 
and advances alone to the female nucleus. This type of behavior has 
been reported in Pinus (Ferguson 1901, 1904), Thuja (Land 1902), 
Juniperus (Nor6n 1904), Cryptomeria (Lawson 1904), and Libocedrus 
(Lawson 1907). In Sequoia (Lawson 1904) the male nuclei escape from 
their cytoplasm before their discharge from the pollen tube, and enter 
the egg alone. In a second group of species the male cytoplasm remains 
intact and invests the fusing sexual nuclei, being clearly distinguishable 
from the cytoplasm of the egg. The pollen tube cytoplasm often plays 

FIG. 119. Fertilization 
in Zamia. Male nucleus 
uniting with egg nucleus at 
center ; cy toplasmicjsheath 
with spiral blepharoplast 
above. Another sperm 
outside egg. X 25. (After 
Webber, 1901.) 



a conspicuous part in the formation of this "mantle." This phenomenon, 
the significance of which can only be conjectured, is found in Taxodium 
(Coker 1903), Torreya calif ornica (Robertson 1904), Torreya taxifolia 
(Coulter and Land 1905), Cephalotaxus Fortunei (Coker 1907), Ephedra 
(Berridge and Sanday 1907; Land 1907), Phyllocladus (Kildahl 1908), 
Juniperus (Nichols 1910), Agathis (Eames 1913), and Taxus (Dupler 

Chromosome Behavior. The behavior of the chromosomes during 
the fusion of the sexual nuclei and the first embryonal division has 
been described in a number of conifers. As a general rule, to judge from 
the data at hand, the chromatin contributions of the two pronuclei do 
not become intimately associated in the fusion nucleus, but remain 
distinguishable until the first embryonal mitosis occurs. Each of the 
pronuclei then gives rise to its complement of chromosomes which 

FIG. 120 Fertilization in Finns. 

A, male nucleus pressing into female nucleus. X 140. B, first embryonal mitosis, 
showing separate paternal and maternal chromosome groups. X 472. (After Ferguson, 

become arranged, often as two separate groups, upon a common 
spindle. Such an independent formation of the male and female 
chromosome groups has been observed in Pinus (Blackman 1898; Cham- 
berlain 1899; Ferguson 1909, 1904) (Fig. 120), Larix (Woyciki 1899), 
Tsuga candensis (Murrill 1900), Juniperus communis (Norn 1907), 
Cunninghamia (Miyake 1910), and Abies (Hutchinson 1915). In 
Sequoia, on the other hand, Lawson (1904) reports that the two nuclei 
form a common reticulum in which the male and female constituents 
cannot be distinguished. With regard to the first embryonal mitosis 
the general opinion has been that all the chromosomes, paternal and 
maternal, split longitudinally, the daughter chromosomes being distri- 
buted to the daughter nuclei as in any other somatic mitosis. This 
type of behavior was described for the chromosomes of Pinus by Miss 
Ferguson (1904) and at once came to be regarded as general for coni- 
fers, as it had been for other organisms. 

A new interpretation differing in certain fundamental points from the 
above has been more recently suggested by Hutchinson (1915), as a result 



of his work on Abies balsamea. According to Hutchinson (Fig. 121) 
there appear in the fusion nucleus two groups of chromosomes, each 
containing the haploid number (16). A spindle is differentiated about 
each group; and the two spindles soon unite to form one, thus bringing 
the two chromosome groups, representing the two parental contributions, 
into closer association. The chromosomes now approximate two by two 
to form 16 pairs. The members of each pair twist about each other and 
become looped; each of them becomes transversely segmented at the 
apex of the loop, forming 32 (2x) pairs of segments; these pairs separate 
to form 64 (4x) chromosomes; a new spindle is formed and 32 (2x) 
chromosomes pass to each pole. 



cnwo NUCUI 

FIG. 121. The behavior of the chromosomes in fertilization and the first embryonal mitosis 
in Abies, according to Hutchinson. (1915.) 

This interpretation of chromosome behavior at fertilization is remark- 
able not only because it indicates features resembling those of the hetero- 
typic prophase, but chiefly because it actually calls for a qualitative 
reduction of the chromatin at the first embryonal mitosis if the chroma- 
tin is not qualitatively the same throughout the nucleus. This impli- 
cation has not been discussed by the advocates of the new theory. The 
chromosomes pair and twist about one another in a way that parallels 
closely their behavior during the prophase of a reduction division. That 
the doubleness seen is due to a pairing and not to a splitting as has 
heretofore been held is supported by the assertion that the pairs are 
present in the haploid number, rather than in the diploid number as 
would be the case were a splitting of all the chromosomes occurring. If 
the two members of each pair were to separate at the first embryonal 



mitosis, a reduction, qualitative as well as numerical, in all respects 
similar to that accomplished in the regular heterotypic mitosis, would 
be brought about if the pairing members are qualitatively different. 
But instead of such a separation, each member of each pair segments 
transversely, giving 4x segments which are equally distributed to the two 
daughter nuclei, each of the latter receiving the diploid number. Since 
the 4x segments become more or less intermingled before their distri- 
bution it is probably impossible to determine just which ones pass to 
each pole. If both halves of one transversely divided chromosome pass 
to one pole (see Fig. 122), that daughter nucleus only, and not the other, 
will receive the kind of chromatin carried by that chromosome, so that 






FIG. 122. Diagram showing the behavior of the chromosomes in fertilization and the 
first embryonal mitosis as usually interpreted (upper part) and according to Hutchinson's 
interpretation (lower part). 

the two nuclei will be qualitatively different. A qualitative reduction 
will have occurred, but without a change in the number of chromosomes, 
since each old chromosome has become two new ones. If, on the other 
hand, the two halves of the transversely segmented chromosome regularly 
pass to opposite poles, each daughter nucleus will receive a half of each 
and every parental chromosome: thus if there are just as many kinds of 
chromatin as there are chromosomes, these nuclei will be qualitatively 
alike, just as they would be had the division been longitudinal instead of 
transverse. But, as has been stated in the chapter on reduction and will 
be developed at greater length in Chapter XVII, there is a considerable 
body of evidence which indicates that each chromosome is not only 
qualitatively different from its fellows, but possesses a linear differen- 


tiation of some sort; so that the separation of the two halves of a trans- 
versely divided chromosme would constitute a qualitative reduction. 
If such actually is the condition of the chromatin, and if the chromosomes 
do behave as Hutchinson supposes, a qualitative reduction must immedi- 
ately follow each fertilization, and half of the resulting body cells must 
have a constitution differing from that of the other half. Since there are 
known no chromosome fusions in which a restoration in the number of 
qualities is known to occur, the number of these qualities in a single 
chromosome would in a few generations be reduced to one: in view of 
the large number of past generations this must have already occurred. 

This new interpretation of chromosome behavior at fertilization and 
the ensuing mitosis is thus seen to offer a direct challenge to those 
theories of heredity that are based upon the idea of chromosomes carry- 
ing linear series of differentiated units. It has now been put forward by 
Hutchinson (1915) for Abies balsamea, by Chamberlain (1916) for 
Stangeria paradoxa, and by Miss Weniger (1918) for Lilium philadel- 
phicum and L. longiflorum. Consequently several investigators have 
renewed the study of fertilization, and evidence contradictory to the 
new theory has been found by Miss Nothnagel (1918) and Sax (1918), 
whose researches are summarized in the following section on the 

Angiosperms. The angiosperms are characterized by the occurrence 
of "double fertilization/' a phenomenon discovered independently by 
Nawaschin (1898) and Guignard (1899). One of the two male nuclei 
formed by the male gametophyte and brought into the embryo sac by 
the pollen tube, enters the egg and fuses with its nucleus, thus forming 
the primary nucleus of the embryo, while the other male nucleus, fuses 
with the two polar nuclei to form the primary endosperm nucleus (Fig. 
123, B). As the male nuclei pass down the pollen tube they are usually 
unaccompanied by any specially differentiated cytoplasm: the male 
gametes are naked nuclei and not complete cells. In some cases, how- 
ever, male cells have been reported (Fig. 123, A). When they are 
liberated in the embryo sac by the rupture of the end of the pollen tube 
any such cytoplasm is indistinguishable from that of the sac and that 
discharged from the pollen tube. The male nuclei may appear in all 
respects similar to other nuclei, or they may be distinctly vermiform, 
as was observed by Mottier (1898) and later by many other workers 
(Fig. 123, E). That such vermiform nuclei have the power of inde- 
pendent movement has been held by Nawaschin (1899, 1900, 1909, 
1910) for Lilium and Fritillaria, by Guignard (1900) for Tulipa, and by 
Blackman and Welsford (1913) and Miss Welsford (1914) for Lilium 
Martagon and L. auratum. The vermiform condition may persist until 
the time of fusion, but in other cases, such as Fritillaria (Sax 1916), it 
gives way to the ordinary shape. This change may occur more rapidly 



in one male nucleus than in the other, so that the two may appear quite 
unlike during the later stages. Miss Welsford also sees in the male 
cytoplasm certain granules which she thinks may represent the vestiges 
of blepharoplasts. 


FIG. 123. Fertilization in angiospcrms. 

A, end of pollen tube from basal portion of style of Lilium auratum, showing two male 
cells and tube nucleus. X 250. (After Welsford, 1914.) B, double fertilization in Lilium 
canadense: male and female nuclei about to fuse in egg; second male and two polar nuclei 
fusing at center of embryo sac; s, synergids, one degenerated; a, antipodals X 250. 
C, fusion of sexual nuclei in egg of Lilium philadelphicum. X 1000. (After Weniger, 
1918.) />, the second male and two polar nuclei in Lilium Martagon. X 750. (After 
Nothnagel, 1918.) E, vermiform male nucleus in contact with egg nucleus in Triticum 
durum. X 600. (After Sax, 1918.) F, spireme stage of triple fusion nucleus in Triticum 
durum, showing distinctness of three chromatin contributions. X 750. (After Sax, 1918.) 
(r, inclusion of cytoplasm in fusing sexual nuclei of Peperomia sintenesii. (After Brown, 

Fusion in Egg. As already stated, one male nucleus passes into 
the egg and fuses with the egg nucleus. So far as observations enable 
one to say, only the male nucleus, and no cytoplasm, enters the egg, a 
point of much importance in connection with the transmission of heredi- 
tary characters from the male parent. It would be a matter of extreme 
difficulty, however, to demonstrate conclusively that in passing through 
the egg membrane the male nucleus is absolutely freed of all adhering 
cytoplasm or chondriosomes; and it must be admitted that such a 
demonstration has not yet been given in any case. The fusion of the two 
sexual nuclei probably occurs in most cases very soon after they come 
in contact, though in certain forms the actual fusion is known to be 


considerably delayed. The chromatin of the two nuclei at the time 
these unite may be in the reticulate (resting) condition, the male and 
female chromatins being indistinguishable in the fusion nucleus. This 
situation was described by most of the earlier workers, including Stras- 
burger (1900, 1901), Mottier (1904), Nawaschin (1898, 1899), and Ernst 
(1902). It has also been reported by Sax (1916) in his recent work on 
Fritillaria. In other cases, as early reported by Guignard (1891), the 
chromatin has already reached the spireme stage characteristic of the 
prophase, the male and female elements being distinguishable on the 
spindle in the ensuing division of the fertilized egg. Such is the condi- 
tion, for instance, in C&lopogon (Pace 1909), Trillium (Nothnagel 1918), 
and Lilium (Weniger 1918). That the same species may show con- 
siderable variation in this respect is indicated by the situation in 
Fritillaria, in which Sax (1916, 1918) finds that fusion, though it usually 
occurs in the resting stage, sometimes takes place after the spiremes 
have been developed. Miss Weniger (1918) reports that in Lilium 
philadelphicum and L. longiflorum the egg nucleus is in the resting con- 
dition and the male nucleus in the spireme stage at the time of union. 

Chromosome Behavior. With regard to the behavior of the two par- 
ental groups of chromosomes, it has been generally held that, whatever 

th pater- 

of. HIP f,j|pp of fhp nqfilftar ^i^ all of them, both pater 
nal and maternal, split longitudinally at the first division of thefe^r- 
tilized egg, the daughter chromosomes so formed being distributedto 
the two"T-esulting nuclei, just as in all the subsequent somatic divisions. 
Recently, however, Miss Weniger (1918) has reported a condition in 
Lilium similar to that described by Hutchinson (1915) for Abies: the 
maternal and paternal chromosomes form pairs and divide transversely 
into daughter segments which pass to the poles* (See p. 296.) With 
this conclusion other recent investigations of fertilization in angiosperms 
are not in agreement. Miss Nothnagel (1918) finds in Trillium no such 
pairing and cross segmentation as Hutchinson and Miss Weniger de- 
scribe, and states that each chromosome splits longitudinally as held 
by Miss Ferguson for Pinus and by cytologists in general. Sax (1918) 
also shows that each paternal and maternal chromosome in Fritillaria 
divides longitudinally, the diploid number (24) passing to each pole. 
In Trillium he reports an essentially similar state of affairs, the diploid 
number here being about 28. He therefore holds that the first mitosis 
in the fertilized egg is like any other somatic mitosis, and that no mech- 
anism for the segregation of factors of inheritance, such as occurs at 
reduction, exists here. The outcome of this controversy is awaited with 
much interest because of its great theoretical importance. 

Endosperm Fusion. The fusion of the second male nucleus with 
the two polar nuclei of the embryo sac to form the primary endosperm 
nucleus may be carried out in a variety of ways. The most commonly 


reported method is that by which the two polars fuse to form an "fifli- 
bryo sac nucleus" before the entrance of the pollen tube, the male 
nucleus later being added Ernst (1902), for example, found this to be 
the method in Paris quadrifolia. Less frequently the male nuclei^s 
meets and fuses with the polar nucleus of the micro pylar end of the sacy 
the other polar then fusing with the iprw1 lir>f Tll1 ' g f] ^ mpfhnH de- 
scribed by Nawaschin (1898, 1899) in his account of the discovery of 
double fertilization in Lilium Martagon and Fritillaria tenella. The 
simultaneous fusion of all three nuclei appears to be a common 
Recurrence: it has recently been described in some detail by Miss Noth- 
nagel (1918) for Trillium and Lilium. Just as in the case of the union 
of the first male nucleus with the egg nucleus, the chromatin of the 
second male and two polar nuclei may be either in the reticulate or the 
spireme condition as they come together. In Lilium Martagon (Noth- 
nagel 1918) (Fig. 123, D) it is in the form of fine strands, intermediate 
between the resting and spireme stages. 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 chromatin: in Lilium longiflorum (Weniger 1918), for 
example, the male nucleus is in the spireme stage while the polar nuclei 
are still in the resting condition. The membranes of the three nuclei 
may persist for some time after they come into intimate contact, and 
even after they have dissolved the chromatic elements of the three con- 
stituent nuclei may in many cases be distinguished if the section has 
been made in a favorable plane. When fusion occurs in the resting 
stage this is not so apparent, but when it occurs in the spireme stage 
the three chromatic groups are made out with little difficulty. 

Endosperm. As the division of the endosperm nucleus approaches 
the spiremes of its three constituent nuclei become increasingly dis- 
tinct, even if one or more of the nuclei have fused in the resting stage. 
Nothnagel (1918), Weniger (1918), and Sax (1918) in their recent studies 
all report this condition (Fig. 123, F). As the spiremes are being 
developed into completed chromosomes all of them (3x in number) split 
longitudinally, no observer reporting such a pairing as some have thought 
to occur between the chromosomes of the egg and first male nuclei. 
Miss Nothnagel describes the formation of a tripolar spindle about the 
chromosomes; the bipolar condition soon develops from this. How 
frequently this may occur is not known. Eventually in any case the 
mitosis proceeds along the usual lines and the two daughter nuclei receive 
3x chromosomes each. This number is characteristic of all the cells of 
the endosperm formed by the repeated division of these nuclei. An 
exceptional condition has been noted by Sax (1918) in Fritillaria. 
Here the lower polar nucleus, because of an irregularity in the mitosis 
giving rise to it, has 24 (2x) chromosomes instead of the normal 12 


(x). Consequently the female parent contributes 30 chromosomes (24 in 
one polar nucleus and 12 in the other) to the endosperm, while the male 
parent contributes only 12; thus the endosperm has 48 (4x) chromo- 
somes instead of the normal 36. 

Although in the great majority of known examples endosperm is 
formed by the repeated division of a triple fusion nucleus, cases are known 
in which it is produced by the polar fusion nucleus (embryo sac nucleus) 
alone without the male, or by the fusion product of the male and one 
polar, or by one polar alone. Combinations of these three methods may 
be found in the same embryo sac. The development of the endosperm 
may be initiated by the formation of a number of free nuclei which are 
parietally placed and in later mitoses become separated by walls, or 
by the formation of walled cells from the start. (See Coulter and Cham- 
berlain, 1903.) 

The term xenia was applied by Focke (1881) to the effect of foreign 
pollen on the endosperm of the resulting seed in angiosperms. Thus if 
maize of a certain strain which produces seeds with white endosperm when 
self-pollinated, is pollinated with pollen from a plant whose seeds have 
red endosperm, the endosperm of the resulting hybrid seeds is red like 
that of the pollen parent. No satisfactory explanation of this phenom- 
enon was at hand until the discovery of double fertilization by Nawas- 
chin and Guignard in 1898-9. It then became clear that the endosperm, 
which was formerly supposed to contain only maternal nuclear material, 
may show endosperm characters of the parent furnishing the pollen for the 
reason that the latter contributes a nucleus to the primary endosperm 
nucleus, so that every endosperm cell contains some nuclear material 
from the pollen parent. 

Normally the endosperm cells are all alike in containing two chromo- 
some sets from the female parent and one set from the male, and the nor- 
mal inheritance of endosperm characters as well as all ordinary cases of 
xenia can be understood on this basis. Mottled or mosaic effects in the 
endosperm of maize hybrids were attributed by Webber (1900) to such 
abnormal modes of endosperm origin as were referred to in a foregoing 
paragraph: some of the cells may have been formed by polar nuclei 
of purely maternal constitution while other cells were the result of the 
independent division of the second male nucleus. Although this explana- 
tion may fit some cases, it is becoming apparent from the work of Emerson 
and others that most of them can be better accounted for on the basis of 
aberrant chromosome behavior, such behavior having been observed in 
certain other organisms. 

Additional evidence is found in all these phenomena for the theory 
that the nuclear substance in some way represents the physical basis of 
inheritance. The second male nucleus not only is concerned in the 
initiation of the development of the endosperm, but xenia shows that it 


also transmits parental characters. Here, therefore, as in the sexual 
fusion in the egg, the two principal effects of fertilization may be 

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64: 115-136. pis. 11-14. 
EAMES, A. J. 1913. The morphology of Agathis australis. Ann. Bot. 27: 1-38. 

pis. 1-4. 92 figs. 
ERNST, A. 1902. Chromosomenreduktion, Entwicklung des Embryosackes und 

Befruchtung bei Paris quadrifolia L. und Trillium grandiflorum Salisb. Flora 

91.1-46. pis. 1-6. 
FARMER, J. B. and WILLIAMS, J. L. 1898. Contributions to our knowledge of 

the Fucaceae; their life history and cytology. Phil. Trans. Roy. Soc. London B 

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FAULL, J. H. 1911. The cytology of the Laboulbeniales. Ann. Bot. 25: 649-654. 

1912. The cytology of Laboulbenia chcetophora and L. Gyrinidarum. Ibid. 26: 
325-355. pis. 37-40. 

FERGUSON, M. C. 1901. The development of the pollen tube and the division 
of the generative nucleus in certain species of Pinus. Ann. Bot. 16: 193-223. 
pis. 12-14. 

1904. Contributions to the knowledge of the life history of Pinus. Proc. Wash. 
Acad. Sci. 6 : 1-202. pis. 1-24. 

1913. Included cytoplasm in fertilization. Bot. Gaz. 56: 501-502. 
FITZPATRICK, H. M. 191 8a. Sexuality in Rhizina undutata Fries. Bot. Gaz. 65: 

201-226 pis. 3 4. 
19186. The cytology of Eucronartium muscicola. Am. Jour. Bot. 5: 397-419. 

pis. 30-32. 

FOCKE, W. O. 1881. Die Pflanzen-Mischlinge. Berlin. 
FOL, H. 1891. Die "Centrenquadrille," ein neue Episode aus der Befruchtungs- 

geschichte. Anat. Anz. 6: 266-274. figs. 10. 
FRASER, H. C. I. 1907. On the sexuality and development of the ascocarp of 

Lachnea stercorea Pers. Ann. Bot. 21 : 349-360. pis. 29, 30, 
1908. Contributions to the cytology of Humaria rutilans. Ibid. 22: 35-55. 

pis. 4, 5. 
FRIES, R. E. 1911. Zur Kenntniss der Cy tologie von H ygrophorus conicus. Svensk. 

Bot. Tids. 6: 241-251. pi. 1. 
GARBER, J. F. 1904. The life history of Ricciocarpus natans. Bot. Gaz. 37: 161- 

177. pis. 9, 10. 
GRAHAM, M. 1918. Centrosomes in fertilization stages of Preissia quadrata (Scop.) 

Nees. Ann. Bot. 32 : 415-420. pi. 10. 
GUIGNARD, L. 1899. Sur les antherozoids et la double copulation sexuelle chez les 

ve*ge"taux angiospermes. Comp. Rend. Acad. Sci. Paris 128: 864-871. figs. 19. 

1900. L'appareil sexuel et la double fe*condation dans les Tulipes. Ann. Sci. 
Nat. Bot. VIII 11: 365-387. pis. 9-11. 

1901. La double fe*condation chez les Renonculac6es. Jour. Botanique 16: 
394-408. figs. 16. 

1902. La double f&ondation chez les Solan^es. Ibid. 16 : 145-167. figs. 45. 


GUILLIERMOND, A. 19 10. La sexualite chez les champignons. Bull. Sci. France et 

Belg. 44: 109-196. 

1920. The Yeasts. (Engl. transl. by F. W. Turner.) N. Y. 
GUYER, M. F. 1907. The development of unfertilized frogs' eggs injected with 

blood. Science N. S. 25: 910-911. 
HAECKER, V. 1895. Ueber die Selbstandigkeit der vaterlichen und mutterlichen^ 

Kernbestandtheile wahrend der Embryonalentwicklung von Cyclops. Arch. 

Mikr. Anat. 46: 579-617. pis. 28-30. 

1899. Praxis und Theorie der Zellen- und Befruchtungslehre. 

HARPER, R. A. 1895. Beitrag zur Kenntniss der Kerntheilung und Sporenbildung 

im Ascus. Ber. Deu. Bot. Ges. 13: (67)- (78). pi. 27. 

1896. Ueber das Verhalten der Kerne bei den Fruchten ntwicklung einiger Asco- 
myceten. Jahrb. Wiss. Bot. 29: 655-685. pis. 11, 12. 

1900. Sexual reproduction in Pyronema confluens and the morphology of the 
ascocarp. Ann. Bot. 14: 321-396. pis. 19-21. 

1905. Sexual reproduction and the organization of the nucleus in certain mildews. 

Carnegie Inst. Publ. 37. 
HARVEY, E. N. 1910. Methods of artificial parthenogenesis. Biol. Bull. 18: 

HEILBRUNN, L. V. 1915. Studies in artificial parthenogenesis. 11. Physical 

changes in the egg of Arbada. Biol. Bull. 29: 149-203. 
1920. Studies in artificial parthenogenesis. 111. Cortical changes and the inia- 

tion of maturation in the egg of Cumingia. Biol. Bull. 38: 317-339. 
HERLANT, M. 1913. Le me*chanisme de la parthenoge*ncse esperimentelle. Bull. 

Sci. France et Belg. VII 60: 381-404. 

1917. fitude sur les bases cytologiques du m6canisme de la parthenoge*nese experi- 
mentelle chez les amphibiens. Arch. d. Biol. 28: 505-608. 

HERTWIG, O. 1875. Beitrage zur Kenntniss der Bildung, Befruchtung, und Thei- 

lung des tierischen Eies, I. Morph. Jahrb. 1. 
HIRAS, S. 1895. fitudes sur la f6condation et 1'embryogenie du Ginkgo biloba. 

Jour. Imp. Coll. Sci. Tokyo 8: 307-322. pis. 31, 32. 
1898. fitudes sur la fe*condation et 1'embryogenie du Ginkgo biloba. (Second 

memoire.) Ibid. 12: 103-149. pis. 7-9. 

1918. Further studies on the fertilization and embryogeny in Ginkgo biloba. 
Bot. Mag. Tokyo 32: No. 378. 

HOYT, W. D. 1910. Physiological aspects of fertilization and hybridization in 

ferns. Bot. Gaz. 49 : 340-370. figs. 12. 
HUTCHINSON, A. H. 1915. Fertilization in Abies balsamea. Bot. Gaz. 60: 457- 

472. pis. 16-20. fig. 1. 
HUXLEY, T. H. 1878. Evolution in Biology. 
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557-602. pis. 8-10. 
1901. Contributions a l'e*tude de la fe*condation chez le Ginkgo biloba. Ann. Sci. 

Nat. Bot. VIII 13: 305-318. pis. 2, 3. 

JONES, W. N. 1918. On the nature of fertilization and sex. New Phytol. 17 : 167-188. 
KEENE, M. L. 1914. Cy to logical studies of the zygospores of Sporodinia grandis. 

Ann. Bot. 28: 455-470. pis. 25, 26. 
KILDAHL, N. J. 1908. The morphology of Phyllocladus alpina. Bot. Gaz. 46: 

339-348. pis. 20-22. 
KOLTZOFP, N. K. 1906. Studien tiber die Gestalt der Zelle: I, Untersuchungen iiber 

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figs. 37. 


LAND, W. J. G. 1900. Double fertilization in Composite. Bot. Gaz. 30: 252- 

260. pis. 15, 16. 

1902. A morphological study of Thuja. Ibid. 34: 249-259. pis. 6-8. 
1907. Fertilization and embryogeny of Ephedra trifurca. Ibid. 44: 273-292. 

pis. 20-22. 
LAWSON, A. A, 1904a. The gametophyte, archegonia, fertilization and embryo 

of Sequoia sempervirens. Ann. Bot. 18: 1-28. pis. 1-4. 
19046. The gametophyte, fertilization and embryo of Cryptomeria japonica. 

Ibid. 18: 417-444. pis. 27-30. 
1907. The gametophytes, fertilization and embryo of Cephalotaxus drupacea. 

Ibid. 21 ; 1-23. pis. 1-4. 
LEVINE, M. 1913. The cytology of Hymenomycetes, especially the Boleti. Bull. 

Torr. Bot. Club 40: 137-181. pis. 4-8. 

LILLIE, F. R. 1901. The organization of the egg in Unio based on a study of its 
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1912. Studies of fertilization in Nereis. III. The morphology of normal fertiliza- 
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Jour. Exp. Zool. 12- 413-476. pis. 1- 11. 

1914. Studies of fertilization. VI. The mechanism of fertilization in Arbacia. 
Ibid. 16:523-590. 

1919. Problems of Fertilization. Chicago. 

LILLIE, R. S. 1908. Momentary elevation of temperature as a means of producing 
artificial parthenogenesis in starfish eggs and the conditions of its action. Jour. 
Exp. Zool. 6:375-428. 

1915. On the conditions of activation of unfertilized starfish eggs under the 
influence of high temperatures and fatty acid solution. Biol. Bull. 28. 260-303. 

LOKB, J. 1910. Die Hemmung verschiedener Giftwirkungen auf das befruohtetc 
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1912. The Mechanistic Conception of Life. Chicago. 

1913. Artificial Parthenogenesis and Fertilization. Chicago. 

LOEB, J. and BANCROFT, F. W. 1913. The sex of a parthenogenetic tadpole and frog. 

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LOEB, J. and WASTENEYS, H. 1910. Warum hemmt Natrium cyanide die Gift- 

wirkung einer Chlornatriumlosung fur das Seeigelei? Biochem. Zeitsch. 2. 

1911. Sind die Oxidationsvorgange die unabhangige Variable in den Lebenser- 
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1912. Die Oxidationsvorgange im befruchteten und unbefruchteten Seesternei. 
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LUTHER, A. 1904. Die Eumesostominen. Zeit. Wiss. Zool. 77: 1-273. pis. 9: 

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MACCURDY, H. M. 1919. Division, nuclear organization and conjugation in 

Arcella vulgaris. Mich. Acad. Sci. Rep. 21: 111-113. 
MACORMICK, F. A. 1912. Development of zygospore in Rhizopus nigricans. Bot. 

Gaz. 63:67-68. 
McCLENDON, J. J. 1912. Dynamics of cell division. Artificial parthenogenesis in 

Vertebrates. Am. Jour. Physiol. 29: 268-301. 
McCuBBiN, W. A. 1910. Development of the Helvellinese. Bot. Gaz. 49: 195- 

206. pis. 14-16 
MEVES, FR. 1899. Ueber Struktur und Histogenese der Samenfaden des Meersch- 

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1908. Die Chondriosomen als Trager erblicher Anlagen. Cytologische Studien 
am Htihnercrabryo. Ibid 72 ; 816-867. pis. 39-42. 

1915. Ueber Mitwirkung der Plastosomen bei der Befruchtung des Eies von 

Filaria papillosa. Ibid. 87: 11 12-46. pis. 1-4. 
1918. Die Plastosomentheorie der Vererbung. Ibid. 92: II 41-136. figs. 18. 

MEYER, K. 1911. Untersuchungen liber die Sporophyt der Lebermoose. 1. 

Entwicklungsgeschichte des Sporogons der Corsinia marchantioides. Bull. Soc. 

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MINCHIN, E. A. 1912. An Introduction to the Study of the Protozoa. London. 
MIYAKE, K. 1901. The fertilization of Pythium deftaryanum. Ann, Bot. 16: 

653-667. pi. 36. 
1910. The development of the gametophytes and embryogeny in Cunninghamia 

sinensis. Bcih. Bot. Centr. 27: 1-25. pis. 5. 
MORGAN, T. H. 1899. The action of salt solutions on the unfertilized and fertilized 

eggs of Arbacia, and of other animals. Arch. Entw. 8: 448-539. pis. 7-10. 

figs. 21. 

1913. Heredity and Sex. New York. 
MOTTIER, D. M. 1898. Ueber das Yerhalten der Kerne bei der Entwicklung des 

Embryosacks und die Vorgange bei der Befruchtung. Jahrb. Wiss. Bot. 31 : 

125-158 pis. 2, 3. 

1904. Fecundation in Plants. Carnegie Inst. Publ. 15. 
_MURRILL, W. A. 1900. The development of the archegonium and fertilization in 

the hemlock spruce (Tsuga canadensis, Carr.) Ann. Bot. 14: 583-607. pis. 31, 

NAGLER, K. 1909. Entwicklungsgeschichtliche Studien liber Amoben. Arch. f. 

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NAWASCHIN, S. 1899. Neue Beobachtungen iiber Befruchtung bei Fritillaria und 

Lilium. Bot. Centr. 77: 62. (Russian account in 1898.) 

1909. Ueber das selbstandige Bewegungsvermogen der Spermakerne bei einigen 
Angiospermen. (Esterreich. Bot. Zeitschr. 69: 457. 

1910. Nahcres iiber die Bildung der Spermakerne bei Lilium Martagon. Ann. Jard. 
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NKMEC, B. 1910. Das Problem der Befruchtungsvorgange. Jena. 

1912. Ueber die Befruchtung bei Gagea. Bull. Internat. Acad. Sci. Boheme, 1-17. 

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NICHOLS, G. E. 1910. A morphological study of Juniperus communis var. depressa. 

Beih. Bot. Centr. 25: 201-241. pis. 8-17. figs. 4. 
NIENBURG, W. 1914. Zur Entwicklungsgeschichte von Polystigma rubrum DC. 

Zeit. f. Bot. 6: 369-400. figs. 17. 
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1907. Zur Entwicklungsgeschichte des Juniperus communis. Uppsala Univ. 

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OVERTON, J. B. 1913. Artificial parthenogenesis in Fucus. Science 37: 841, 844. 
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KABL, C. 1889. Ueber ZelUheihuig. Anat. Anz. 4: 21-30. figs, 2. 


RAMLOW, G. 1914. Beitrage zur Entwicklungsgcschichte der Ascoboleen. My col. 

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ROBERTSON, A. 1904. Studies in the morphology of Torreya californica. 11. The 

sexual organs and fertilization. New Phytol. 3: 205-216. pis. 7-9. 
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Arch. Mikr. Anat. 45: 339-369. pis. 21, 22. 
SARGANT, E. 1896. The formation of the sexual naclei in Lilium Martagon. I. 

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1897. Same title. II. Spermatogencsis. Ibid. 11: 187-224. pis. 12, 13. 
SAWYER, M. L. 1917. Pollen tube and spcrmatogenesis in Iris. Bot. Gaz. 64: 

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SAX, K. 1916. Fertilization in Fntillaria pudica. Bull. Torr. Bot. Club 43: 

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1918. The behavior of the chromosomes in fertilization. Genetics 3. 309-327. 

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SCHAUDINN, F. 1896. Ueber die Copulation von Artinophrys sol. Sitaber. Acad. 

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SCHIKORRA, W. 1910. Ueber die Entwicklungsgescnichte von Monascus. Zeitschr. 

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SHARP, L. W. 1912. Spermatogenosis in Equi&etum. Bot. Gaz. 64: 89-119. 

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1914. Sperm'atogcncsis in Marsilia. Ibid. 68: 419-431. pis. 33, 34. 
1920. Spermatogenesis in Blasia. Ibid. 69: 258-268. pi. 15. 
SMITH, B. G. 1919. The individuality of the germ-nuclei during the cleavage of the 

egg of Cryplobranchus alleghaniensis. Biol. Bull. 37. 246-287. 
STEIL, W. N. 1918. Method for staining antherozoid of fern. Bot. Gaz. 65: 

562-563. 1 fig. 
STEVENS, F. L. 1899. The compound oosphere of Albugo bhti. Bot. Gaz. 28: 

149-176. pis. 11-15. 

1901. Gametogenesis and fertilization in Albugo. Ibid. 32: 77-98. pis. 1-4. 
STRASBURGER, E. 1877. Ueber Befruchtung und Zeiltheilung. Jen. Zeitschr. 11. 
1884. Neue Untersuchungen uber die Befruchtungsvorgang bei den Phanero- 

gamen, als Grundlage fur eine Theone der Zeugung. Jena. 
1892. Schwarmsporen, Gameten, pflanzlichen Spermatozoiden, und das Wesen der 

Befruchtung. Histol. Beitr. 4: 49-158. pi. 3. 
1897. Kerntheilung und Befruchtung bei Fucus. Jahrb. Wiss. Bot. 30: 351-374. 

pis. 27, 28. 

1900. Einige Bemerkungen zur Frage nach der "doppelten Befruchtung" bei 
den Angiospermen. Bot. Zeit. 58: 293-316. 

1901. Ueber Befruchtung. Ibid. 59: 11, 353-368. 

TROW, A. H. 1895. The karyology of Saprolegnia. Ann. Bot. 9: 609-652. pis. 

24, 25. 
1899. Observations on the biology and cytology of a new variety of Achlya amen- 

cana. Ibid. 13: 131-179. pis. 8-10. 
1901. Biology and cytology of Pythium uliimum, n. sp. Ann. Bot. 16: 269- 

312. pis. 15, 16. 
1904. On fertilization in the Saprolegniacece. Ibid. 18: 541-569. pis. 34-36. 


WAGER, H. 1890. On the structure and reproduction of Cystopus candidus Lev. 

Ann. Dot. 10: 295-342. pis. 15,16. See also pp. 89-91. 
1899. The sexuality of fungi. Ibid. 13: 575-597. 
WALDEYEK, W. 1888. Ueber Karyokinese und ihre Beziehung zu den Befrucht- 

ungsvorgangen. Arch. Mikr. Anat. 32: 1-122. figs. 14. (Engi. transl. in 

Quar. Jour. Micr. Sci. 30: 159-281. pi. 14. 1889.) 
WALTON, A. C. 1918. The oogenesis and early embryology of Ascaris canis Werner 

Jour. Morph. 30: 527-604. pis. 9. fig. 1. 
WARBURG, O. 1908. Beobachtungen iiber die Oxidationsprozesse im Seeigelei. 

Zeitschr. Physiol. Chem. 67. 

1910. Ueber die Oxidationen im lebenden Zellen nach Versuchen am Seeigelei. 
Ibid. 66. 

1911. Untersuchungen iiber die Oxidationsprozesse im Zellen. Munchener Med. 
Wochenschr. 57. 

1914. Beitrage zur Physiologic der Zelle, inbesondere iiber die Oxidationsgesch- 

windigkeit in Zellen. Ergeb. d. Physiol. 14. 
WEBBER, H. J. 1900. Xenia, or the immediate effect of pollen in maize. U. S. 

Dept. Agr., Div. Veg. Path, and Physiol., Bull. 22: pis. 4. 
1901. Spermatogenesis and fecundation in Zamia. TL S. Dept. Agr. Bur. Pit. 

Ind. Bull. 2. pp. 100. pis. 7. 
WELSFORD, E. J. 1907. Fertilization in Ascobolus furfuraceus. New Phytol. 6: 

1914. The genesis of the male nuclei in Lilium. Ann. Bot. 28: 265-270. pis. 16, 


WENIGER, W. 1918. Fertilization in Lilium. Bot. Gaz. 66: 259-268. pis. 11-13. 
WHEELER, W. M. 1895. The behavior of the centrosomes in the fertilized egg of 

Myzostoma glabrum Leukart. Jour. Morph. 10: 305-311. figs. 10. 
1897. The maturation, fecundation and early cleavage of Myzostoma glabrum 

Leukart. Arch. d. Biol. 16: 1-77. pis. 1-3. 
WILDMAN, E. E. 1913. The sperm atogenesis of Ascaris megalocephala with special 

reference to the two cytoplasmic inclusions, the refractive body and the "mito- 
chondria": their origin, nature and r61e in fertilization. Jour. Morph. 24: 

421-457. pis. 3. 
WILSON, E. B. 1900. The Cell in Development and Inheritance. 2d ed. 

1901. Experimental studies in cytology. I. A cytological study of artificial 

parthenogenesis in sea urchin eggs. Arch. Entw. 12: 529-596. pis. 11-17. 

figs. 12. 
WINGE, O. 1914. The pollination and fertilization process in Humulus lupulus L. 

and H. Japonicus. Comp. Rend. Trav. Lab. Carlsberg 11. 
WOODBURN, W. L. 1920. Preliminary notes on the embryology of Reboulia hemis- 

phcerica. Bull. Torr. Bot. Club. 46: 461-464. pi. 19. 

WOYCICKI, Z. 1899. (On fertilization in Coniferae.) pp. 57. pis. 2. (Russian.) 
YAMANOUCHI, S. 1906. The life history of Polysiphonia violacea. Bot. Gaz. 42: 

401-449. pis. 19-28. 
1908. Spermatogenesis, oogenesis, and fertilization in Nephrodium. Ibid. 45: 

145-175. pis. 6-8. 



The life cycle in all bryophytes and vascular plants is characterized 
by a regular alternation of two well marked phases or generations: the 
gametophyte, which arises from the spore and produces gametes; and the 
sporophyte, which arises from the fusion product of two gametes and 
produces spores. In such a normal life cycle the number of chromosomes 
in the nuclei is doubled at the union of the gametes and reduced to the 
original number at sporogenesis ; the gametophyte is therefore the haploid 
generation and the sporophyte the diploid generation, their limits being 
marked by the two cytological crises, fertilization and reduction. Such 
an alternation of haploid and diploid phases has been discovered in the 
life cycles of many algae and fungi also, so that the general conception 
of alternation of generations has been extended to these lower groups. 
This, however, is not the place for a discussion of the homologies implied. 
It should be added that gametophyte and sporophyte may arise not only 
from each other, but either generation may also multiply by vegetative 

Many instances in which the above typical life cycle is departed from, 
and in which the correlation between the alternation of two generations 
and periodic changes in chromosome number is broken, are now known, 
the conspicuous examples being found among the ferns and certain 
angiosperms. The very convenient classification of such abnormalities 
drawn up by Vines (1911) is given as the basis for the present portion 
of the chapter. All dates and the matter included within square brackets 
have been added by the present author. 

"In the first place, the sporophyte may be developed either after an 
abnormal sexual act, or without any preceding sexual act at all, a con- 
dition known as apogamy. In the second, the gametophyte may be 
developed otherwise than from a post-meiotic spore, a condition known 
as apospory. 1 

1 [Apogamy in ferns was discovered by Farlow in 1874. Apospory was'discovered 
in mosses by Pringsheim in 1876 and in ferns by Druery in 1884. General discussions 
of these phenomena are given by Winkler (1908) and Strasburger (19096).] 




Apogamy. The cases to be considered under this head may be 
arranged in two groups: 

1. Pseudapogamy: sexual act abnormal. The following abnormalities 
have been observed: 

(a) Fusion of two female organs: observed (Christman 1905) in 
certain Uredineae (Caoma nitens, Phragmidium speciosum, 
Uromyces Caladii) where adjacent archicarps fuse: male cells 
(spermatia) are present but functionless. 

(6) Fusion between nuclei of the same female organ: observed in the 
ascogoniurn of certain ascomycetcs, Humaria granulata (Black- 

FIG. 124. Apogamy in ferns. 

A, nuclear migration in gametophyte cells of Laslrcea pseudo-mas var. polydactyla. 
X 500. (After Farmer and Digby, 1907.) B, section through gametophyte, showing 
young sporophytie tissue () "engrafted" into surrounding gametophy tic tissue (0) . 
(After Farmer and Digby.) C, sporophyte arising apogamously from gametophyte in 
Pteris cretica: 6 1 , first leaf; v, stem apex; w, root. (After de Bary.} 

man 1906), where there is no male organ; Lachnea stercorea 
(Fraser 1907), where the male organ (pollinodium) is present 
but apparently functionless. [A similar condition has been 
reported in A scobolus furfur aceus (Welsford 1907), Aspergillus 
repens (Dale 1909), and Ascophanus carneus (Cutting 1909).] 
(c) Fusion of a female organ with an adjacent tissue-cell: observed 
(Blackman 19046) [Blackman and Fraser 1906] in the archicarp 
of some Uredinese (Phragmidium violaceum, Uromyces Poce, 
Puccinia Poarum) : male cells (spermatia) present but function- 




There is no female organ: fusion takes place between two adjacent 
tissue-cells of the g imetophyte ; the sporophyte is developed from 
diploid cells ["grafted tissue "] thus produced, but there is no 
proper zygote as there is in a, 6, and c: observed (Farmer [and 
Digby] 1907) in the prothallium of certain ferns (Lastrcea pseudo- 
mas y var. polydactyla) [Fig. 124, A]: male organs (and sometimes 
female) present but functionless. Another such case is that 
of Humaria rutilans (ascomycote), in which nuclear fusion 

FKJ. 125. 

A, cell fusion in the sporangium of Aspidium falcatum. X 1950. (After R. F. Allen 
1911.) B, incomplete nuclear division in sporangium of Nephrodium hirtipes. X 1250. 
(After Steil, 1919.) C, apogamy and sporophytic budding in the embryo sac of Alchemilla 
pastoralis: egg developing apogamously below; cell of nucellus forming an embryo above; 
two polar nuclei and one synergid nucleus at center. (After Murbeck, 1902.) 

has been observed (Fraser 1908) in hyphse of the hypothecium: 
the asci are developed from these hyphse, and in them meiosis 
takes place; there are no sexual organs. [A similar condition 
has been reported in Helvetia crispa (Carruthers 1911) and 
Poly stigma rubrum (Blackman and Welsford 1912). It has 
already been pointed out (p. 291) that many students of the 
ascomycetes deny the existence of a nuclear fusion in the 
archicarp or vegetative cells, holding rather that the only 


fusion in the life cycle is that observed in the ascus, and that 
this fusion is the real sexual act .J 

[(e) Fusion of two haploid sporocytes: In Aspidium falcatum (R. F. 
Allen 1911) a haploid sporophyte arises by vegetative apogamy 
from a haploid gametophyte. In the sporangium the 16 
haploid sporocytes fuse in pairs, producing eight diploid cells 
(Fig. 125, A). In these cells reduction occurs, 32 haploid 
spores resulting.] 

2. Eu-apogamy: no kind of sexual act. 
(a) The gametophyte is haploid : 

(a) The sporophyte is developed from the unfertilized haploid 
oosphere : no such case of true parthenogenesis has yet been 
observed. [Kusano (1915) has observed the division of 
the haploid nucleus of an unfertilized egg in a few excep- 
tional cases in the orchid, Gastrodiaelata. Parthenogenctic 
development proceeds no further. The unfertilized egg of 
Fucus has been made to begin development by artificial 
means (Overton 1913), but the cytological facts are not 
known here. Motile gametes of certain other algae have 
been observed to develop without conjugation, as in 
Ectocarpus tomentosus (Kylin 1918).] 

(ft) The sporophyte is developed vegetatively from the gameto- 
phyte and is haploid: observed in the prothallia of certain 
ferns, Lastrcea pseudo-mas, var. cristata-apospora (Farmer 
and Digby 1907), and Nephrodium molle (Yamanouchi 
1908). [In the gametophytes of Nephrodium molle, which 
has antheridia but no functional archegonia, Yamanouchi 
found no nuclear migrations such as Farmer described 
in Lastrcea (see Id) ; but there was haploid grafted tissue, 
from which a haploid sporophyte developed. In Nephro- 
dium hirtipes (Steil 1919) a haploid sporophyte arises by 
vegetative apogamy from a haploid gametophyte. When 
there are eight sporogenous cells in the sporangium there 
is an incomplete nuclear and cell division (Fig. 125, 5), 
each nucleus coming to have the diploid number of chromo- 
somes. These eight diploid cells function as sporocytes 
and produce 32 haploid spores. Steil at first (1915) 
adopted Allen's interpretation (\e) for his material, but 
later decided that the phenomenon observed was one of in- 
complete division, and not one of fusion. In this case, 
as in Aspidium falcatum, apogamy is offset not by apospory 
but by an abnormal course of events in the sporangium. 
In Aspidium falcatum the sporophyte arises as in the 
examples mentioned in this paragraph, but because of 


the presence of a cell and nuclear fusion it is classified under 


(6) The gametophyte is diploid (see under Apospory): 

(a) The sporophyte is developed from the diploid oosphere: 
observed in some Pteridophyta, viz. certain ferns (Farmer 
1907), Athyrium Filix-fcemina, var. clarissima, Scolopend- 
rium vulgare, var. crispum-Drummondce, and Marsilia 
(Strasburger 1907); also in some Phanerogams, viz., 
Composite (Taraxacum, Murbeck 1QQ4; Antennaria alpina, 
Juel 1898, 1900; sp. of Hieracium, Rosenberg 1906): 
Rosaceae (Eu-Alchemilla sp., Murbeck 1901, 1904, Stras- 
burger 1905 [Fig. 125, C]): Ranuncul^cese (Thalictrum 
purpurascens, Overton 1902). [Also in the lily, Atamosco 
(Pace 1913), and Burmannia (Ernst 1909). Besides this 
form of apogamy ("ooapogamy" or "generative apo- 
gamy") Antennaria may also develop embryos from 
diploid synergids (" vegetative apogamy") and from cells 
of the nucellus ("sporophytic buddirg"). A similar 
variety of embryo origins is found in certain other angio- 
sperms. In many cases the chromosome number in 
apogamous species is about twice as large as that of nearly 
related forms reproducing sexually (Rosenberg 1909).] 
(/?) The sporophyte is developed vegetatively from the gameto- 
phyte: observed (Farmer [and Digby] 1907) in the fern 
Athyrium Filix-foeminaj var. clarissima. 

In all cases enumerated under Eu-apogamy, apogamy is 

associated with some form of apospory except Nephrodium 

molle, full details of which have not yet been published. 

[It is possible that a behavior like that in Aspidium 

falcatum (\e) or in Nephrodium hirtipes (2a/3) may occur 

in Nephrodium molle.] Many other ferns are known to be 

apogamous, but they are not included here because the 

details of their nuclear structure have not been investigated. 

Apospory. The known modes of apospory may be arranged as 

follows : 

1. Pseudapospory: a spore is formed but without meiosiSj so that it is diploid 
observed only in heterosporous plants, viz. certain species 
of Marsilia (e.g. Marsilia Drummondii) where the megaspore has a 
diploid nucleus (32 chromosomes) and the resulting prothallium and 
female organs are also diploid (Strasburger 1907); and in various 
Phanerogams, some Composite (Taraxacum and Antennaria alpina, 
Juel 1898, 1900, 1904), some Rosacese (Eu-Alchemilla, Strasburger 
1905), and occasionally in Thalictrum purpurascens (Overton 1902), 
where the megaspore ([and] embryo-sac) is diploid; in some species 


of Hieracium it has been found (Rosenberg 1906) that adventitious 
diploid embryo-sacs are developed in the nucellus: these plants 
are also apogamous. [In Marsilia Drummondii, which Shaw 
(1897) and Nathansohn (1909) had shown to be apogamous, Stras- 
burger (1907) found that, although normal reduction occurs in 
some of the megasporocytes, giving spores with 16 chromosomes, 
other megasporocytes undergo two divisions neither of which is 
reductional: the first division is homceotypic in character and the 
second is an additional vegetative mitosis without a hornologue 

FIG. 126. 

A, gametophyte with antheridium (anth.} and rhizoids (r) arising aposporously from 
tissue of sorus in Polystichum angulare var. pule her rimum; sp, sporangia. X 70. (After 
Bower.) B, gametophyte with archegonia arising from tip of pinnule in Polystichum. 
X 10. (After Bower.) 

in the normal cases. The resulting spores are therefore diploid, 
and ooapogamy follows.] 

2 Eu-apospory: no spore is formed of this there are two varieties: 
(a) With meiosis: this occurs in some Thallophyta which form no 
spores; the sporophyte of the Fucacese bears no spores, con- 
sequently meiosis takes place in the developing sexual organs. 
The Conjugate Green Algae also have no spores, meiosis 
taking place in the germinating zygospore which develops 
directly into the sexual plant. 


(6) Without ineiosis: the gametophyte is developed upon the sporo- 
phyte by budding; that is, spore-reproduction is replaced by a 
vegetative process: for instance, in mosses it has been found 
possible to induce the development of protonema, the first stage 
of the gamete phyte, from tissue cells of the sporogonium: 
[In this way l. and Em. Marchal (1909, 1912) were able to 
produce in Mnium, Bryum, Phascum, and Amblystegium 
diploid gamctophytes; these in turn produced tctraploid 
sporophytes which bore diploid spores. In one case (Ambly- 
stegium) a tetraploid garnetophyte was regenerated from 
cells of the tetraploid sporophyte.] Similarly, in certain ferns 
(varieties of Athyrium Filix-fcemina, Scolopendrium vulgare, 
Lastrcea pseudo-mas, Polystichum angulare, and in the species 
Pteris aquilina and Asplenium dimorphum), the gametophyte 
(prothallium) is developed by budding of the leaf of the sporo- 
phyte [commonly from the margin of the leaf or from the tissue 
of the sorus (Fig. 126)], and in some of these cases it has been 
ascertained that the gametophyte so developed has the same 
number (2x) of chromosomes in its nuclei as the sporophyte 
that bears it that is, it is diploid. 

Apospory has been found to be associated frequently with 
apogarny [in the life cycle]; in fact, in the absence of meiosis, 
this association would appear to be inevitable." 


The natural development of an egg without having been fertilized by 
a male gamete is a phenomenon which is apparently of much more 
frequent occurrence in animals than in plants. The best known examples 
are found among the rotifers, crustaceans, and insects, parthenogenesis 
being the regular mode of reproduction in some species. Other modes 
also usually occur in such organisms under certain conditions or after a 
certain number of generations. Parthenogenesis is reported in some 
protozoa (Plasmodium vivax, Schaudinn 1902), where the macrogamete, 
after certain nuclear changes, continues the life cycle without fusing 
with a microgamete. Moreover, as has already been described in the 
preceding chapter, parthenogenesis may be artificially induced in the 
eggs of other animal groups, notably echinoderms, mollusks, and amphi- 
bians, and around this fact centers much of the significant work of modern 
experimental biology. In commenting upon parthenogenetic develop- 
ment Minchin (1912, p. 137) points out that " . . . the gamete which has 
1-his power is always the female ; but this limitation receives an explanation 
from the extreme reduction of the body of the male gamete and its 

1 The cytological results of researches on maturation and development in cases of 
parthenogenesis have recently been summarized by Paula Hertwig (1920). 


feeble trophic powers, rendering it quite unfitted for independent repro- 
duction, rather than from any inherent difference between the two 
sexes in relation to reproductive activity/' 

Many normally parthenogenetic animal eggs are known to have the 
diploid^ chromosome number as the 'result "of a~failure of^rerltrctieftr-a 
condition par3HSigIiE^IE^own as bdapogamy in plants. On the 
contrary, there are some which, unlike any known vascular plant, are 
haploid, reduction having taken place in the normal fashion. Partheno- 
genesis is often associated with certain irregularities in the behavior 
of the polar bodies, as will be noted in the following descriptions of some 
well known examples. In the majority of recorded cases the partheno- 
g^netic egg produces but one polar body; in some, however, two are 
formed as in all zygogenetic eggs (those developing after having been 

It was long ago noticed by Blochmann (1888; see Wilson 1900, pp. 
281-4) that in Aphis both zygogenetic and parthenogenetic eggs are 
produced; the former -produce the usual two polar bodies while the 
latter have but one. It was also seen that the polar bodies are not 
budded off as separate cells, but remain within the membrane of the 
egg. Weismann (1886, 1887), working on rotifers, concluded that the 
second polar body has something to do with parthenogenetic develop- 
ment; and Boveri (1887d, 1890), who had seen the chromosomes of the 
second polar body transform themselves into a nucleus in the egg of 
Ascaris, made the suggestion that this second polar body might unite 
with the egg nucleus and so initiate development. Brauer (1894) an- 
nounced that this is precisely what occurs in Artemia, a phyllopod 
crustacean. In this organism two types of parthenogenesis are found. 
In some cases the nucleus of the second polar body, with 84 chromosomes, 
actually does unite with the egg nucleus, likewise with 84, causing 
"fertilization" and the resulting development of an individual with the 
diploid number (168) of chromosomes. In other cases only one polar 
body is produced, but reduction is accomplished in the division forming 
it, and the resulting haploid egg develops parthenogenetically into an 
individual with only 84 chromosomes. 

In Phylloxera carycecaulis (Morgan 1906, 1908, 1909, 1910, 1915) 
only one polar body appears, but here no reduction occurs: the diploid 
egg develops parthenogenetically. In Nematus lacteus (Doncaster 1906) 
two polar bodies are produced, but reduction fails and the diploid egg 
proceeds to develop as in Phylloxera. 

It has long been known that the eggs of the honey bee, Apis mellifica, 
will develop either zygogenetically into females or parthenogenetically 
into males. It has been shown in both cases that there are two polar 
bodies (Blochmann) and that a normal reduction in the number of 
chromosomes occurs (Nachtsheim 1912, 1913). The fertilized eggs 


develop into workers or into queens with the diploid number (32) of 
chromosomes; those not fertilized develop into drones with the haptoid 
number (16). (At the time of spermatogenesis in the drone no further 
reduction in chromosome number occurs: the spermatozoa retain the 
number present in the body cells (16).) 

In the gall-fly, Neuroterus lenticularis, Doncaster (1910-1911) has 
shown that there are two classes of parthenogenetic females. The egg of 
the first class gives off no polar bodies, retains the diploid number (20) 
of chromosomes, and develops parthenogenetically into a sexual female. 
The egg of the second class gives off two polar bodies, retains the reduced 
number (10) of chromosomes, and develops parthenogenetically into 
a male. (The offspring of the sexual females and males constitute the 
next generation of parthenogenetic females.) 

There are thus several organisms in which both zygogenetic and 
parthenogenetic eggs are produced. In some of them, such as the bee, 
in which the same egg can develop in either way, the two classes of eggs 
show no morphological differences. In other forms, such as a species of 
Melanoxanthus (a plant louse) and Sida crystallina (crustacean), they 
may differ considerably. The parthenogenetic egg, for example, may 
contain much less yolk than the zygogenetic one : it is less highly differen- 
tiated, and " still retains the capacity to initiate dedifferentiation and 
reconstitution independently of union with a male gamete. In this 
respect it resembles the less highly specialized cells of other tissues 
rather than the gametes " (Child 1915, p. 408). 

It has recently been shown that frogs which have been induced to 
develop parthenogenetically from punctured eggs (Bataillon's method) are 
of both sexes (Loeb 1921). The chromosome number in the females has 
not been determined, but both Parmenter (1920) and Goldschmidt (1920) 
report the diploid number in males so derived. The origin of this diploid 
condition has not been satisfactorily explained. Parmenter suggests 
that it may be due to the retention of one polar body, or to a premature 
division of the chromosomes without cytokinesis just before the first 
cleavage. This promises to be an interesting case in connection with 
the mechanism of sex-determination. 

Conclusion. To review the various theories which have been advanced 
to account for the origin of parthenogenesis, its relation to other forms of 
reproduction, and its significance in the life history, is a task which lies be- 
yond the scope of the present work: it has been our purpose only to indicate 
some of the outstanding cytological facts in certain conspicuous instances 
of the phenomenon. The cytological features have been accurately 
ascertained in only a very few cases, and these show little agreement. 
Furthermore, it is in artificially induced rather than in natural partheno- 
genesis that the physiological conditions are best known. In view of 
these facts it appears more than probable that many more cytological 


and physico-chemical data must be secured before any theory ad- 
equately harmonizing all the observed phenomena of parthenogenesis can 

be formulated. 

Bibliography 13 

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" "$ 

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The chief interest of cytology at the present time probably lies in the 
relation which it bears to the subject of heredity. From the time when 
the problems of cell research first began to take definite shape, especially 
since a connection between the activities of the cell and the phenomena 
of inheritance was suggested, the efforts of most cytologists have con- 
tributed directly or indirectly to the solution of two great and closely 
interrelated problems of biology: the problem of ontogenetic develop- 
ment and the problem of heredity. The aid which cytology has afforded 
in these respects has been invaluable. Not only has it been able to 
discover a large number of the significant facts of individual development, 
or ontogeny, but it has also thrown a flood of light upon many obscure 
matters in the field of heredity, and has so come an important factor 
in the'study of phylogeny and evolution. 

The Law of Genetic Continuity. "The most fundamental contribu- 
tion of cell-research to the theory of heredity/ 7 says Wilson (1909), "is 
the law of genetic continuity by cell-division. Cells arise only by the 
division of preexisting cells ... In each generation the germinal stuff 
runs through the same series of transformations; hence that reappearance 
of the same traits in successive generations that we call heredity/' 

It is by the light of the above law that we are enabled to see some- 
thing of the nature of the material continuity which exists between suc- 
cessive stages of the ontogenetic development, and also between succetfs- 
ive generations. It is to be remembered, in the first place, that all the 
cells of the adult multicellular organism are derived by repeated division 
from the single cell (ordinarily a zygote or a spore) with which develop- 
ment starts, so that the causes of events occurring at any particular stage 
are to be sought largely in the reactions of cells at earlier stages; and, in 
the second place, that the material link connecting two successive gen- 
erations is a single organized cell, usually a gamete or a spore, which 
means that the heritage of a long ancestry is in some way represented in 
this single cell and its capabilities. "The conception that there is an 
unbroken continuity of germinal substance between all living organisms, 
and that the egg and the sperm are endowed with an inherited organiza- 
tion of great complexity, has become the basis for all current theories of 
heredity and development" (Locy, 1915, p. 224). 



Cytological studios have therefore centered mainly about the general 
organization of the egg (chiefly that of animals) as related to the character 
of the organism arising from it (the problem of development), and about 
the roles played by the various cell organs of the gamete in the transmis- 
sion of heritable characteristics from one generation to the next (the 
problem of heredity). The character of the principal modern theory of 
heredity to which these studies have led is due in no small measure to the 
influence of a number of earlier hypotheses, such as those of Darwin and 
deVries, and especially that of Weismann. ! These hypotheses will be 
reviewed in Chapter XVIII, where their relation to the modern cytolog- 
ical interpretation of heredity, set forth in this and the following three 
chapters, will be discussed. ' 

It is obvious that an account of the physical basis of heredity would 
require for completeness not only a description of the structural changes 
by which visible materials are transmitted and distributed during garnc- 
togenesis, fertilization, and development; but also a review of many phy- 
siological processes which accompany these changes, and through which 
many characters are brought to expression. In these chapters attention 
will be limited largely to the structural aspects of the problem. 
Among the physiological changes those occurring at the time of fertiliza- 
tion are best known, and have already been discussed in Chapter XII. 

The R6le of the Nucleus. It was Ernst Haeckel (1866) who first 
advanced the hypothesis that "the nucleus of the cell is the principal 
organ of inheritance." Cytological evidence in support of this view, 
announced by Haeckel as a speculation, was brought forward by O. 
Hertwig (1875 etc.), Strasburger (1878, 1884), van Benedcn (1883 etc.), 
and a number of other investigators, who described the behavior of the 
nucleus in the various stages of the life cycle, particularly in somatic 
cell-division, maturation, and fertilization. Two of these workers, O. 
Hertwig and Strasburger, who had discovered the fusion of the gamete 
nuclei at the time of fertilization in animals and plants respectively, 
definitely announced the theory, now supported by a considerable body 
of observational and experimental evidence, that the nucleus is the 
"vehicle of heredity. " They held that hereditary transmission is 
through the nuclei of the gametes, and that the chromatin is the special 
inheritance material, or "idioplasm/ 7 about which there had been so 
much speculation. This view was at once widely adopted by biologists. 

The efforts of many cytologists were now directed toward the further 
elucidation and verification of this nuclear hypothesis of heredity, and 
many observations and experiments apparently demonstrated its essen- 
tial correctness. It was noted that, so far as could be discerned, the 
spermatozoon in many cases brings nothing but nuclear material into 
the egg, so that hereditary transmission from the male parent must be 
through the nucleus alone. A similar condition was later reported in 



plants, Guignard, Nawaschin (1910), and Welsford (1914) pointing out 
that in Lilium only the male nucleus enters the egg, its accompanying 
cytoplasm being rubbed off and left behind. (See p. 299.) Certain 
ingenious experiments of Boveri (1889, 1895; also 1909 and 1918) led 
to the same conclusion regarding the nucleus. Boveri induced the fer- 
tilization of enucleated fragments of Sphcerechinus eggs (a phenomenon 

FIG. 127. 

A, egg of Spha'rechinus yratiularix undergoing artificially induced cleavage mitosis; 
spermatozoon of Stronuyloccntrotux livid an has entered and taken the form of a chromosome 
group. B, cytokinesis beginning; one blastomere will have a purely maternal nucleus, 
and the other a hybrid nucleus. (Diagrammed after Herbst, 1009.) 

FIG. 127 bis.- 

-Diagram showing the irregular distribution of the chromosomes by a 
quadripolar mi to tic figure. (After Boveri.) 

known as merogony) by spermatozoa of Echinus, and obtained larva) 
which were purely paternal in character. From this it was argued that 
it is the sperm nucleus alone, and not the egg cytoplasm, that transmits 
the hereditary characters from one generation to the next in this case. 
Other experiments of a similar nature, however, turned out differently, 
as will presently be noted. Certain echinoderm hybrids, furthermore, 
show paternal larval characters even when the egg nucleus has not been 


A strong piece of evidence supporting Boveri's conclusion was fur- 
nished by Herbst (1909). By treating eggs of Sphcerechinus with valeri- 
anic acid Herbst caused them to undergo cleavage artificially. While 
the cleavage mitosis was in progress a spermatozoon of Strongylocentrotus 
was allowed to enter the egg, where it at once gave rise to its group of 
chromosomes (Fig. 127). These, however, arriving too late to join 
regularly in the mitosis, were incorporated in neither of the daughter 
nuclei of the first cleavage : they resumed the form of a nucleus, and this 
was included in one of the blastomeres. This blastomere therefore 
contained two nuclei, one maternal and one paternal, which combined 
during subsequent stages, whereas the other blastomere had a maternal 
nucleus only. Herbst regarded such nuclear behavior as responsible for 
the frequently found larvse which are hybrid in character on one side 
and purely maternal on the other. This experiment has been held to 
show not only that it is the nucleus of the spermatozoon which brings in 
the paternal characters, but also that it is the chromosomes alone that are 
responsible. It is assumed, though perhaps without sufficient evidence, 
that the other nuclear materials (karyolymph etc.) which may be present, 
as well as any cytoplasmic elements, have opportunity to mix generally 
with the egg cytoplasm, since the membrane of the male nucleus breaks 
down and leaves the chromosomes lying free before the egg divides into 
the two blastomeres. The paternal characters, however, appear only 
where the chromosomes come to be located that is, in the cells compos- 
ing one-half of the organism. In his work on multipolar mitoses in di- 
spermic eggs (Fig. 127 bis; see also p. 163) Boveri (1902, 1907) was able 
to show further that abnormal chromosome distribution is associated 
with abnormalities in development in a very definite way; and that if 
isolated blastomeres resulting from such abnormal divisions be made to 
develop independently, completely normal larvae result only where there 
is statistical reason to believe that a full complement of the qualitatively 
different chromosomes is present. 

The nuclear theory had its opponents from the beginning. Verworn, 
Waldeyer, Rauber, and other early investigators held that the cytoplasm 
as well as the nucleus must be concerned in the hereditary process, since 
the spermatozoon in many cases does bring cytoplasm into the egg, and 
also because neither nucleus nor cytoplasm can function independently 
of the other. This view received support in certain experiments which 
seemed to discount the power of the nucleus in controlling heredity. 
Loeb (1903) found that when a sea urchin egg was fertilized by a starfish 
sperm the resulting larva possessed purely maternal characters, the 
sperm nucleus exerting no visible hereditary effect. The same thing was 
noted by Godlewski (1906) in crosses between sea urchins and crinoids. 
Godlewski made the further significant observation that when enucleated 
egg fragments of Parechinus (sea urchin) were fertilized by sperm of 


Antedon (crinoid) the larvae so produced, contrary to BoverFs results, 
were maternal in character: they were like the mother, which had pre- 
sumably contributed cytoplasm only, and not like the father, which had 
furnished the nucleus. Fertilization by a spermatozoon had here pro- 
duced a developmental stimulus but no amphimixis (the combining of 
hereditary lines), so far as could be judged from the appearance of the 
larvae. Even if the male cytoplasm were admitted to have no heredi- 
tary role, it nevertheless seemed that the cytoplasm of the egg was clearly 
so concerned. 

In his work on sea urchin hybrids Baltzer (1910) was able to show 
why it is that some such larvae are maternal in character while others 
have the characters of both parents. When an egg of Strongylocentrotus 
fertilized by a spermatozoon of Sphcerechinus undergoes its first cleavage 
division the paternal chromosomes behave irregularly; they fail to become 
incorporated in the daughter nuclei and are lost. Those individuals 
which develop far enough show maternal skeletal characters. In the 
reciprocal cross, on the contrary, all of the chromosomes behave normally 
and the resulting larvae are truly hybrid in character. Thus in the first 
cross, in which the paternal chromosomes are lost, the spermatozoon 
furnishes only a developmental stimulus and has no appreciable effect 
on the character of the new individual; whereas in the second cross, in 
which the paternal chromosomes are included in the blastomere nuclei, 
the spermatozoon not only furnishes the developmental stimulus but 
also contributes paternal characters to the new individual. This is 
particularly convincing evidence in favor of the view that the chromo- 
somes are in some way responsible for the development of parental 
characters in the offspring. 

In a posthumous paper Boveri (1918) reported an additional observa- 
tion which, he believed, goes far toward explaining the conflicting results 
of different investigators. He found that egg fragments, and even whole 
eggs, may often have chromatin in a form that easily escapes observation, 
but which can exert its usual influence on development. In accordance 
with his earlier observations, enucleate egg fragments of Sphcerechinus 
fertilized by spermatozoa of Strongylocentrotus may develop into purely 
paternal larvae. Most of them, however, are intermediate in charac- 
ter, resembling the maternal parent also in certain features. Having 
previously (1895, 1905) demonstrated that the size of the nuclei in 
merogonic larvae is proportional to the number of chromosomes they 
contain (see Chapter IV), Boveri was able to show that the nuclei of the 
intermediate larvae are diploid rather than haploid, so that it is clear that 
the supposedly enucleate fragments in such cases must have contained 
chromosomes. It is probable, Boveri believed, that the maternaHarvae 
obtained by Godlewski may be accounted for in a similar fashion. 

It was pointed out by Strasburger (1908), who had come to believe in 


the complete monopoly of the nucleus in the transmission of hereditary 
characteristics, that the maternal character of Godlewski's larvae could 
be explained on the assumption that the early developmental stages do 
not require the expression of the hereditary capabilities of the nucleus, 
but are dependent more directly upon mechanical causes. Boveri (1903, 
1914), as a result of his hybridization experiments, strongly emphasized 
the view that the spermatozoon has an influence upon all of the larval char- 
acters; but he pointed out that the larval stages by themselves are not 
sufficient grounds upon which to establish complete conclusions regarding 
the respective roles of nucleus and cytoplasm, since the general course 
of the early developmental stages in such organisms is immediately 
dependent to a very large extent upon the general organization of the egg. 

This brings us to a brief consideration of the " promorphology " of 
the highly organized animal egg, and of the relation which exists between 
this organization and the character of the organism developing from it. 
Of the large amount of work done in this field only a hint can be given 

The Promorphology of the Ovum. There arose very early two views 
regarding the organization of the egg which recall the older theories of 
preformation and epigenesis (Chapter I). According to one, most fully 
expressed in W. His's Theory of Germinal Localization (1874; see Wilson 
1900, p. 397), the embryo is prelocalized in the general cytoplasm of the 
egg not preformed in the old sense of Bonnet, but having its various 
parts represented by substances with definite relative positions. This 
view found support in those cases in which a single isolated blastomere of 
the two-celled stage develops into a half-larva instead of a complete 
smaller larva (Roux on the frog, 1888 ; Crampton on the marine gastropod, 
Ilyanassa, 1896); and especially in Beroe, a ctenophore, which produces an 
incomplete larva even if a portion of the unsegmented egg be removed 
(Driesch and Morgan, 1895). 

Opposed to the above view was that which held the egg to be isotropic 
and without any predetermination of embryonic parts. Certain well 
known experiments appeared to bear out this conclusion. It was found 
in the frog (Pfluger 1884; Roux 1885), the sea urchin (Driesch 1892), an 
annelid (Wilson 1892), andAscaris (Boveri 1910) that very abnormal types 
of cleavage can be artificially induced, but that normal larvae nevertheless 
result. A number of cases were also described in which complete embryos 
arose from single isolated blastomeres of the two-celled stage (Fundulus, 
Morgan 1895; and other forms), or even from those of the sixteen-celled 
stage (Clytia, Zoja 1895). Had there been any prelocalization of parts 
in the egg it is difficult to see how normal or complete embryos could 
have arisen in such abnormal ways as these. 

It appears that the eggs of different animal species vary greatly 
in the degree and fixity of their internal differentiation. In some cases 


the egg is virtually isotropic, and through several succeeding cell gene- 
rations the blastomeres are cquipotential, that is, equally capable of 
developing into any part of the body or even into the whole of it. Thus 
the embryonic parts, and hence many of the individual's characters, are 
not definitely marked out until a comparatively late stage. On the 
contrary, there are forms in which the axis of polarity and certain funda- 
mental embryonic parts are roughly delimited in the egg cytoplasm in 
such a way that an alteration in the relative positions of the egg materials 
brings about a corresponding alteration in the character of the resulting 
individual. As an illustration of such internal differentiation may be 
taken the case of Styela, an ascidian, described by Conklin (1915). In 
the egg of Stijela there arc four or five distinct kinds of plasma arranged 
in a definite order and distributed in a regular manner as cleavage pro- 
ceeds, each kind eventually giving rise to a certain portion of the embryo. 


FKJ. 12S. Kggs of various animals, showing the patterns assumed by the material s 
which give rise to the various body regions. In the first three the egg has undergone 
division, and the plasmas becoming ectoderm, mesoderm, and endoderm are represented 
in clear white, cross-hatching, and parallel ruling respectively. In the fourth egg two 
divisions have occurred, and several definitely arranged substances are distinguishable. 
(After Conklin, 1915.) 

Substances which are yellow, gray, slate-blue, and colorless give rise 
respectively to muscle and mesoderm, nervous system and notocord, 
endoderm, and ectoderm. " Thus within a few minutes after the fertiliza- 
rion of the egg, and before or immediately after the first cleavage, the 
anterior and posterior, dorsal and ventral, right and left poles are clearly 
distinguishable, and the substances which will give rise to ectoderm, 
endoderm, mesoderm, muscles, notocord and nervous system are plainly 
visible in their characteristic positions" (Conklin 1915, p. 118). If 
such eggs are placed in a centrifuge the various substances may be 
made to assume an entirely abnormal stratified arrargement, which 
in turn "may lead to a marked dislocation of organs; the animal may be 
turned inside out, having the endoderm on the outside and its skin and 
ectoderm on the inside, etc/ 7 (p. 321). Such a behavior emphasizes 
the determinative character of the cytoplasmic pattern clearly present 
in many eggs. It has further been noted that the eggs of various animal 
phyla are characterized by distinct patterns in the arrangmeent of their 
visibly different materials (Fig. 128). "The polarity, symmetry and 


pattern of a jellyfish, starfish, worm, mollusk, insect or vertebrate are 
foreshadowed by the characteristic polarity, symmetry and pattern of the 
cytoplasm of the egg either before or immediately after fertilization " 
(Conklin, p. 172-5). That the arrangement of the embryonic parts is 
not solely dependent upon such visible egg substances is shown by the 
observations of Morgan (1909c, 19100) and Boveri (19106) on centrifuged 
eggs of Arbacia, Ascaris, the frog, and other forms. Here it is found 
that the displacement of the various substances does not necessarily 
cause a dislocation of the body parts of the embryo: hence the setting 
apart of the embryonic regions must be dependent upon a polarity in the 
egg which at least in many cases is not disturbed by the experimental 
alteration in position of the visible egg substances. But in either case 
differentiation appears to be related to a cytoplasmic organization. 
From this it would appear that the characters which such an organism 
inherits from the preceding generation do not belong to one category and 
are not transmitted in the same way. There are first those general 
characteristics of organization which are the direct outgrowth of a corre- 
sponding organization in the egg cytoplasm. Secondly, there are the 
Mendelian characters which appear later in the ontogeny and which there 
is every reason to believe are represented in some way in the chromosomes 
of the gamete nuclei (Chapter XV). Boveri thus distinguished two 
periods after fertilization: an early one in which the course of develop- 
ment is dependent on the organization of the egg cytoplasm, only general 
metabolic functions of the chromosomes being active ; and a later one in 
which the specific hereditary powers of the chromosomes are brought to 
expression, the right chromosomal combination then proving to be 
necessary for normal development. 

The question naturally arises as to how much the cytoplasmic organ- 
ization may be due in turn to the activity of the nucleus during the 
differentiation of the egg as to whether the general characters which are 
the direct outgrowth of this organization may or may not be ultimately 
dependent, as are the clearly Mendelian characters, on nuclear factors. 
Conklin (1915) comments upon this point as follows: "In this differentia- 
tion and localization of the egg cytoplasm it is probable that certain 
influences have come from the nucleus of the egg, and perhaps from the 
egg chromosomes. There is no doubt that most of the differentiations of 
the egg cytoplasm have arisen during the ovarian history of the egg, and 
as a result of the interaction of nucleus and cytoplasm; but the fact 
remains that at the time of fertilization the hereditary potencies of the 
two germ cells are not equal, all the early stages of development, includ- 
ing the polarity, symmetry, type of cleavage, and the pattern, or relative 
positions and proportions of future organs, being foreshadowed in the 
cytoplasm of the egg cell, while only the differentiations of later develop- 
ment are influenced by the sperm* In short the egg cytoplasm fixes the 


general type of development and the sperm and egg nuclei supply only 
the details" (p. 176). 

Plastid Inheritance. Certain cases of "plastid inheritance " have 
been brought forward to show that the character of aii organism may not 
be entirely due to factors delivered to it by the gamete or spore nuclei. 
It has been pointed out that two successive generations of cells repro- 
ducing by division resemble each other for the obvious reason that the 
organs of any given cell may actually become the corresponding organs of 
the 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 
rnulticellular individual (Ulothrix etc.), or associates with others of its 
kind to form a colony (Hydrodictyon, Pediastrum; Harper 1908, 1918ab), 
the color of the successive colonies or multicellular individuals is a charac- 
ter that is transmitted directly by the repeated division of chloroplasts. 
Thus, as Harper urges, the nucleus is not required here to account for the 
resemblance between successive generations of cells or individuals, so far 
as this character is concerned. 

A similar interpretation has been placed by some geneticists upon the 
inheritance of " chlorophyll characters" in the higher plants, the supposi- 
tion 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 are accordingly held to be 
due to an abnormal condition or behavior of the chloroplasts. 

Such a case is that of Mirdbilis jalapa albomaculata, described by 
Correns (1909). In plants of this race there are some branches with 
normal green leaves, some with white leaves/and some with "checkered" 
(green and white) leaves. Flowers are borne on branches of all three 
types. In all cases crosses between unlikes result in seedlings with the 
color of the maternal parent: inheritance is strictly maternal. 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 
chlorophyll. In neither case does the pollen affect the color of the 
resulting individual. The explanation offered by Correns for the color- 
less condition is that it is due to a cytoplasmic disease which destroys 
the chloroplasts. It is therefore delivered directly to the next generation 
in the egg cytoplasm, and is not transmitted by the male parent because 
no male cytoplasm is brought into the egg at fertilization. If it had been 
due to nuclear factors it would have been transmitted by both parents, 
since the nuclear contributions of the two are equal. This condition is 
analogous to that occasionally found in animals, in which bacteria may 


be carried from one generation to the next in the egg cytoplasm, causing 
a direct inheritance of the disease. But such pathological cases are not 
to be confused with, or thought to contradict, normal Mendelian heredity, 
which, as will be seen in the following chapter, is closely bound up with 
nuclear phenomena. They are rather to be regarded as examples of 
repeated reinfection. 

Results differing from those of Correns were obtained by Baur (1909) 
in his researches on Pelargonium zonale albomarginata. This form, which 
is characterized by white-margined leaves, often has pure green and pure 
white branches, as in Mirabilis. Crosses either way between flowers on 
these two kinds of branches result in every case in mosaic (green and 
white) offspring: inheritance is here not purely maternal as in Mirabilis. 
Although Baur admits for this case the possibility of a Mendelian inter- 
pretation if a segregation of factors for greenness and whiteness in the 
somatic cells be allowed, he thinks it more probable that inheritance in 
this instance is not a matter of chromosomes and Mcndelism at all, but 
is rather due to a sorting out of green and colorless plastids, themselves 
permanent cell organs, in the somatic cells. In order to account for 
inheritance through both the male ancj the female, Baur assumes that 
primordia of plastids are brought in through the male cytoplasm as well 
as the egg cytoplasm, a conclusion directly contradictory to that of 
Correns. Ikeno ( 1917) , working on variegated races of Capsicum annum. 
obtained results similar to those of Baur on Pelargonium^ and concluded 
that transmission of variegation is not through the nucleus, but through 
plastids contributed by both parents. 

Although the results and interpretations of Correns and Baur are at 
present irreconcilable except on the basis of assumptions not warranted 
by known facts, they agree in the conclusion that plastid inheritance is 
not Mendelian, but is due rather to extra-nuclear factors. Baur reports 
corroborative evidence in Antirrhinum (1918). Opposed to this con- 
clusion is that of Lindstrom (1918), who has clearly shown in the case of 
certain variegated races of maize that the inheritance of characters due 
to unusual plastid behavior is strictly Mendelian. This means that the 
distribution or degree of prominence of the plastids, although these may 
be organs with their own individuality, depends upon the activity of 
Mendelian factors in the chromosomes, which represent the only known 
cell mechanism in which there is at present any hope of finding an expla- 
nation for the distribution of Mendelian characters (Chapter XV). In 
Lindstrom's plants plastid inheritance appears to be as much a nuclear 
matter as the inheritance of any other character manifested in the extra- 
nuclear portion of the cell. 

On the basis of the data at hand the tentative conclusion seems fully 
justified that all cases of chlorophyll inheritance do not belong to one 
category. Some of them are clearly to be accounted for on the same basis 


with other Mendelian characters, whereas others appear to require an 
explanation of another kind. The results of work in progress at Cornell 
University on variegated races of maize points in this direction. One 
of the most interesting problems in cytology and genetics at present is 
that concerning the manner in which extra-nuclear bodies, such as plas- 
tids and their primordia, may account for certain types of inheritance, 
and the extent to which their behavior may be influenced by the 

Aleurone Inheritance. We may here refer to the attempt which has 
been made to explain the inheritance of aleurone color in maize endosperm 
on the basis of a somatic segregation of special cell organs in the form of 
granular primordia, which multiply by fission and develop into aleurone 
bodies of various types and colors. But since aleurone and other endo- 
sperm characters are inherited in Mendelian fashion, as shown by East 
and Hayes (1911, 1915), Collins (1911), and Emerson (1918), and since 
there has been adduced in support of the supposed sorting out of primor- 
dia no evidence approaching in cogency that upon which the chromosome 
theory has been built up, geneticists generally are of the opinion that the 
chromosomes with their well known mechanism of segregation offer the 
best promise of an explanation of the inheritance of aleurone characters, 
though all admit that other organs may play a part in bringing these 
characters to expression. Furthermore, the case for the self-perpetuity 
of the aleurone grain is much weakened by the fact of their artificial pro- 
duction by Thompson (1912). 

The theory that chondriosomes are concerned in heredity has been 
discussed in Chapters VI and XII. 

General Conclusions. In conclusion the statement may again be 
made that as genetical researches multiply it becomes increasingly clear 
that the characters in which an individual resembles that from which it 
sprang are not in every case transmitted to it in the same manner. Those 
characters which are inherited according to Mendelian rules, to anticipate 
a conclusion based on evidence to be presented in the next chapter, in all 
probability owe their repeated appearance in successive generations to 
"factors" of some sort which are transmitted by the chromosomes of 
the nucleus. This applies also to those characters which, while Men- 
delian in distribution, depend for their expression upon the presence 
of other cell organs (plastids) which may have an individuality of their 

All or nearly all of the hereditary contribution made by the male 
parent must in most organisms be in the above form, since the male 
gamete consists almost exclusively of nuclear material. The female 
gamete, or egg, in addition to the clearly Mendelian characters repre- 
sented by factors in its nucleus, may at least in the case of many animals 


contribute certain general characters, such as polarity, symmetry, and 
general type of early development, which are the direct outgrowth of an 
elaborate organization present in the egg cytoplasm. It is true that this 
organization is the result of processes in which the nucleus cooperates 
during the differentiation of the egg, and those who hold to the universal 
applicability of the Mendelian interpretation would assume that the 
type of organization must depend upon Mendelian factors carried in the 
nucleus. However this may be, the fact remains that the two gametes 
at the time of fertilization are not equal in hereditary potency, as 
Conklin states. So far as the clearly Mendelian characters are con- 
cerned, however, all evidence goes to show that they are precisely 

The direct inheritance of metidentical characters, such as the above 
mentioned green plastid color in Pediastrum, and the indirect inheritance 
of colony characters in the same form, afford other examples of hereditary 
transmission otherwise than through the nucleus. With respect to 
colony characters, Harper has shown in a striking manner, bothmHydro- 
dictyon &nd Pediastrum, that the characteristic form and type of organiza- 
tion assumed by the colony are the results of interactions between the 
form, polarities, adhesiveness, surface tension, etc. of the free-swimming 
swarm spores which aggregate to build it up. The swarm spore has an 
individual organization of a particular type, but its capabilities show it to 
be devoid of any arrangement of its protoplasmic parts corresponding 
either to its future position in the colony or to the arrangement of 
the cells in the colony as a whole. The character of the colony 
thus depends upon the interactions of its component units and is 
in no way represented in any one of them. Consequently it is held by 
Harper that no system of spatially arranged factors in a special germ 
plasm is required to account for the regular reappearance of such cell and 
colony characters in these' organisms, and that such facts must be reck- 
oned with in attempting to explain heredity and development in terms 
of the cell. 

By whatever means they are transmitted, it is evident that most 
characters must be brought to expression through the activity of the cell 
system as a whole, the process involving a long series of reactions in 
which all or nearly all of the cell constituents play their parts. At the 
present time little or nothing is known of the real nature of the " factor" 
or of the manner in which it may influence the development of a character. 
In general, then, we may say that the heritage bequeathed by an indi- 
vidual to its offspring is in most organisms transmitted mainly through the 
nucleus, since it is very largely upon this organ that the development or 
non-development of particular characters in the organism depends; but 
also that the development of the characters in the offspring, however these 


may be transmitted, involves all of the cell organs as well as a complicated 
and orderly series of intercellular reactions and responses. These two 
phases, the transmission of a heritage of factors and the develop- 
ment of the organism's characters as the result of their influence, 
must both be very much more fully known before either can be adequately 

To some of the more cogent evidence upon which these general con- 
clusions are based we shall now turn. 

Bibliography at end of Chapter XVIII. 



The classic researches carried out by Mendel a half-century ago on 
the hybridization of garden peas are now so well known that a detailed 
description of them would be superfluous here. Moreover, since the 
main principles of Mcndelisrn are illustrated in the results of the simplest of 
MendePs experiments, a review of one or two of the latter will for our 
purposes be sufficient. 1 

A Typical Case of Mendelian Inheritance. 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. 129). All the plants 
of the first hybrid generation (Fi) were tall like one of their parents. 
When these tall hybrids were self-fertilized or bred to one another, it 
was found that the second hybrid generation (F 2 ) comprised individuals 
of the two grandparental types, tall and dwarf, in the relative numerical 
proportion of 3:1. It was further found that the tall individuals of this 
generation, though alike in visible characters, were unlike in genetic con- 
stitution: 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 generation both tall and dwarf plants in the 
proportion of 3 : 1, showing that they were hybrids with respect to tallness 
and dwarfness. The dwarf plants of the second hybrid generation (F 2 ) 
produced nothing but dwarfs when interbred; they were "pure" for 
dwarfness. From these facts it was evident that the plants of the F 2 
generation, although they formed only two visibly distinct classes, were 
in reality of three kinds: pure tall individuals, tall hybrids, and pure 
dwarfs, in the relative numerical proportions of 1 :2 :I. 

The explanation offered by Mendel for these phenomena may be 
briefly stated as follows (Pig. 129). The germ cells produced by the 

pure tall plant carry something (now termed a J^ggT, represented here 
\ .. _ 

, l Detailed accounts of the many facts of Mendelism may be found in more special 
wo'rks on the subject. See Morgan et al. 1915, Chapters 1 and 2; Bateson 1913; 
Castle, Coulter et al 1912; Castle 1916; Coulter and Coulter 1918; Babcock and 
Clausen 1918, Chapter 5; Punnet 1919; Darhishire 1911; Morgan K>19; Thomson 
1913; East and Jones 191. 




by T) which makes the resultirg plant tall. The germ cells of the dwarf 
plant carry something (t) causing the dwarf condition. In the first 





FIG. 129. A typical Mendelian cross between tall and dwarf peas, showing dominance 
of the tall over the dwarf condition in the first hybrid generation (Fi), and the 3: 1 ratio of 
tall plants to dwarfs in the second hybrid generation (Fz). At the right is shown the 
corresponding distribution of the Mendelian factors for tallness (T) and dwarf ness (t). 

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 (F\) produces germ cells the two factors for tallness and 
iwarfness separate, half of the germ cells receiving T and the other half 
receiving t. Each gamete therefore carries either one or the other of the 
;wo factors in question, but n^rar a piven gamete is "pure" 

Cither for J 1 or for L This sp y r flgait iinn in the germ cells of factors pre- 
viously associated in the individual without their having been altered by 
this association is the central feature of the entire series of Mendelian 
phenomena, and is often referred to as Mendel 1 s first law. Since, now, 
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) 


FIG. 130. Blending inheritance ("incomplete dominance") in Mirabilis jalapa, showing 
1:2:1 ratio of three genotypes in Ft. (Adapted from Correns.) 

four combinations are possible : a T sperm with a T egg, a T sperm with a 
t egg, a t sperm with a T egg, and a t sperm with a t egg. These four 
combinations result respectively in a tall plant (pure dominant, TT), two 
tall hybrids (Tt and tT), and a dwarf plant (pure recessive, if). It is 
obvious that in the long run these three types will occur in the ratio of 

MendeFs researches on peas included also a study of si# other pairs 
of heritable characters (now known as allelomorph pairs), the two 
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 are entirely independent of each other in inheritance 
(Mendel 's second law; now modified; see p. 384). All these phenomena he 
interpreted on the basis of the hypothesis that .each character is in some 
wav renresented bv a factor in the cells, new combinations of factors 


being formed at fertilization and the members of each allelomorphic pair 
of factors separating when the germ cells are formed. 

The Mendelian proportion of pure forms and hybrids is more easily 
followed in cases of " incomplete dominance." the pure dominants here 
being visibly distinguishable from the hybrids. Such a case is that of 
Mirabilis jalapa, the four-o'clock (Fig. 130). If plants bearing pure red 
flowers (var. rosea) are crossed with those bearing pure white flowers 
(var. alba) the result is an F ] generation of intermediate pink-flowered 
plants. When these pink hybrids are bred among themselves the result- 
ing FZ generation comprises plants of three visibly different types : pure 
dominants with red flowers, hybrids with pink flowers, and pure recessives 
with white flowers, in the numerical ratio of 1:2:1. 

Terminology. We may here introduce certain terms prominent in the 
literature of genetics. The genotype is the entire assemblage of factors which q.ty 
orftfl.njsm actually possesses in its constitution, irrespective of how many of 
tihfisp, may be expressed in externally visible characters. The vhenotypeAs the 
aggregate of externally visible characters, irrespective of any oth^r factors, 
unexpressed in char acters T which may be present in the organism. For illustra- 
tion : in the case of the tall and dwarf peas there are in the second hybrid genera- 
tion (F z ) three genotypes (with respect now only to the Single character pair 
discussed) : TT, Tt, and it, represented respectively by pure tall plants, tall 
hybrids, and dwarfs; but there are only two phenotypes: tall and dwarf, because 
of the fact that 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 constitu- 
tions, and the two can be distinguished only by a study of their progeny. In 
Mirabilis, however, there are in the Ft generation not only three genotypes 
represented, but also three phenotypes, since the i 

the hybrids c^ternntty iinlikf* either of the pure forms. 

An individual is said to be homoz^o^ jor a given allelomorphic 
pair if it has received the same factor from the two parents a pea, for example, 
with the constitution TT or it. If it has both members of the pair,, such as Tt, 
It jsjsajdj/ojpe hetejwzygow. It mav be homozygous for some allelomorphic pairs 
for others^jor it may .._goncejvablx_ Jie _either_hgmozygous or 
ajyLQf itsjgjiaracters. Thus an organism with the genotypic 

3onstitution AABbcc is homoZygous for the characters represented by A A and 
?c, and heterozygous for those represented by Bb. It is thus a pure dominant 
svith respect lo A and a f a pure recessive with respect to C and c, and a hybrid 
#ith respect % B and b. The phenotypic appearance of the organism would be 
letermined by the dominant factors A and B and by the recessive c; a given 
lominant factor dominates only its recessive allelomorph, and not the recessive 
actors belonging to other pairs. It is a common practice to represent dominant 
'actors or characters by capital letters arid their respective recessive allelomorphs 
>y the corresponding small letters. 

The Cytological Basis of Mendelism. Having before us some of the 
priricipal facts of Mendelism and Mendel's interpretation of them, we 



may now turn to the cytological basis of the Mendelian phenomena, and 
inquire what visible mechanism there is in the cell which will in any way 
help us toward an understanding of the striking behavior of the Mendelian 

The behavior of the chromosomes at the critical stages of the life 
cycle as described 'in the chapters on reduction and fertilization must 
first be recalled. (See Fig. 131.) It has been shown that their history 
is as follows. Each parent furnishes the offspring with a set of chromo- 
somes, the two sets (represented in the diagram by A BCD and abed) 
being associated in all the cells of the offspring. When gametes (or 
spores followed later by gametes in the case of higher plants) are to be 

Union of simplex groups 

Pup lex group* 
ABCD *Dod 

Duplex groups 


Simplex groups 

FIG. 131. Diagram showing the history of the chromosomes in the typical life cycle of 
animals. (After Wilson, 1913.) See also Fig. 77. 

formed by the new individual the chromosomes pair two bjjvwo (svnap- 
sis), the two homologous members of each pair coming from the two 
parental sets. In the first maturation division (usually) the two members 
of each pair separate and enter different daughter cells: this is reduction, 
or the separation of entire chromosomes, presumably qualitatively differ- 
ent, instead of qualitatively similar halves of chromosomes as in somatic 
division. In the second maturation division all the chromosomes split 
longitudinally (equationally), so that as the result of the two divisions 
there are four gametes (or spores), two of them differing from the other 
two in chromatin content. The somatic chromosomes are therefore 
segregated into two unlike groups : eachj^amete (or spore) has a single jgt 
of chromosomes, thejget_being composed of one member of each of the 
pairs formed at synapsis. This set represents the contribution made to 
the following generation. 



It will be recognized at once that the above is precisely the sort of 
distribution shown by the characters in MendePs experiments: two groups 


FIG. 132. Mendelian inheritance in black and albino guinea pigs. 



FIG. 133. Chromosome history in the cross represented in Fig. 132, showing the 
parallelism between the distribution of a single homologous pair of chromosomes and that 
of a single allelornorphic pair of Mendelian characters. 

of (factors for) characters are brought together at fertilization and are 
associated in the body of the offspring. When the germ cells are formed 


the (factors for the) two characters forming each allelomorphic pair 
separate and pass to different gametes (or spores). Thus the chromo- 
somes and the characters alike form a duplex group in the body cells and 
a simplex group in the gametes (or spores) : the chromosomes, like the 
character^ formjiew combinati^^ajt^erUlization and arc segregated 
when the gametes (or scores) are formed. In the diagram the letters 
ABCDabcd stand equally well either for chromosomes or for characters. 
In view of these facts it appears extremely probable that chromosomes 
and Mendelian jchara,cters have a definite causal J'^lationship _of _sonie 
kind : it is scarcely conceivable that the exact and striking parallelism 
that they show can be without significance. 

The precise nature of this correspondence between chromosome be- 
havior and character distribution can be even more clearly shown by a 
consideration of the history of a single homologous pair of chromosomes 
in a typical Mendelian cross. If a pure white (albino) guinea pig be mated 
to an individual of a pure black strain the offspring are all black; black 
is completely dominant over white (Fig. 132). If these black hybrids 
are bred among themselves they produce in the F 2 generation three black 
animals to one white, or, more precisely, one pure black to two black 
hybrids to one pure white. Let us now follow a single pair of chromo- 
somes of each of the original animals through these two generations. 

At the left in Fig. 133 are represented the two animals, pure black 
and pure white, their chromosomes being drawn in solid black and outline 
respectively. In the black animal the two chromosomes pair at synapsis 
and separate to the two daughter cells at the first maturation mitosis, 
and split longitudinally at the second, so that each of the gametes re- 
ceives a single chromosome representing a longitudinal half of one of the 
original pair. A similar process occurs in the white individual. Unions 
between the gametes of the two animals now result in the FI hybrids, 
each of which has one chromosome from its black parent and one from 
its white parent (not counting the chromosomes of other pairs). When 
these hybrids form gametes, as is seen at once in the diagram, the pa- 
ternal and maternal members of the chromosome pair separate, with the 
result that half the gametes receive one of them and half the other. 
There are thus two kinds of spermatozoa and two kinds of eggs T one kind 
Carrying the paternal chromosome and the other carrying the maternal 
one. Chance combinations now result in a generation (F 2 ) of animals, 
one-quarter of which have derived both fihrn^ w mps of the nair jp 
question from the black grandparent, one-half of which have derive^ 
one chromosome of the pair from each grandparent, frnd on<^q]ifl,rtfir of 
which have derived them both from the white grandparent. Moreover, 
these animals are respectively pure black, hybrid black, and pure white, 
in the proportion of 1:2:1. Thus it is seen that there is a direct paral- 
lelism, notwiy between chromosome sets and character groups, but alsc 


and T. compactum) 42 (hcxaploid). He concludes that the one-grained 
wheats are the ancestral forms from which the emmer and spelt wheats 
have arisen through changes in chromosome number. This is precisely 
the conclusion which Schulz (1913) and Zade (1914, 1918) had reached 
on other grounds. Kihara (1919) found further that by crossing emmer 
and spelt wheats fertile hybrids with 35 chromosomes could be obtained, 
and that these in future generations produced forms with varying chromo- 
some numbers because of the irregular manner in which the chromo- 
somes are distributed at the time of reduction. (See p. 253.) As a 
general ^rule hybrids produced Jby crossing forms . with differenLchromo- 

jspjne_ numbers are sterile, but when they are fertile and their chromosome 

junnber is odd. Ihro^isj^j^ly^ 

^several generations un.til..the__number again becomes_settled. In some 
r ;ases the number thus settled upon is that of the original ancestor with 
he lower number (the (Enothera mutants of deVries and Stomps cited 
xbove), whereas in other cases (Triticum) it is that of the ancestor with 
the higher number. The manner in which many such changes in number 
occur is not yet known. 

A study of the chromosomes in the genus Crepis has been made from 
this point of view by Rosenberg (1918, 1920). He finds four species, 
including C. virens, with three pairs of chromosomes, eight species with 
four, four species with five, one species with eight, one species with nine, 
and three species with 21. In Crepis the chromosomes differ markedly 
in size, and Rosenberg concludes that the species with three, four, and five 
pairs have arisen through such irregular distribution of the smaller chro- 
mosomes as has actually been observed in the maturation divisions, 
together with recombinations occurring at fertilization. The segmenta- 
tion of the larger chromosomes of the complement is not thought to 

In an extensive investigation of the chromosomes of Zea Mays 
Kuwada (1919) has found cytological confirmation of the conclusion of 
Collins (1912) that this species, which for some years has played a 
conspicuous role in genetical investigations, is in all probability a hybrid 
between Euchlcena mexicana (teosinte) and some other unknown form 
belonging to the nearly related Andropogonese. Owing to their in- 
equality in size Kuwada is able to distinguish what he considers to be 
the chromosomes of the two supposed ancestral derivations in the cells 
of certain races of maize. Thus gemini with components of unequal 
size are frequently observed in the microsporocytes. 

A nimals. The most complete description of the chromosomes in a large 
number of closely related animal species is that given by Metz (1914, 19166) 
for the Drosophilidse. In about 30 species Metz has identified no less than 
12 main types of chromosome groups, all but one of them being found in 
the genus Drosophila. In Fig. 137 are shown diagrammatically the 12 


principal types as they appear with their characteristic arrangements at 
the time of cell-division. Type A is that found in Drosophila melano- 
gaster (formerly known as D. ampelophila), upon which the greater part 
of the genetic work in these flies has been done; it is also characteristic 
of several other species. Here there are two pairs of large bent "euchro- 
mosomes," one pair of sex chromosomes, and one pair of very small 
"m-chromosomes." In some of the other species it is seen that the 
position of one or both of the large pairs is occupied by two pairs but 

<(o> <-;>='(,;>;>% 
. ii, it. it. 






Fia. 137. The 12 principal types of chromosome groups found in the cells of the Droso- 

philidae. (After Metz, 1916.) 

half as large, and there is much evidence to show that these have arisen 
by a segmentation of the large chromosomes. Furthermore, the m- 
chromosomes do not appear in some species, but it is not yet certain 
whether they are actually lost through irregular mitoses or are fused 
with some of the larger chromosomes of the group. Since irregular 
mitoses resulting in abnormal distributions of chromosomes are actually 
observed in Drosophila, and are known to be accompanied by changes 
in the hereditary constitution, there can be little doubt that by this and 
other means all the types of chromosome groups have been derived from 


one or two original types, and that the specific differences exhibited by 
the organisms are related to these differences in their chromosome 

This conclusion is supported by the observations of MeClung, Robert- 
son, and others on the chromosomes of other insect families. In the 
grasshoppers, for example, Robertson (1916) finds that the various 
chromosomes of the complement form a regular graded series and 
can be identified in all the species and genera studied. The nearer the 
relationship the mor$ nearly simjl^r are the 

Robertson states that the degree of relationship is as clearly expressed 
in the nucleus as in the externally visible characters, and that the 
evidence jpHin.fl.tpa f.lmf. Hpanfmt by variation from a common ancestral 
series of chromosomes is paralleled by Hfigrftps of variation in somatic 

Mutations Accompanied by No Change in Chromosome Number. 

In most of the examples of jthis class it has been found that the mutant 
behaves in a strictly Mendelian manner, usually being recessive tO-thc 
type from which it sprang. This observation falls into line with the fact 
that the number and behavior of the chromosomes remain the same ;_the 
operation of the Mendelian mechanism is not disturbed. Consequently 
if the origin of mutations of this class is dependent on the chromosomes 
it must be due to a change of some kind occurring within the chromosome 
and affecting the character of its factors, or genes. That such factor 
mutations An take place is the hypothesis upon which a large school of 
geneticists is attempting to account for many of the observed phe- 
nomena of inheritance. Such mutations may involve either a single 
gene only _(" point mutation ") or a group of ^enes occupying a given 
region of a. chromosome ('^regional njntatJ ""^ Furthermore, they 
may apparently occur eithgrjn the germ cells or in the somatic cells, 
but seem to be most frequent in the former at the time of^jnatration, 
For the reason that only one or two gametes (or spores followed later by 
gametes in most plants) among the large number produced reveal the 
presence of the altered gene in their effect upon the offspring. The 
mutation in the gene must here take place after the multiplication of 
the germ cells has been nearly or quite completed; otherwise the effect 
would be manifested by a larger number of gametes (or spores) . If, as 
is true of the majority of cases, the mutation is such as to result in a 
recessive character, this character does not manifest itself until it meets 
a similarly mutated gene in the homozygous individual. Thus such 
an alteration may remain latent for many generations, or may never 
come to expression at all. 

Factor mutg^jons occurring in somatic (me ri^maticX-Cells result in 
ghat are known as t{ vegetative mutations." These are of two principal 
kinds: bud sports and chimeras. In the case of the bud sport, which is 


believuu to be due to a factor mutation in the very young bucl, the entire 

typic constitution _and_exhibits an appearance often strikingly different 
From that oL the other branches or flowers, of the plant. Such a factor 
mutation occurring in a partially developed shoot or organ results in a 
chimera .^njwhich a jistinct portion of the mature stnjcjture ? commonly a 
sector, differs genotvpically and in appearance from the 
By some geneticists vegetative mutations are thought to 

be due to a somatic segregation of allelomorphic factors in a heterozygous 
individual and their consequent independent activity in different por- 
tions of the body. 

The nature of the change which may thus occur in the gene is unknown, 
since the nature of the gene itself is entirely a matter of conjecture. 
Although it has been suggested that the gene, because of its relative 
stability, may be simply a molecule. JHsjnorc probably a 

colloidal aggregate, possibly enzymatic in nature, which j capable, of 
growth and division. As such it could not be expected to be absolutely 
stable, as some geneticists have thought, but_changes wouldJiL all likeli- 
hood take place occasionally by addjtjon^loss^r .rearrangement jrfjbhc 
constituent atoms of _the_ molecule. The probable rate of change of the 
genes in Drosophila has been calculated by Muller and Altenburg (1919). 
What the agencies are which cause such changes is also unknown. Some. 
e videncejias been brought forward to showjthat genesjnay be modified 
by external lnflucnces x _Mit by many .it .is regarded as of very doubtful 
value. The stimuli to which the genes respond by undergoing some 
constitutional change are probably for the most part internal ones. 
Although the number of ways in which a gene may change is limited by 
its own organization, the possible changes are nevertheless numerous, 
so that it is very probable that many variations which constitute initial 
steps in evolution originate in this manner. 1 

Conclusion. The following paragraphs are quoted from East and 
Jones (1919, pp. 76 ff.): 

"The relation between fact and theory in the Mendelian conception of 
inheritance is this: Various kinds of animals and of plants were crossed and the 
results recorded. With the repetition of experiments under comparatively 
constant environments these results recurred with sufficient regularity to justify 
the use of a notation in which theoretical factors or genes located in the germ cells 
replaced the actual somatic characters found by experiment. Later, the ob- 
served behavior of the chromosomes justified localizing these factors as more or 
less definite physical entities residing in them. Now the data from the breeding 
pen or the pedigree culture plot and the observations on the behavior of the 
chromosomes during gametogenesis and fertilization are facts. The factors are 
part of conceptual notation invented for simplifying the description pf the brqed- 

1 See the discussion of these points by Cpnklin (1919-1920). 


ing facts in order to utijigg them for thejaur.pQses.Qf prediction, just as the chemi- 
cal atom is a conception invented for the purpose of simplifying and making 
useful observed chemical phenomena. As used mathematically, both the geneti- 
cal factor and the chemical atom are concepts, but biological data lead us to 
believe that the term factor represents^ biological reality of whose nature jwe 
are ignorant, just as a molecular formula represents a physical reality of a nature 
yet but partly known. 

>l With this distinction in mind, one may treat the factor or the atom from 
two points of view, either as a mathematical concept or a physical reality. As 
a mathematical_concept it is the unitjyf heredity, andji unit in any notation must 
1x3 stable. If one describes a hypotheFical unit by which to describe phenomena 
and this unit varies, there is really no basis for description. He is forced to 
hypothecate a second fixed unit to aid in describing the first. 

" The point at issue in this connection may be explained as follows : Characters 
do^vary from generation to generation, and the question to be decided is, how 
much of this variation is due to the recombination of factors (considered now as 
physical entities) and how much is due to change in the constitution of the 
factors themselves . . . 

" . . . We believe there should be no hesitation in identifying the hypotheti- 
cal factor unit with the physical unit factor of the germ cells. Occasional changes 
in the constitution of these factors, changes which may have great or small 
effects on the characters of the organism, do occur; but their frequency is not 
such as to make necessary any change in our theory of the factor as a permanent 
entity. In this conception biology is on a par with chemistry, for the practical 
usefulness of the conception of stability in the atom is not affected by the knowl- 
edge that the atoms of at least one element, radium, are breaking down rapidly 
enough to make measurement of the process possible." 

Bibliography at end of Chapter XVIII. 



In the present chapter attention will be devoted to the cytological 
aspects of the inheritance and determination of sex. 1 Much that is not 
cytological in nature will enter into consideration, but it is far from 
irrelevant: it has a direct bearing on the main cytological problem and 
must be included in order that the latter may be placed in its proper 
setting, and that the larger problem of sex may not be misrepresented by 
being considered only from the cytological point of view. 

From early times few essentially biological matters have been of more 
interest to man than that of the determination of sex. Until recent 
years this interest has been prompted largely by practical motives: the 
ability to control sex in man and his domesticated animals is something 
which has long been desired. Of the many early ideas entertained on the 
subject the majority were the outcome of defective generalization and 
superstitious conjecture, and may be encountered in thinly veiled form at 
the present day, but a review of them all would be out of place here. The 
modern scientific interest in the problem of sex is far from being a purely 
practical one. The great bulk of recent research has been done not 
merely for the sake of the practical benefits which knowledge in this 
field might confer, but mainly in the hope that it may lead to an under- 
standing of the origin, nature, and biological significance of sex itself, 
and to a solution of some of the problems of heredity. For this reason 
studies have not been confined to man and his economically important 
animals; any animal or plant, no matter how obscure, that will yield 
evidence is exhaustively investigated, and there can be no doubt that 
knowledge gained from such studies will, if sound, be directly applicable 
to practical ends. 

Experimental Evidence for Sex-determination. During the closing 
decades of the nineteenth century many researches were carried out in the 
hope of identifying the controlling 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. Among all the ideas put forward the 
most suggestive, in view of what has more recently been ascertained, 

1 See Correns (1907), Correns and Goldschmidt (1913)*Morgan (1913), Doncaster 
(1914), and the works cited at the beginning of the preceding chapter. 


SEX 355 

was that of Geddes and Thomson (1889), namely, that the two sexes 
differ primarily in the character of their metabolism, the female sex 
being characterized by the preponderance of anabolic processes and the 
male sex by those essentially katabolic in nature. This conception is 
important not only in connection with the question of sex control, but 
chiefly with respect to the more fundamental problem of the nature of 
sex itself. 

The long early period during which sex was 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 automatically 
regulated by some mechanism or condition within the cell, and as rela- 
tively unalterable by external agencies. , This conclusion, definitely 
reached by Cu&not (1899) for animals and by Strasburger (1900) for 
plants, received the support of a number of experimental researches on 
animals and dioecious plants. Some of the latter will first be mentioned. 

It was found by Blakeslee (1906) that in certain strains of a mold, 
Phycomyces, there are produced in the germ sporangium two kinds of 
asexual spores, which give rise to "plus" and " minus" mycelia respec- 
tively. The "plus" (male?) mycelium later produces spores which 
develop only into "plus" mycelia and so on indefinitely, while the 
"minus" (female?) strain perpetuates only the "minus" condition: in 
both cases the sex seems to be fixed by some mechanism functioning at 
the time of spore formation. 

In certain dioecious mosses (l. and m. Marchal 1906, 1907) two 
kinds of spores are produced in equal numbers in the capsule. Those of 
one kind develop into male gametophytes (bearing antheridia only) and 
those of the other kind produce female gametophytes (with archegonia 
only). In no way were the Marchals able to alter the sexes of these 
plants. Furthermore, new gametophytes formed by regeneration from 
the old ones were just as rigidly fixed as to sex/]JProtonemata regenerated 
from the tissue of the sporophyte, however, gave rise to leafy branches 
bearing both antheridia and archegonia. Both sex potentialities were 
therefore present in the sporophytic tissue and in the diploid game- 
tophytes regenerated from it, whereas the normal haploid gametophytes 
produced from spores were either purely male or purely female. 1 The 
gametophytes of Marchantia (Noll; Blakeslee 1906) are similarly fixed 
as to sex : if propogated repeatedly from gemmae the sex in any given line 
remains the same in spite of alterations in the environmental conditions. 
In Sphcerocarpos Douin (1909) and Strasburger (1909) were able to show 
that two spores of a Single tetrad produce male gametophytes while the 
other two produce females/J 

The obvious conclusion to be drawn from the above cases is that in 
such forms a .,s^arat|<M^crf Jil^_sexes Jakesjplace^ during sporpgmesis. 

1 Diagrams of these experiments are given by Morgan (1919a, pp. 152-3). 


Both sexes are represented in the sporophyte (diploid) generation, as 
shown particularly by the mosses, but the spores, though morphologically 
similar, are of two distinct kinds : male-producing and female-producing. 
Since it is precisely at sporogenesis that reduction occurs, the natural 
inference is that a separation of qualitatively different sex-factors of some 
kind occurs in the heterotypic division, the sexes of the future gameto- 
phytes thus being automatically determined. J 

That a somewhat similar qualitative difference may exist in the 
microspores of many angiosperms, resulting in the frequent dioecious 
condition of the sporophyte, was concluded by Correns (1907) from his 
researches on Bryonia hybrids. He was best able to interpret the 
phenomena observed on the hypothesis that the eggs are all similar in 
having the female sex " tendency;'' that there are two kinds of micro- 
spores and hence two kinds of male gametes, with male and female 
"tendencies" respectively; and that in the sporophyte the male tendency 
dominates the female. Darling (1909) was inclined toward a similar 
conclusion for Acer Negundo. 

^ Strasburger (1910) in a general discussion of the subject growing out 
of his researches on Elodea, Mercurialis, and other plants, summarized 
the situation in plants as follows. In monoecious mosses the separation 
of the sexes occurs in the somatic divisions at the time the sex organs 
are formed. The separation has been secondarily joined with reduction, 
so that in the derived dioecious mosses it occurs at sporogenesis. In the 
homosporous pteridophytes it takes place at some stage in the game- 
tophyte before the formation of the sex cells, as in monoecious mosses, 
though in some cases (Equisetum, Onodea, and others) a marked physio- 
logical dicecism is present. In hetcrpsporQjus pteridophytes and all 
seed plants the garnetophytes are dioecious but the sporophytes may be 
either monoecious (hermaphroditic) or dioecious. In monoecious forms the 
sexes are separated at some stage prior to the development of megaspores 
and microspores, whereas in dioecious forms it must take place at some 
other point in the life cycle, since the two kinds of sporophytes (mega- 
spore-bearing and microspore-bearing) are distinct from their initial 
stages. There is some evidence to show that such dioecism is due to a 
differentiation among the pollen grains and hence among the male 
gametes: some grains have a strong male tendency which dominates the 
female tendency of the egg, male progeny resulting; while other grains 
have a weak male tendency dominated by the female tendency of the egg, 
female offspring being produced. In brief, as sex separation became 
joined with reduction in forms with monoecious gametophytes, the 
dioecism of the gametophyte and heterospory (first physiological and then 
morphological) followed; and this in turn led to the dioecism of the 
sporophyte also. Finally, in such advanced forms there appears to be a 
differentiation among the spores of one sex, theinicrospQres, giving male 
gametes of two types. The sex of the resulting offspring therefore 

SEX 357 

depends here upon the type of male gamete functioning, as is known 
to be the case in so many animals. It has been suggested by Allen (1919) 
that the separation of the sex-factors in dioecious seed plants may possibly 
occur in the division which differentiates the two male nuclei in the 
pollen tube, rather than at the divisions producing the microspores. 
That this interpretation cannot be applied to Mendelian factors in general 
is evidenced by the fact that in maize hybrids the embryo, with very 
rare exceptions, has been found to be like the endosperm with respect 
to factors introduced by the pollen parent. So far as these factors are 
concerned, therefore, the two male nuclei must be qualitatively similar. 

Strasburger's conclusion regarding monoecious mosses is confirmed 
by the recent experiments of Collins (1919) on Funaria hygrometrica* In 
this species the gametophytes arising from spores are bisexual (monoe- 
cious), but if gametophytes are produced by regeneration from the 
antheridia or perigonial leaves of a single "male flower," they all bear 
antheridia only. Collins thinks it possible that dicecism may have 
arisen as a result of vegetative multiplication following such a somatic 
segregation in the tissue of the monoecious gametophyte. 

In animals also there is much evidence, aside from that afforded by 
the chromosomes to be discussed below, in favor of the view that sex is 
internally controlled. The following illustrative cases may be cited. 
The egg of the bee may develop either parthenogenctically or after 
fertilization by a spermatozoon: in the former case a male (drone) results 
and in the latter a female (queen or worker, depending on the nature of 
the food). In Phylloxera (Morgan 1906, 1908, 1909, 1910) there are two 
sizes of eggs produced by the females of the second parthenogenetic 
generation: both may develop parthenogenetically after forming one 
polar body, the larger ones into females and the smaller into males. 
Fertilized eggs always develop into females. In Hydatina (Whitney 
1914, 1916, 1917) the female-producing eggs form one polar body while 
the male-producing eggs form two. Two kinds of eggs are also produced 
in Dinophilus (Malsen 1906; Nachtsheim 1919), but in this form both 
are regularly fertilized. In the nine-banded armadillo (Newman and 
Patterson 1909, 1910) one fertilized egg commonly gives rise to four new 
individuals, and the four are invariably all male or all female. Analogous 
instances of polyembryony are also known in insects. Human twins, 
if "identical" (produced by the same egg), are invariably of the same 
sex; if " fraternal" (produced by different eggs) they may or may not be 
of the same sex. It would therefore seem that sex in such cases as these 
must be determined either in the egg before fertilization or at the moment 
fertilization occurs. 1 

1 The determination of sex in the egg before fertilization, as in Phylloxera and 
Dinophilus, is termed by Haecker "progamic" sex-differentiation; if determination 
occurs at the moment of fertilization, as in the bee, it is "syngamic" sex-differentia- 
tion; and if it occurs after fertilization, as may possibly be the case in some forms, it 
is "epigamic" sex-differentiation. 


^ W ,<A*. C> *"*" 1 

Sex-Chromosomes. The theory of the automatic determination of 
sex and its relative, if not absolute, fixity has had one of its strongest 
supports in the results of certain researches on the spermatogenesis of 
animals. In 1891 Henking noticed in certain insects that half of the 
spermatozoa contain an extra body, which he thought might be a 
nucleolus. It was subsequently shown by Paulmier (1899), Montgomery 
(1901), and de Sinty (1901) that this body is not a nucleolus but an 
extra or " accessory " chromosome. Henking's misinterpretation had 
apparently been due to the fact that the accessory chromosome often 
does not transform into a portion of the reticulum along with the 
other chromosomes ("autosomes"); but remains condensed and closely 
resembles a nucleolus. Half of the spermatozoa in these animals there- 
fore have one more chromosome than the others: hence the male is 
said to be "heterogametic," or "digametic." It was at once suggested 
by McClung (1902) that the accessory chromosome in some way 
determines sex that eggs fertilized by one kind of spermatozoon 
develop into females, while those fertilized by the other kind become 
males. This represents the first attempt to connect a given character 
with a particular chromosome. An extensive series of researches was 
now undertaken by Wilson, Miss Stevens, McClung, and a number of 
other cytologists, who discovered among insects many striking instances 
of the phenomenon. Accessory chromosomes (also referred to as oex- 
chromosomes, heterochromosomes, idiochromosomes, x-chromosomes, 
x-elements, and supernumerary chromosomes) of a number of different 
types were found, not only among insects, where they are best displayed, 
but also in certain echinoderms, nematodes, mollusks, and vertebrates, 
including birds and man. A number of representative cases will now 
be described. 

Male Heterogametic. In the threadworm, Ascaris (Bovcri) (Fig. 138) 1 
there is in each body cell and primary sperriiatocyte of the male a single 
heterochromosome, which seems to be attached to, or to constitute a 
portion of, one of the four autosomes. At the time of reduction this 
passes undivided to one daughter cell at the first division and divides at 
the second, so that half of the sperms only receive it. In the female there 
are two such heterochromosomes, every egg receiving one. If, now, an 
egg is fertilized by a sperm without a heterochromosome the resulting 
individual has only one (that from the egg) and develops into a male. 

1 For the sake of brevity and clearness these diagrams are drawn as if only one 
maturation mitosis occurred in spermatogenesis and oogenesis. It will be understood 
that there are two divisions, resulting in four sperms instead of the two shown, and 
in an egg and three polar bodies instead of the two eggs shown. The diagrams. merely 
indicate that two sorts of sperms and one kind of egg are produced, and how this 
is brought about. In the cases of Lyg&us and Prionidus the number of autosomes 
shown (4) is not the actual number present. See the review of the subject of sex 
chromosomes by Wilson (1911). 

SEX 373 

to their archegonia, but the male gametophytes could not be made to 
develop archegonia. In Osmunda regalis japonica and Asplenium nidus, 
which are monoecious, Nagai (1915) found that the concentration of the 
Knop's nutrient solution used has a controlling influence over the kind 
of sex organ appearing, the number of antheridia in general decreasing 
with the concentration. 

These results, taken together with the fact that many gametophytes, 
especially those of homosporous pteridophytes, are monoecious, show that 
the capabilities of both sexes can be present in the haploid nucleus, as 
Strasburger thought, although in many forms the visibly developed sexes 
may be automatically determined by some cell mechanism. 

General Discussion. We have now reviewed some of the evidences 
which have led to two general theories of sex and its determination. One 
theory represents an attempt to account for the phenomena in question 
on the basis of a morphological cell mechanism whereby Mendelian or 
other factors are distributed in a definite and fixed manner, whereas on 
the other theory it is held that they are the results of a physiological 
differentiation manifesting itself chiefly in alterable levels of metabolism. 
Although these two conceptions may appear to be mutually exclusive 
if expressed in too uncompromising a form, both must contain elements 
of truth. It is beyond question that the two manifestations of sexual 
differentiation, the physiological and the morphological, are both of 
importance and cannot be ultimately irreconcilable:* our task is to 
determine their relative significance and to discover the nature and 
degree of their mutual interdependence. It seems clear that the digam- 
etic condition when present in dioecious forms does regulate the ratio 
of the sexes: under all ordinary circumstances the sex of the individual 
is here dependent upon the kind of gamete which gives rise to it (or the 
kind of spore in the case of certain gametophytes). But it is to be 
emphasized that the dimorphism shown by such gametes or spores is not 
entirely a morphological one, or even mainly so : in many cases no morpho- 
logical difference can be detected although the two are clearly different in 
physiological behavior, as shown by the spores of Phycomyces and 
certain bryophytes. It is generally inferred that here a structural 
difference, although invisible, is nevertheless present. 

In this connection it may be recalled that the differences between the 
male and female gametes, irrespective of any differentiation which may be 
present among those of either kind, are both physiological and morpho- 
logical. The primary characters of sex are those possessed by the 
gametes themselves, and the principal distinction between the male and 
female gametes seems to be a physiological one which is manifested in 
their mutual attraction and fusion. Any visible morphological differ- 
entiations that they may possess are to be regarded as secondary adapta- 
tions to unlike functions, because of the fact that in many of the lower 


organisms there is no discernible structural difference between the 
male and female gametes, and further because structural differences 
may be annulled in certain instances (some gregarines). Any material 
differences present in visibly similar gametes are more probably chemical 
in nature, the structural difference being of a molecular order. Indeed, 
there is probably no physiological difference without a structural differ- 
ence of this sort. If the term structure be extended to include molecular 
constitution the discussion over the relative priority of structural and 
physiological differentiation becomes futile, for at this level the two are 
aspects of one and the same change. It is only when we restrict the term 
structure to the grosser, visible features that we can speak of physiological 
differentiation as preceding alteration in structure. Ultimately structural 
and functional changes are indistinguishable. Just as in the gametes 
of the two sexes, so also in the unisexual individuals which the gametes 
produce there may be striking differences of both morphological and 
physiological natures; but if we use the term morphological only with 
reference to visible features the primary distinction between the sexes 
in organisms of all grades is apparently one of physiological state, this 
distinction and its result (sexual reproduction) being of the greatest 
biological importance. 

Taking into consideration all organisms, low and high, it seems 
probable that any dimorphism among the gametes of one sex or the other 
has in some way been developed in connection with the maintenance of 
the above mentioned difference in physiological state in organisms of a 
certain level of advancement. Different organisms show all degrees in 
the differentiation among the gametes of one sex: some are marked by an 
absence of any visible difference either in the gametes or in the her- 
maphroditic individuals produced; in others the gametes (of one sex) are 
visibly similar but result in male and female individuals in regular ratio ; 
and finally there are those in which the gametes are of two kinds both 
physiologically and morphologically, the two kinds controlling the pro- 
duction of individuals of the two sexes. It is in organisms of the last type 
especially that the question of sex-determination finds the adherents of 
the chromosome-Mendelian theory and those of the metabolic theory 
in disagreement. Is the sex of the individual inevitably dependent 
upon the type of gamete functioning (usually the kind of sperm fer- 
tilizing the egg), or is it possible to overcome the effect which the 
chromosome mechanism may have by influencing sufficiently the 
metabolism of the organism? If the sex of an individual is so changed, 
does the chromosome mechanism undergo a corresponding alteration? 

Those who have developed the chromosome-Mendelian theory have 
perhaps too often held that the two sexual states, maleness and female- 
ness, are in their ultimate analysis mutually exclusive that they are two 
fundamental and qualitatively different alternative characters depending 

SEX 375 

unalterably upon unit factors. The hereditary factors or genes are 
usually regarded by geneticists as unmodifiable except by sudden muta- 
tions. Failure to distinguish between the modification of genes and the 
modification of the interaction of genes during ontogenesis has led many 
to the view that the sex of the individual must be rigidly fixed at fertiliza- 
tion in digametic and dioecious forms, or at reduction in the case of dioe- 
cious gametophytes like those of Sphcerocarpos. It is very difficult ta 
reconcile any inflexible theory of this nature with the great diversity of 
situations known without resorting to hypotheses of somatic segregation 
of factors, alterations in dominance, and other assumptions not well 
supported by observational evidence. Such difficulties are encountered 
in the common hermaphroditic condition of gametophytes, which are 
haploid; in the possibility of causing the development of the second 
sex in gametophytes normally unisexual (Onocled) ; and especially in the 
numerous cases of sex intergrades, in which it is possible not only to con- 
trol the relative amounts of maleness and femaleness in hermaphroditic; 
forms, but also to produce all intermediate grades between male and 
female individuals, and furthermore to reverse the sex in unisexual forms, 
even in certain species with sex-chromosomes (moths and probably 

If, in accordance with the ideas of many biologists, sex is held to 
be a 'quantitative, "fluid" character associated with a continuous series 
of physiological states which may pass into one another, the way is open 
for the explanation on a common basis of all cases of hermaphroditism in 
both haploid and diploid individuals, of sex intergrades, and of the experi- 
mental modification of sex. At the same time the influence of the sex- 
chromosomes or even of smaller factors within them may be allowed. 
As Riddle (1917) states, organisms have, had the problem of producing 
germs of two metabolic levels, and in some cases this has led to the 
establishment in the two sexes of two amounts of chromatin or even of two 
different chromosome complements. The sex-chromosomes, or units 
contained within them, act with others in the maintenance of two 
diverse levels of metabolism in the gametes and in the offspring, and with 
these levels are correlated the two conditions which we distinguish as 
male and female. Even if the sexes in such cases do not differ in the 
quality of their chromatin, they at least differ quantitatively in this 
respect, in agreement with the theory that sex is a quantitative character. 
The chromosome difference being only one factor in a complex system 
producing the two sexual states, and no single element in this system 
being the sole determiner of sex, it is not impossible that the effect of this 
one factor should be annulled by sufficiently altering the other factors 
and thus modifying the action of the factorial system as a whole. The 
same is to be said of other characters also. What an organism inherits 
is not simply this or that character or sex, but rather a tendency to 


develop a definite group of characters, including a particular sex, under 
a given set of environmental conditions. 

In those organisms possessing heterochromosomes the sex of the 
individual under all ordinary circumstances is dependent upon the kind 
of sperm (or, in some cases, the kind of egg) functioning at fertilization, 
and does not change thereafter. Furthermore, it apparently cannot be 
changed by many methods commonly supposed to be efficacious in this 
respect. So far the chromosome theory is valid; but it does not follow 
from this that the sex which is characterized by a certain physiological 
state and is correlated with a certain type of chromosome complement 
and a variety of secondary sexual characters, is so firmly fixed that it 
cannot be altered by any extraordinary means. The metabolic state, 
even though its regulation may be accomplished in part through a visible 
mechanism, is the resultant of a complex series of reactions which may be 
interfered with at many points. In some cases this metabolic state has 
been artificially altered to a degree sufficient to bring about an actual 
reversal of the sex. It is admitted that other heritable characters de- 
finitely associated with constant genes are greatly modified in the manner 
and degree of their expression by environmental influences, and the 
evidence now at hand indicates that no exception to this rule can be made 
in the case of sex. 

In criticizing the results and interpretations of Riddle, Morgan (1919a) 
points out that the behavior of a certain sex-linked character worked out 
by Strong (1912) indicates that the females which were " changed into 
males " have the male chromosome complement, and that sex is as much 
a matter of chromosomes here as elsewhere. He declares further that 
there is as yet no known case in which the sex determined by a chromo- 
some mechanism has been changed by other agencies in spite of the 
chromosome arrangement. The evidence here points to the conclusion 
that when an alteration of the sex is induced, this does not occur with- 
out a corresponding alteration in the chromosome mechanism. In Droso- 
phila, however, Sturtevant (1920) finds that the intersexes observed by 
him are modified females with the usual two -XT-chromosomes. Here, 
therefore, certain male characters at least are present in an organism with 
the female chromosome complement. 

The number of instances of change of sex in forms normally controlled 
by a chromosome mechanism will probably increase as the nature of 
sexual differentiation becomes more fully known and as experimental 
technique improves; but it is also probable that in animals the sex of 
which we are most desirous of controlling, practical difficulties may pre- 
vent the attainment of satisfactory results. Slight differences in the 
responses of the two kinds of male gametes (or female gametes) might 
conceivably make possible a control over the kind functioning, but it 
seems more probable that the sex of the individual will be found to be 

SEX 377 

more easily influenced, if at all, after fertilization. But it is quite un- 
known whether or not an individual which had undergone a reversal of 
sex would be as successful biologically as a normal one. Unusual fea- 
tures may be expected in a sexually functional organism with the chromo- 
some complement normally accompanying the other sex, if such an 
organism should be found; but such interesting questions can only be 
answered by the facts yielded by further research. 

All questions of sex control are secondary to the main problem of the 
ultimate nature of sex, a problem which reveals itself with increasing 
clearness as primarily a physiological one. The question of the origin 
and significance of sex is one which lies outside the scope of this work. 

Bibliography at end of Chapter XVIII. 


In Chapter ^y attention was directed to the remarkable parallelism 
jvvhich exists between the distribution of the M_endelian characters and 
that of the chromosomes. A vast number of breeding experiments with 
both plants and animals have shown that nff combinations of characters 
are formed at the time of fertilization, whenjbwo parental_sets of chromo- 
somes are brought togethe^and^that a segregation of characters occurs 
at the time of reduction, when the chromosomes are sorted out into two 
groups.. Moreover, the distribution^of a single allelpmorphic pair_j)f 
jMendelian characters parallels precisely that of a single homologous pair 
qfjchrompsomes. These facts indicate clearly that chromosomes and 
characters are in some manner causally related. This conclusion is 
strongly supported by the cytological aspects of sex inheritance, maleness 
and femaleness in a large number of reported cases being definitely corre- 
lated with the activity of certain distinguishable chromosomes. 

It has also been pointed out that the hypothesis upon which these 
phenomena are generally interpreted is that the characters are repre- 
sented in the chromosomes bv material factors, or genes T which in some 
way control the development of characters in the individual. Since, now, 
an organism usually has many more Mendelian character pairs than it has 
chromosome pairs, one pair of chromosomes must as a rule carry genes 
iomnore than one pair of characters. Furthermore, the different pairs 
of_chromosomes are entirely independent of one another in distributign. 
It would therefore follow that if two allelomorphic character pairs have 
thfiJL genes located in different chromosome pairs, they will be quite 
independent of each other in their inheritance through a series^of genera- 
tions; whereas^if their genes are lqcatgd_jtf jbhe_ samg^pgir _pf chromp* 
somes^the^^ be inherited^ together. The latter condition the 
persistent association of characters belonging to different allelomorphic 
pairs through a series of generations actually exists and is known as 
linkage. ^ 

The phenomenon of linkage was discovered in 1906 by Bateson and 
jPunnett in the sweet pea. They found flower color to be linked with the 
shape of the pollen grain: purple flowers nearly always had long grains, 
while red flowers had round grains. The possible relationship between 
linkage and the chromosome hypothesis was pointed out byJLockJn the 
same year. Linkage relations have since been worked out in a consider- 




able number of plants and animals, and are especially well known irt 
the case of the fruit fly, Drosophila melanogaster, owing to the exhaustive 
researches of Morgan and his coworkers. 

A Typical Case of Linkage. As a typical example may be taken the 
following case of linkage in Drosophila (Fig. 145). A male fly with white 
eyes and yellow body is mated to a female with red eyes and gray body. 



FIG. 145.- 

-Linkage in Drosophila. Red eyes in black ; gray bodies stippled ; white eyes 
and yellow bodies unshaded. 

The flies of the Fi generation all have red eyes and gray bodies, since red 
is dominant over its allelomorph white, and gray is dominant over its 
allelomorph yellow. If, r now, the females of this generation are " back- 
crossed " to males with both of the recessive characters, 1 white and yellow, 

1 This back-crossing to the pure recessive is the common method of testing the 
genotypic constitution of hybrids. 


flies of four types appear in the next generation, as shown in the dia- 
gram: white-yellow, white-gray, red-yellow, and red-gray. Since one 
parent in this last cross is a double recessive, these results show that 
the F\ red-gray female must produce eggs of these four genotypic 

All four types, however, are not produced in equal numbers. Those 
flies with the same combinations as were shown by their grandparents, 
white-yellow and red-gray, together comprise 99 per cent of the total 
number; only 1 per cqnt show the other possible combinations, white- 
gray and red-yellow. It thus appears that if the two characters, red 

a hybrid together (i.e., contributed b 

same parent) they cpmg out together in the next generation in nearly all 
cases : they are definitely ^ linked^nd^this is explained on the hypothesis 
that their genes are located in the same chromosome. The same is 
obviously true of their respective allelomorphs, white eyes and yellow 
body: their genes are carried in the other chromosome of the homologous 
pair. Were the two allelomorphic pairs of genes carried in different pairs 
of chromosomes no such linkage would occur : the two characters red and 
gray, and similarly the two characters white and yellow, would then be 
present together in 50 per cent of the flies, the chance frequency, rather 
than 99 per cent. How it is that the linkage is broken in some cases, 
giving 1 per cent with exceptional combinations, is a question to which 
we shall return later in the chapter. 

Sex-linkage. A very interesting special case of linkage is seen in 
the phenomenon of sex-linkage, which may be illustrated by the following 
example (Fig. 146) (Morgan 1910). If a red-eyed wild male is mated to a 
white-eyed female (a member of a race descended from -white-eyed 
mutants) the F \ individuals are white-eyed males and red-eyed females color has hf>pn transferred from onfi SPY to thft nt.hfty ; a. nf 

" criss-cross " inheritance. If these FI flies are bred together, the F 2 
generation comprises four types: red-eyed males and females, and white- 
eyed males and females. Turning now to the chromosomes, if the dis- 
tribution of the sex-chromosomes is followed through these generations 
this striking fact is revealed : red eye color appears in every fly, male or 
female, which possesses the .XT-chromosome of the original red-eyed male; 
and white eyes appear in every male which receives one of the X-chromo- 
somes of the original white-eyed female, and in every female receiving 
two of them. This is taken by Morgan to mean that the original ixiale's 
^-chromosome carries the dominant factor for red eyes, while each of 
the X-chromosomes of the original white-eyed female carries a recessive 
factor for white eyes. In all the flies it is seen that the presence of one 
Jf-chromosome is correlated with maleness, and that of two -XT-chromo- 
somes with femaleness (compare Fig. 140); and that the two types of 
eye color under consideration follow the distribution of these chromo- 



somes they are sex-linked characters. 1 So far as is known, the F- 
chromosome of the male carries no sex- or sex-linked factors. This 
general interpretation is directly applicable 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 F\ and F% are different: in F\ all flies 
of both sexes have red eyes, while in F z all the females and one-half of 
the males have red eyes, white eyes appearing only in one-half of the 
males. (See Morgan et al. 1915, pp. 16-20; Babcock and Clausen 1918, 
pp. 74-77.) 

FIG. 146. Sex-linkage in Drosophila. Three successive generations at left; red eyes 
shown in black. The history of the sex-chromosomes through these generations shown at 
right; X-chromosome of original male shown in black. (Adapted from Morgan.) 

In such cases as the above it is evident that characters other than 
sex may be referred to certain chromosomes of the complement: it is 
possible not only to tell which chromosomes have to do with sex, but 
also to identify the ones concerned in the production of red and white 
eye colors. A large number of such sex-linked characters have been 
identified in Drosophila, and several have been found in other animals. 
Human colorblindness is a character which is inherited in a manner 
analogous to that of sex-linked characters in Drosophila, and its me- 
chanism is apparently the same. The presence of this defect more 
commonly in men than in women, and its appearance in so few individ- 
uals in affected lines, are due to the fact that it is both a recessive and a 

1 Sex-linked characters are not to be confused with sex-limited characters. The 
latter are those found exclusively in one sex, and are now referred to as secondary 
sexual characters. 



sex-linked character, precisely like white eyes in Drosophila. It occurs 
in a woman only if both of her ^-chromosomes bear factors for it, 
which means that such a factor must have been received from each 
parent; whereas one such factor is sufficient to produce colorblindness in 
a man, because his F-chromosome carries no factors which might domi- 
nate 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. From these facts it follows that a 
colorblind woman transmits the defect to all of her sons and to half of 
her grandsons and granddaughters; whereas a colorblind man transmits 
the defect to none of his children and only to one-half of his grandsons. 1 

The first sex-linked character known in plants was that of narrow 
rosette leaves in the red campion, Lychnis dioica (Shull 1910, 1911), a 
plant which appears to have the XY type of sex inheritance, but in which 
no distinguishable sex-chromosomes have been identified. 

Non-disjunction. The chromosome interpretation of sex and of 
sex-linkage has received an interesting confirmation in a phenomenon 
discovered by Bridges (1913). In a certain strain of Drosophila the 
white-eyed females were observed to give rise to a certain proportion of 
" unexpected " forms. Most of their offspring (92 per cent) were red-eyed 
females and white-eyed males, as expected in such an experiment, but 
some of them (8 per cent) were white-eyed females and red-eyed males. 
A long series of crosses showed that these results could be accounted for 
if it were assumed that in the original white-eyed female both of the X- 
chromosomes passed together to one pole in the reduction division instead 
of separating as they should. This was termedgo^-dz's?^f {foff (Fig. 147) . 
As a result the eggs, instead of having the normal single X -chromosome, 
would have either two or none, and the distribution of the sexes and the 
sex-linked characters would be altered in the manner observed. In a 
cytological examination of the flies in which these abnormal phenomena 
appear Bridges showed that this non-disjunction of the X-chromosomes 
does occur occasionally in the female (Fig. 148). The chromosome 
theory thus received confirmation. < *j\.n abnormal distribution of the 

in hfl.n 4 wif.h an fl.hnnr.Tnq,] 

sex-linked factors" (Morgan). Additional genetic and cytological data 
have since been furnished by Bridges (1916) and Safir (1920). 

Linkage Groups. An extensive series of studies on linkage relations 
in various plants and animals has brought out the fact that ffi^ Mfimfolift-fl 
characters of a given organism fall into a certain number of ."linkagp 
groups," the members of each group being linked to one another in 
variou^ degrees but showing no linkage with the members of other groups. 
It appears further, when the relationships of enough characters have 
been worked out, that jhe number of linkage groups is the same a 

1 This case is fully explained by Babcock and Clausen (1918, p. 197). 



jpf the chromosome pairs. Drosophila melanogaster, in which linkage 
relations have been most fully analysed, has four pairs of chromosomes 
(Fig. 148) : two large " euchromosome " pairs, one pair of sex-chromosomes, 

M- 000^0 

IKJjLJ Kl*S V y N -- X ^~S 

FIG. 147. Non-disjunction and its results in Drosophila. The two large circles in 
first row represent male and female flies producing sperms and eggs respectively. Non- 
disjunction in the female gives 2 kinds of eggs, with XX and with no sex-chromosomes, 
instead of the normal single kind with one X. At fertilization there are possible 4 combi- 
nations rather than 2, as shown in the large circles of second row. Owing to the several 
ways in which her 3 sex-chromosomes may be distributed at maturation, the female repre- 
sented by the third circle produces 4 kinds of eggs. When mated to a normal male (below 
horizontal line) with his 2 kinds of sperms, 8 combinations are possible (last row). Nos. 
1, 4, and 5 are normal flies and give^the usual types of progeny. Nos. 2, 6, and 7, owing 
to the presence "of 3 sex-chromosomes, give exceptional results when bred. Types No. 3 
and No. 8 do not appear in the cultures, probably because they die very early. The 
original male has red eyes and the original female white eyes. Red eyes (represented by 
dots) appear in every fly bearing the JSf-chromosome of the original male, as in Fig. 146. 
Compare Morgan 1919a, Figs. 93 and 94. (Diagram based on data of Bridges and Morgan.) 


FIG. 148. The chromosomes of Drosophila melanogaster as they appear during mitosis in a 
female, a male, and a non-disjunctional female. (After Morgan.) 

and one pair of very small "m-chromosomes." The Mendelian charac- 
ters in Drosophila fall into four linkage groups, and it is noteworthy 
that one of these groups contains only two known characters. Each 


jhromosome pair therefore seems to be responsible for a certain group 
of characters. It has been shown above that one of these groups, 
the sex- and sex-linked characters, can be definitely assigned to the pair 
of sex-chromosomes; and Morgan further believes that the factors 
for the two characters of the small linkage group are located in the 
m-chromosomes. The two remaining linkage groups, which contain 
many characters each, are assigned to the large euchromosome pairs. 
Each chromosome is accordingly regarded as a body containing the fac- 
tors or genes for a considerable number of characters; and on the basis 
of the evidence to be presented below it is concluded that these genes, 
differing thus in their hereditary potencies, are arranged in the chromo- 
some in a linear series as suggested by Roux many years ago. 

In plants the best known cases of linkage are in Zea Mays, in which 
Emerson and his students at Cornell have identified six linkage groups, 
and Pisum, which has so far shown four linkage groups (White 1917). 
Since maize has 10 pairs of chromosomes, four more groups may be 
expected, while in Pisum, which has seven pairs, three more groups will 
probably be established; in fact seven independently inherited characters 
are known. It is an interesting fact that Mendel, in his famous researches 
on Pisum, happened to select for study seven pairs of characters belonging 
to the seven different groups, and so did not detect the phenomenon of 

From the foregoing considerations there arises an interesting and 
very important question. If two homologous chromosomes, each carry- 
ing factors for a certain group of characters (those of one group allelo- 
morphic to those of the other group), separate into different gametes 
(or spores) at the time of reduction, how does it happen that occasionally 
there appears an individual with some of the characters of each group? 
And if a single chromosome carries a series of factors for a certain group 
of characters, how shall we account for the occasional individual with 
some of these characters but not the rest? To state the problem in the 
terms of linkage, if each group of linked characters is represented by a 
series of genes in a given chromosome, how is the linkage broken in 
a certain percentage of cases, with the resulting formation of new link- 
age groups, as shown by the exceptional red-yellow and white-gray flies 
in the experiment described at page 379? A solution to this problem has 
been offered in the Chiasmatype Theory. ' 

The Chiasmatype Theory. In our discussion of chromosome con- 
jugation it was pointed out (p. 257) that various opinions have been 
entertained regarding the nature of the association between the members 
of the synaptic pair. Some workers have held that the chromosomes 
fuse completely and lose their identity, and that the two chromosomes 
appearing on the first maturation spindle are not to be looked upon as 
identical with those which entered into conjugation. On the contrary, 


some reason is limited in these cases and some others to the sex which is 
heterozygous for the sex-factors. On the contrary, in the grasshopper, 
Apotettix, Nabours (1919) has shown that some crossing over occurs in 
both sexes, and the same appears to be true in Primula (Gregory; Alten- 
burg 1916), the rat (Castle and Wright 1916), and Zea (Emerson). IA 
Paratettix, in which no crossing over has been demonstrated, Miss 
Harman (1920) reports that the homologous chromosomes do not 
conjugate until the end of the prophase, and suggests that their indepen- 
dence during the early stages may account for the absence of crossing 

General Discussion. In the foregoing pages a brief account has been 
given of the main points in the theory developed by those who have made 
the most thoroughgoing attempt to relate the phenomena of heredity to a 
visible cell mechanism. To follow out the details of its application does 
not lie within the scope of this chapter: it is here intended only to furnish 
a starting point for cytological studies in this field by indicating the 
common ground upon which cytology and genetics meet. It is import- 
ant, however, to differentiate between evidence which is genetical and 
that which is cytological in nature; and further to remind ourselves to 
what extent observed fact and hypothesis respectively have been woven 
into the theory. Caution is particularly necessary in this latter regard, 
since the general nature of many of our ideas of inheritance is traceable 
in part to the speculative theories of Weismann. Weismann's theories 
of heredity and development, which are summarized in the next chapter, 
were primarily " corpuscular " or " particulate " theories: the phenomena 
of heredity and development were referred to distinct material units 
which in some way were able to bring about the development of the 
heritable characters in the individual and their transmission from one 
generation to the next. Bearing in mind the phenomena of inheritance 
reviewed in the preceding chapters, especially the behavior of the Men- 
delian characters, it is difficult to escape the conclusion that. differential 
factors of some sort, which in an unknown manner initiate the series of 
reactions resulting in the several characters, are carried in the nucleus. 
To determine the nature of these factors and to discover the real relation 
existing between them and the developed characters are among our 
greatest problems. That the factors or genes are discrete units is a 
hypothesis which is not only plausible, but has also proved itself to be 
most useful. If such factors exist, the chromosomes afford a means of 
precisely the kind required to account for the observed distribution of 
characters throughout a series of generations. Hence from Roux and 
Weismann onward the factors have been lodged in the chromosomes. 

But it is when these factors are directly sought with the aid of the 
microscope that disappointment is met. The frequently observed 
granules or chromomeres in the chromatin thread or chromosome are 



accepted by some geneticists as the desired material genes; but, as pointed 
out in the chapters dealing with somatic mitosis and reduction, many 
cytologists are very uncertain as to the morphological status and signifi- 
cance of these bodies, which seem to them to be far too inconstant in 
number and behavior to represent the units in question. Although it is 
tempting to look upon the chromatic granules as the units which current 
theories of heredity seem to require, it must be admitted that the 
observational evidence is insufficient to warrant the categorical state- 
jnents frequently made to the effect that the chromosome is composed of 
,a definite number of more elementary visible chromatic units, which 
have definite space relations and are the significant units in the cellular 
mechanism of heredity. On the other hand, the careful observations of 
Wenrich (1916) have shown that in the grasshopper, Phrynotettix (Fig. 
155), the chromatic granules are relatively constant in size and position 

Fio. 155. Chromosome pair "B" in conjugation from the spermatocytes of 13 differ- 
ent individuals of Phrynotettix magnus, showing constancy in size and arrangement of the 
principal chromomeres. The same constancy is shown in the different cells of a single 
individual. X 1500. (After Wenrich, 1916.) 

in a given member of the chromosome complement, even in different 
individuals; and they furthermore show a close correspondence in the two 
homologous chromosomes as they pair at synapsis. This is one of the 
most striking pieces of direct cytological evidence yet brought forward in 
support of the theory that the chromosome is a " chain of factorial beads " 
(Harper), and heightens the probability that the postulated units of 
inheritance will turn out to be more than purely conceptual ones. 

Whatever may be the value of the chromatic granules, one can hardly 
fail to recognize the highly suggestive nature of the arrangement of the 
chromatin in a thin thread, its frequently beaded appearance, and its 
accurate longitudinal fission into two equal parts at the time of cell- 
division. In the absence of direct and convincing cytological evidence 
for the presence of various "qualities" arranged in a series along the 
thread, we may still look hopefully for the support which it would seem 
that the theory of Roux must sooner or later have. It must be admitted 
that at present the evidence for the existence of genes is in the main 
genetical rather than cytological. 


> Similarly unsatisfactory is the cytological evidence for the breaking 
1 and reunion of the chromatin threads required by the crossing over hypo- 
thesis. Since the hypothesis was put forward by Janssens (1909) adequate 
and convincing descriptions of this process have been singularly wanting, 

, A 
V B 

A ' I 

FIG. 156. Diagrams illustrating various possibilities concerning the compound ring 
tetrads in Orthopteran spermatocytes, following the outlines of Janssens's figures, but 
showing also the relations of the chromatids. At the left in each of the upper figures is the 
longitudinal tetrad-rod from which the ring-series arises, showing results of assumed early 
cross-overs in B 1 and C 1 . A, the compound ring as conceived by McClung, Robertson, etc., 
with the four resulting chromatids at A 1 (no cross-overs). J9, a compound ring, such as 
might follow a two-strand cross-over at each node, giving the results shown in B 1 . C, a 
compound ring giving the results shown in Janssens's diagrams, resulting from a two- 
strand cross-over between two pairs of threads, in regular alternation at successive nodes. 
The result (C 1 ) is four classes of chromatids, as shown in C n . (Figure and legend from 
Wilson and Morgan, 1920.) 

particularly in those cases in which experimental results would make its 
establishment most desirable. Wilson (19126), Robertson (1916), and 
Wenrich (1916, 1917) point out that the figures formed by the chromo- 
some tetrads in the spermatogenesis of certain insects may be interpreted 


without recourse to the hypothesis of chiasmatypy, and that the observa- 
tions and figures of Janssens do not prove the existence of that phe- 
nomenon. Robertson, for example, holds that the "chiasma" figures are 
more simply explained as the result of a tendency on the part of the four 
chromatids to open out partly along the conjugation plane and partly 
along the plane of splitting, without any actual breaking and recombina- 
tion (Fig. 156). Wilson (Wilson and Morgan 1920), however, thinks it 
" highly probable that the cytological mechanism of crossing-over must be 
sought in some process of torsion and recombination in the earlier stages 
I of meiosis perhaps during the synaptic phase or slightly later and that 
this process may leave no visible trace in the resulting spireme-threads." 

During the time when the homologous chromosomes in the form of 
slender threads are twisted about each other in the early prophase of the 
heterotypic mitosis there is abundant opportunity for the required break- 
ing and union to occur, and appearances often lend themselves well to 
such an interpretation. If the side-by-side position is not assumed until 
later in the prophase (Scheme B, Chapter XI) the time during which such 
interchanges might occur is much shorter. But it is a matter of extreme 
practical difficulty in either case to determine whether or not the plane of 
separation is the same as the plane of union at a given crossing point. 
The forces controlling the breaks and recombinations as well as the fre- 
quencies with which they occur in the different chromosome pairs are 
even more difficult to imagine. The difficulty of accounting for these 
phenomena, however, does not weigh heavily as an argument against 
their occurrence. Whether or not chiasmatypy actually takes place is a 
question which must be settled primarily by direct evidence, and the need 
for careful search for such evidence cannot be too strongly emphasized. In 
the opinion of the cytologist the behavior of each chromosome as a whole 
must be much more thoroughly known before cytological interpretations 
of the phenomena of inheritance involving any smaller units which the 
chromosome may contain can be regarded as more than hypotheses, 
valuable as these hypotheses may be in the correlation of genetic data. 

At this point it may be well to recall (see Chapter XI) that all cytolo- 
gists do not agree that the synaptic mates maintain such an independ- 
ence (except at crossover points) as is presupposed by the advocates of 
the chiasmatype theory. A number of observers have reported an actual 
fusion of the conjugating threads, the resulting pachyt&ie thread $ub- 
sequently splitting, probably along the line of this fusion. It may 
accordingly be suggested, in line with the hypotheses discussed by Allen 
(1905), that if the threads actually carry or consist of discrete units or 
genes, and if these units do not themselves fuse during the process, such 
a resplitting of the pachyt^ne thread, if not wholly along the fusion plane 
because of a twist of the thread or of the plane itself, would bring 
about a redistribution of the genes as effectively as would the chiasmatype 


process as originally proposed. 1 The splitting of chromatic threads is, 
moreover, a process already known to occur in all other mitoses. But 
interpretations involving the actual fusion of the conjugating threads 
have been adversely criticized with much effect by Gr^goire (1910), and 
only further research on the cell can lead us to an adequate evaluation of 
the above outlined suggestion. 

Other Theories of Linkage. The chiasmatype hypothesis is not the 
only one which has been advanced to account for the phenomenon of 
linkage. Most prominent among other attempts to solve this problem is 
that of the English geneticists, especially Bateson, Punnett, and Trow, 
who have advanced what is known as the Reduplication Hypothesis. In- 
stead of accounting for the new factor combinations manifested by a cer- 
tain percentage of the gametes on the basis of an interchange of factors in 
the chromosomes at the time of reduction, these investigators seek to 
explain them by postulating a series of differential divisions in the earlier 
cells of the germ cell lineage, whereby Mendelian factors, not carried by 
chromosomes, are segregated in such a manner that the observed types of 
gametes are produced. Furthermore, the various factors are supposed to 
be segregated successively, and at such stages in the cell lineage that the 
proliferation or reduplication of the cells with new combinations of factors 
shall account for the ratios in which the new types appear. Although 
the differentiation of the somatic and early germ cells is accompanied by 
visible differences in the constitution of their cytoplasm (see p. 406), 
there is at hand no cytological evidence for such a segregation of heredi- 
tary units as is thought to occur by the proponents of the Reduplication 
Hypothesis. So long as this is the case, discussion of the hypothesis, 
together with the subhypotheses formulated to meet certain serious objec- 
tions, hardly belongs to cytology. One fact, however, pointed out by 
Morgan (1919a) as very significant in this connection, is found in the 
results of some experiments by Plough (1917). Plough investigated the 
effects of temperature on the frequency of linkage breaking (crossing over) 
in Drosophila. Not only did he find that temperature does affect the 
amount of crossing over, but the effect was clearly produced at the time 
of maturation and not earlier^ This evidence is directly opposed to the 
view that the new factor combinations are formed during cell-divisions 
some time prior to reduction. 

Another effort to account for the results of crossing over without 
resorting to the chiasmatype process is represented in a suggestion 
(Goldschmidt 19176) to the effect that the two factors of an allelomorphic 
pair are held to their places in the two homologous chromosomes by a 
pair of variable forces, which allow them to exchange places in a certain 

J A form of this interpretation of synapsib has suggested itself also to Dr. 
C. W. Metz and Dr. E. G. Anderson, who inform the author that such a hypothesis 
will in all probability conform satisfactorily to the data of 


proportion of cases without involving a rupture of the chromosomes. These 
forces, however, are purely conjectural. It is pointed out by Jennings 
(1918), moreover, that the gametic ratios theoretically resulting from 
such a process do not agree with the actual ratios observed in Drosophila. 

Value of the Chromosome Theory of Heredity. Whatever judgment 
may ultimately be rendered on the chromosome theory of heredity as 
outlined in these chapters, it must be agreed that the value of this theory 
in the present state of our knowledge can hardly be overestimated. 
Through its use a huge number of the observed facts of inheritance are 
being reduced to order: the painstaking investigation of the interrelation- 
ships of all the known heritable characters of even a single organism 
such as Drosophila cannot fail to be a great service to biological science. 
Its appeal to the cytologist, as Wilson states, is largely through the man- 
ner in which it seeks to make use of known cell mechanisms rather than 
entirely hypothetical processes. Those portions of the theory which 
are as yet unsupported by the results of direct cytological observation, 
though not contradicted thereby, at least have the virtue of affording a 
useful and graphic representation of the mutual behavior of hereditary 
characters. Notwithstanding the statement that "the graphic repre- 
sentation of the location of the factors is a type of representation common 
to every set of phenomena which can be expressed as percentages " (Trow 
1916), these hypotheses are of great value, for by aiding in the correla- 
tion of the facts of inheritance they serve to increase the number of 
observed phenomena statable in terms of order; and the reduction of 
experience to order and the statement of this order in simple formulae, 
together with the search for new truth, constitute the principal tasks 
of science. If this work of correlation has been well done the whole 
body of facts can readily be placed under another theoretical interpre- 
tation and described in a new set of terms should occasion require. 

Although it may be that the chiasmatype hypothesis of linkage is in 
certain points inadequate, mathematically (Trow 1916) or otherwise, it is 
nevertheless true, as we have already seen, that it fits the case very well. 
At the same time we may remind ourselves that the fact that a hypothesis 
works well is no guarantee of its ultimate truth. But even if the chiasma- 
type interpretation should have to be ever so greatly modified as new 
facts accumulate, it is scarcely to be doubted that the chromosome theory 
of heredity in some form will turn out to be in accord with the truth. 
With respect to this general theory Wilson (1909) writes as follows: 

"I stand with those who have followed Oscar Hertwig and Strasburger in 
assigning a special significance to the nucleus in heredity, and who have recog- 
nized in the chromatin a substance that may in a certain sense be regarded as the 
idioplasm. This view is based upon no single or demonstrative proof. It 
rests upon circumstantial and cumulative evidence, derived from many sources. 
The irresistible appeal which it makes to the mind results from the manner in 


which it brings together under one point of view a multitude of facts that other- 
wise remain disconnected and unintelligible. What arrests the attention when 
the facts are broadly viewed is the unmistakable parallel between the course of 
heredity and the history of the chromatin-substance in the whole cycle of its 
transformation. In respect to some of the most important phenomena of 
heredity it is only in the chromatin that such a parallel can be accurately traced. 
It is this substance, in the form of chromosomes, that shows the association of 
exactly equivalent maternal and paternal elements in the fertilization of the 
egg. In it alone do we clearly see the equal distribution of these elements to 
every part of the body of the offspring. In the perverted forms of development 
that result from double fertilization of the egg and the like it is only in the 
abnormal distribution of the chromatin-substance by multipolar division that we 
see a physical counterpart of the derangement of development. Only in the 
chromatin-substance, again, do we see in the course of the maturation of the 
germ cells a redistribution of elements that shows a parallel to the astonishing 
disjunction and redistribution of the factors of heredity that are displayed in the 
Mcndelian phenomenon. " 

With more particular reference to the chiasmatype hypothesis Wilson 
(1913) says: 

"This, admittedly, is a bold venture into a highly hypothetical region. Its 
justification is the pragmatic one that it 'works/ The hypothesis gives us the 
only intelligible explanation that has yet been offered for a series of undoubted 
facts; and it is certainly worthy of the most attentive further examination . . . 
We have much to gain and nothing to lose by the use of explanatory hypotheses 
that are naturally suggested by the facts and help us to formulate them for 
analysis, so long as such hypotheses are not allowed to degenerate into dogmas 
accepted as an act of faith, but are only used as instruments for further. observa- 
tion and experiment." 

Bibliography at end of Chapter XVII I. 


The theory of heredity described in the foregoing chapters, though 
resting on its own foundation of observational and experimental evidence, 
shows in some of its features the influence of certain earlier speculative 
hypotheses, particularly those set forth by Weismann. 1 Some of the 
conceptions embodied in these hypotheses are consequently involved in 
cytological and genetical discussions of the present day, and for this 
reason we shall here outline their main points, briefly indicating wherein 
our modern theory has advanced beyond them. 

Although conceptions of other types arose very early, many of the 
hypotheses in question were based on the assumption that the phenomena 
of heredity and development are the result of the activity of ultimate 
living particles of ultramicroscopic size. Thus Herbert Spencer (1864) 
built up a theory of considerable proportions about his 'physiological 
units/ and these formed the prototype of the units postulated in many 
later theories. Of these theories the most prominent were those of 
Darwin, Nageli, de Vries, and Weismann. 

Darwin's Hypothesis of Pangenesis. In his Variations of Plants and 
Animals under Domestication (1868) Darwin included a chapter on his 
" Provisional Hypothesis of Pangenesis," which, though offered Only as a 
suggestion, excited great interest in the field of biology, especially after 
the advances made in cytology a few years later. In several points it 
closely resembled a theory propounded by Buffon more than a century 
earlier (1749). Darwin clearly saw in the cytological aspects of heredity 
one of the great biological problems of the future, but his only specula- 
tions on the subject were embodied in the pangenesis hypothesis, .which 
may be stated as follows : 

All the cells of the organism at all stages of development give off small 
particles, or gemmules, which multiply by fission and circulate throughout 
all parts of the body. These gemmules pass to the germ cells, carrying 
with them the power to reproduce cells like those from which they came. 
In this way units representing all the kinds of cells composing the organ- 
ism are collected in the gametes (or spores or buds) and are thus passed 
on to the next generation. During the embryogeny of the new individual 
the gemmules are so distributed that at the proper times and places they 

1 See Kellogg (1907), Delage and Goldsmith (1913), Thomson (1899, 1913), and 
Conklin (1015). 



develop into cells like those from which they originally migrated, in 
this manner building up a new individual like the parent. Some of the 
gemmules do not function until a comparatively late stage in the onto- 
geny, and others may remain latent through several generations: on 
these two assumptions it is possible to account for the late appearance of 
certain characters and for the fact that others may "skip" one or more 
generations. It is further supposed that some gemmules remain latent 
in the individuals of one sex: thus, for instance, the characters normally 
present only in the male may be transmitted through the female. 

In the many criticisms of this hypothesis the tendency has been to 
judge and condemn it solely on the ground of the supposed transportation 
of the gemmules from the body cells to the germ cells, for which no direct 
evidence has ever been discovered. It should not be forgotten, however, 
that Darwin suggested an explanation for the phenomena of heredity 
on the basis of representative material units in the cells, a conception 
which was of the greatest importance in that it constituted the starting 
point for later fruitful investigations and theories. The migration of 
the gemmules was postulated largely to account for the phenomena of 
regeneration and the inheritance of acquired somatic modifications. 
Since regeneration may be explained as well on other grounds, and since 
the evidence for the inheritance of acquired somatic modifications is 
for the most part of such extremely doubtful value, such a migration of 
representative units, first denied by Galton (1875), has come to be re- 
garded as unnecessary. A theory postulating representative particles 
but no such migration was that of de Vries. 

De Vries's Theory of Intracellular Pangenesis. According to de 
Vries (1889) the particles of hereditary substance,, or pangens, do not 
represent different kinds of cells as Darwin thought, but stand rather for 
different elementary characters or qualities out of which the many visible 
characters of the organism are built up. Furthermore, these living 
elements or pangens do not pass from cell to cell, but merely circulate 
between the nucleus, where a complete outfit of them is conserved, and 
the other parts of the cell hence the term " intracellular pangenesis." 
In this way the characters brought into the new individual through the 
nucleus are delivered to the cell as a whole. Contrary to the idea of 
Darwin and especially to that of Weisrnann (see below), jail the cells (or 
nuclei) ^of the body contain pangens fp all the hereditary characters: 
thgj^are^not sorted out as development proceeds. 

Nageli's Idioplasm Theory. A highly speculative theory of a some- 
what different type was that formulated by Nageli (1884) five years 
before that of de Vries. Protoplasm was thought by Nageli to be made 
up of a vast number of fundamental living units; these he called micellce. 
As a result of the ways in which these moleculaf Complexes or micellae 
may* be arranged, there are in the cell two bfeds of protoplast : in nutri- 


live protoplasm, or trophoplasm, the micellae have no regular orienta- 
tion, whereas in idioplasm they are oriented in a particular manner. 
According to Nageli the phenomena of heredity are due to the constitu- 
tion and transmission of this idioplasm; idioplasm is the physical basis of 
inheritance. It is not confined to the nucleus, but forms an elaborately 
constituted network extending throughout all the cells of the organism. 
By arranging themselves in various groupings within this network the 
micellae are able to bring about the development of the many specific 
characters. The further details of this highly "fragile" hypothesis are 
summarized in convenient form by Delage and Goldsmith (1913), who 
point out that in spite of its many unsupported assumptions it did involve 
two fertile ideas: first, that there are two kinds of protoplasm, one of 
which carries the characters of the organism ; and second, that there are a 
limited number of elementary characters which combine in various ways 
to produce the many visible characters. 

Weismann's Theory. The most highly developed and influential of 
all such speculative theories was that of Weismann. On the basis of the 
conception of pangens Weismann built up the highly involved system 
of hypotheses set forth in his Das Keimplasma of 1892 and in more 
elaborated form in his Evolution Theory of 1902. Certain modifications 
were later made. 

As Delage and Goldsmith have noted, Weismann incorporated in his 
theory several of the stronger points of earlier theories, such as Darwin's 
conception of representative particles, Nageli's elementary characters, 
and de Vries's intracellular migration of particles. With Nageli he dis- 
tinguished between nutritive morphoplasm and hereditary idioplasm or 
germ-plasm, but unlike Nageli he identified the idioplasm with the 
chromatin of the nucleus. His conception of the constitution of the 
idioplasm was essentially as follows: 

The ultimate unit in all living matter is the biovhore, which is a 

O 0tf!Hf~J**rrw - 

minute living particle capable of growth and reproduction a vital unit. 
The many kinds of biophores in a given cell represent the many characters 
of that individual cell: they are not bearers of the characters as such 
(though Weismann often spoke of them in this fashion), but are rather 
factors upon whose presence the development of the characters depends. 
The biophores are grouped to form vital units of a higher order, known as 
d^IMMt^ s - The determinant, since it is composed of the many kinds 
of biophores in the cell, 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 determinants in the organism as there are types of cells, 
or " independently variable parts," to b^ developed. The determinants 
are in turn grouped into i$s. A single id contains all the kinds of deter- 
minants, and so stands for the sum of all the characters of the organism: 
: t contains the " complete architecture" of the germ-plasm. 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" which have been contributed by past genera- 
tions. The ids are identified with the visible chromatin granules in the 
nuclear reticulum or in the chromatin thread during mitosis. In most 
*ciases the ids are grouped to form idants, or chromosomes. In some forms 
which have a large number of granular chromosomes it is possible that 
each is composed of but one id. The id therefore, rather than the 
chromosome, is the unit of primary importance. In case there are 
several ids in a chromosome (idant) they are arranged in a linear series. 
The idea that the chromosomes are all alike since they carry closely simi- 
lar ids was later (1913) modified by Weismann, largely as the result of 
the demonstration that very minute characters are segregated in 
Mendelian fashion. 

With the aid of this elaborate mechanism Weismann explained onto- 
genetic development in the following manner. Mn the fertilized egg from 
which the individual is to develop all the Kinds of determinants are 
present :")thoes of the female parent are contained in the egg nucleus 
and those of the male parent are brought in by the nucleus of the 
spermatozoon. During the long series of cell-divisions beginning with 
the fertilized egg and ending with the completion of the mature organism, 
the many kinds of determinants are sorted out through a progressive 
disintegration 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. y when that cell is finally formed, the determinant splits up into its 
constituent biophores; and these, through their action upon the cell 
elements, 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. For Weismann, therefore, development (ontogenesis) was 
definitely bound up with the evolution or unfolding of a complex struc- 
ture contained in the fertilized egg. Although he did not hold that 
the units in the egg have the same spatial relations as their corresponding 
characters or structures in the adult, it has been said with some degree 
of truth that he transferred preformationism to the nucleus. 

Such being Weismann's conception of development, how did he account 
for heredity? If the various kinds of body cells in an individual are 
characterized by different types of determinants, how is it that the germ 
cells, or gametes and fertilized egg through which this individual is 
to give rise to the next generation, possess a complete outfit of deter- 
minants? According t&TDarwin's hypothesis, outlined in the foregoing 
pages, representative particles or gemmules are contributed by all the 
body cells at all stages to the germ cells, by which they are transmitted 



to the next generation. (See Fig. 157, A.) Such a contribution of 
elements from the body cells to the germ cells was denied completely by 
Weismann. He held rather that a certain portion of the complete germ- 
plasm (idioplasm; chromatin) of the fertilized egg is carried along un- 


FIG. 157. Diagram illustrating the hypotheses of Darwin and Weismann. The large 
circles represent successive generations of individuals, and the small circles their germ 
cells. For the sake of simplicity inheritance is shown as uniparental rather than biparental. 
A, Darwin's Hypothesis of Pangenesis. The branching solid lines ending in arrows repre- 
sent the sorting out of the hereditary units (gemmules) during ontogenesis; the dotted 
arrows show the migration of gemmules from the body cells to the germ cells, by which 
they are carried into the next generation. B, C, Weismann's theory of the continuity of 
the germ-plasm, with no contribution of hereditary units from the body cells to the germ 
cells. In one case (B) the germ cells are set aside at the beginning of ontogenesis, and in 
the other (C) much later. In both cases the "complete germ-plasm", is delivered to the 
germ cells through a shorter or longer series of equational divisions (heavy lines). 

changed and delivered inta<2t to the germ cells, ft had been shown 
(Haeckel 1874; Rauber 1879; Jaeger 1878; Nussbaum 1880; Galton) 
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 can h$ve 


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) 
at all: they are present from the beginning of development with the full 
Hereditary outfit, and by a few equational divisions they give rise to the 
gametes. This is represented in Fig. 157, B. In the more usual case of 
those animals and plants in which the germ cells appear later in the onto- 
geny 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 fertilized egg with the germ cells 
the germ track (Keimbahri) maintain the undiminished germ- plasm 
(Fig. 157, C). Thus in this case as in the other there is a continuity of 
the germ-plasm, if not a continuity of the germ cells (unless meristematic 
cells also be regarded as germ cells). Since the germ-plasm of any 
generation is derived directly from that of the preceding one, it is continu- 
ous through an unlimited number of generations; and the successive somas 
(bodies) are, so to speak, side branches given off at intervals from the main 
stream of the germ-plasm. 

In elaborating the above views Weismann (1885, 1892) insisted 
strongly upon the independence of the "potentially immortal" germ- 
plasm and the transient and mortal soma 1 . Hfe 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 originating in the germ-plasm of the germ 
cells or germ track as responses to internal (nutritive etc.) or external 
environmental stimuli, or as the result of recombinations of hereditary 
units at the time of fertilization (amphimixis). Weismann admitted 
that the germ-plasm, though remarkably stable, might be altered directly 
by the environment 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 would cause the reappearance of the same somatic modifica- 
tion in the next generation. With Weismann, as with Mendel, the main 
problem of heredity was not to discover how the characters of the organ- 
ism get into the germ cells which it produces, but rather how the char- 
acters of an organism are represented in the germ cell from which it is pro- 
duced (Darbishire 1911, Chapter 12). He attempted to showhow it is 
that the stream of gef m-plasm on the one hand maintains a stability suffi- 
cient to account for the resemblance between the successive bodies spring- 
ing from it at intervals, and on the other hand undergoes orderly changes 
responsible f or r thg^ evolutionary advance shown in a long series of 
generations. In the words of Agar (Bower, Kerr, and Agar, 1919), 
^According to Darwin, parents truly transmit their characteristics to 
n See discussion of senescence in Chapter VII. 


their offspring (by means of the gemmules). According to the modern 
view [Mendel; Galton; Weismann], however, children resemble their 
parents not, strictly speaking, because the latter have passed something 
on to them, but because both have been produced from the same 
germ-plasm" (p. 91). "The parent is rather the trustee of the germ- 
plasm than the producer of the child " (Thomson 1913). 

Weismann attempted further to account for the variations effective 
in evolution on the basis of his theory of Germinal Selection. He sup- 
posed 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 the nutritive conditions, are favored 
thereby and grow stronger and more influential, while others undergo 
changes in the opposite direction. The cells or parts of the organism 
receiving the determinants 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. In this manner Weismann accounted for the 
preservation of small variations not yet of selective value, and for 
continued variation along definite lines (orthogenesis) in both plus and 
minus directions. Thus for him selection was the cardinal principle 
which ruled not only over organisms, but also over cells, ids, deter- 
minants, and biophores. As he himself stated it, "This extension of the 
principle of selection to all grades of yital units is the characteristic 
feature of my theories. " ' 

Some Modern Aspects of Weismannism. Although the distinction 
between soma cells and germ cells is not now drawn so sharply as in the 
days of Weismann, it is nevertheless of interest to note certain facts 
adduced in support of his contention that the germ-pZasw is continuous. 

In Ascaris megalocephala (Boveri 1887c, 1889, 1891, 1892, 1904; 
Zacharias 1913) it is observed that at the second cleavage mitosis the 
chromsomes in one blastomere remain entire, while in the other blastomere 
they become broken up into smaller pieces, some of which are lost in the 
cytoplasm and are not included in the daughter nuclei (Fig. 158, A). 
This process is called "chromatin diminution." At the third and fourth 
cleavage mitoses a similar diminution occurs in all the blastomergs 
but one; in this one the chromosomes remain entire. At the fifth division 
it is seen that in the one undiminished cell no further diminution occurs 
as it divides, and its descendants become the germ cells. The primary 
germ cell is therefore set apart at the fourth mitosis; and, whereas the 
other embryonic cells giving rise to somatic structures have undergone a 
diminution, the entire chromatin outfit is delivered to the germ cells 
through the undiminished cells of the germ track. A similar condition 
is present in Miastor (Kahle 1908; Hegner 1912, 1914). In Ascaris 



cam's (Walton 1918) the germ cells are similarly set aside at the seventh 
cleavage mitosis. 

j(/In criticizing this supposed evidence for the independence and con- 
tinuity of the germ-plasm Child (1915) points out that, since undi- 
minished cells may give rise to other cells as well as germ cells in the early 
divisions, the process observed may represent merely a segregation of 
different organs rather than a separation of the germ-plasm from the 
soma; and that the non-diminution of the chromatin in the germ track 
may be the result of the differentiation of the germ cells rather than its 
cause, the differentiation at this stage being primarily a physiological 


FIG. 158. 

A, chromatin diminution in Ascaris megalocephala. The second cleavage mitosis is in 
progress: all the chromatin is retained in the upper blastomere, from which the germ 
cells are to arise, whereas chromosome diminution occurs in the lower blastomere, which 
is to give rise to the somatic cells. (After Boveri.) B, third nuclear division in the yet 
unsegmented egg of Chironomus confinis showing the early setting aside of the primitive 
germ cells at the lower end. (After Hasper.) 

(metabolic) one. He refers to certain later researches of Boveri (1910), 
which apparently show that "the occurrence or non-occurrence of chro- 
matin diminution in a nucleus depends, not upon its qualitative con- 
stitution, but upon its cytoplasmic environment." From this it is 
concluded that "the 'germ path' is a feature of the cytoplasm, and the 
cytoplasm is not, properly speaking, a part of the germ-plasm at all, 
but represents the soma of the cell" (p. 327). 

In support of this conclusion we may cite, as does Child, those cases 
among insects (Hasper on Chironomus, 1911 ; Hegner on Miastor, 1912, 
1914) and copepods (Haecker 1897, 1902; Amma 1911) in which the 
substance of the future germ cells may be distinguished very early in 
the embryogeny, even in the undivided egg, either as a visibly differen- 


tiated region of the cytoplasm (Keimbahn-plasma) (Fig. 158, B), or 
by the presence of certain cytoplasmic granules or inclusions (Keimbahn 
determinants). These latter are ultimately delivered to the definitive 
germ cells, the nuclei at the same time showing no differences in the germ 
and soma cells. Although such cases seem to show that "the factors 
determining what shall become germ cells and what somatic structures 
apparently exist in the cytoplasm and not in the nuclei" (Child 1915, 
p. 329), it is nevertheless very significant for the chromosome theory of 
heredity that only in the germ cells, whatever the cause of their differ- 
entiation from the other cells of the body, should the chromatin be 
retained in the complete state in the cases of Ascaris and Miastor. 
Whatever may be the relation of the chromatin to differentiation, and 
whatever may be the degree of its independence of the soma -plasm, it 
is noteworthy that here it is precisely in the germ cells and in the cells of 
the germ track the cells especially important in heredity that the 
chromatin shows an unbroken continuity from cell to cell and conse- 
quently from generation to generation. Were the chromosome mechan- 
ism disturbed in these cells as it is in the somatic cells, or should 
"diminished" cells regenerate a completely normal organism, a serious 
obstacle would be in the path of the chromosome interpretation of here- 
dity as now formulated. The actual behavior of the chromatin in the 
germ track of Ascaris argues for rather than against the chromosome 
theory, at least as regards hereditary transmission. 

A much used argument against Weismann's theory of development 
(ontogenetic differentiation) is found in the phenomenon of regeneration. 
It is well known that in certain animals and especially in plants a portion 
of the body consisting solely of differentiated cells may under certain 
conditions give rise to a complete individual with functional germ cells. 
Weismann accounted for such regeneration on the basis of an additional 
hypothesis which stated that during the sorting out of the hereditary 
units in the process of cell differentiation certain "supplementary 
determinants" are carried along unaltered, and that later, if occasion 
arises, these cause the development of the differentiated cells into an 
organism with all the usual characters. Since in certain cases (Begonia) 
almost any cell of the body may undergo regeneration into a complete 
plant, it is evident that all of the body cells must have a "complete" 
germ-plasm.}^Hence the distinciton between a germ-plasm limited to 
cells capable of producing an entire individual, and a soma-plasm present 
only in somatic cells without such power, becomes of no value. Every 
cell capable of regeneration germ cell, -meristem cell; or differentiated 
somatic cell contains the complete germ-plasm, which appears to be 
simply the chrpmatin possessed by all the cells alik^Lack of power to 
regenerate is not due to a lack of complete germ-plasm but to other 
conditions associated with the degree of differentiation shown by the 


cells. In thus using the terms germ-plasm and soma-plasm (somato- 
plasm) synonymously with chromatin and cytoplasm respectively, 
Weismann's conception of the chromatin as the substance especially 
important in heredity remains, although his theory of the dependence 
of ontogenetic differentiation upon a sorting out of qualitatively differ- 
ent units of this substance during developments no longer helcL 

This use of the term germ-plasm is general among geneticists, who 
are concerned with the problems of heredity, and may be distinguished 
from that of certain students of the physiology of development, by whom 
germ-plasm is regarded as "any protoplasm capable, under the proper 
conditions, of undergoing regression, rejuvenescence, and reconstitution 
into a new individual, organism, or part" (Child 1915, p. 462). From this 
latter point of view the germ-plasm would be regarded as either the 
complete protoplast capable as acting as so described, or, as Child is 
inclined to believe, only an abstract idea merely a term standing for 

Weismann's theory of the sorting out of hereditary units, during onto- 
genesis was abandoned not only because of irs inapplicability to the 
results of certain experiments, but also because no support for it <.ould 
be found in a direct study of the cell mechanism. Strasburger and other 
investigators insisted strongly that so far as can be ascertained the 
division of the chromatin at each somatic mitosis is exactly equational, 
there being not the slightest indication of such a difference in the chro- 
matin of the two daughter cells as might be expected were the divisions 
qualitative (erbungleich) . To this Weismann had only to reply that 
since the differentiation is a matter not of ids or of idants but of determi- 
nants, the two nuclei would be visibly alike in spite of their qualitative 
difference. Although certain cases have been described in which growth 
is not equal in all of the chromosomes during the early stages of develop- 
ment, and although the two daughter nuclei may .become differentiated 
through unequal nutrition after their formation, as Strasburger suggested, 
most biologists have adopted the view that all of the somatic nuclei are 
qualitatively alike in their chromatin content so far as its hereditary 
powers are concerned. They have thus followed de Vries (1889) in 
holding that factors for all of the hereditary characters are present in 
all of the somatic cells, a conclusion strongly supported by the facts of 
regeneration. The ontogenetic differentiation of the cells which mani- 
fests itself largely in cytoplasmic changes, as well as the relative regen- 
erative powers which these cells possess, are attributed for the most part 
to physiological causes, the latter in large measure determining what 
hereditary capabilities of the various cells shall come to expression. 
The distinction between the view of Weismann and that of more recent 
investigators is made clear in the two diagrams of Fig. 159, which have 
been copied from Conklin (1919-1920). 



Notwithstanding the fact that many changes have been made in its 
details, Weismann's theory of heredity proved to be of much greater value 
than his theory of development. Morgan (Morgan et al. 1915, pp. 223- 
227) points out that Weismann made three contributions to the study of 
genetics, which may be stated in three propositions: (1) The germ-plasm 





FIG. 159. The behavior of the hereditary units in ontogenesis according to Weismann 
(A) and the current interpretation (B). In A the determinants in the nucleus (1, 2, 3, 4) 
are supposed to be distributed differentially to the various somatic cells. In B the genes 
(1, 2, 3, 4) are distributed equally to every cell, but the cytoplasm is distributed differen- 
tially. The same genes working upon different cytoplasms produce different results in 
various somatic cells. (Diagrams and legend from Conklin, 1919-1920.) 

contains independent elements which may be substituted one for another 
without undergoing change; (2) a segregation of maternal and paternal 
factors, pair by pair, occurs at one period in the history of the germ cells; 
(3) the behavior of the chromosomes is specifically applicable to the 
problems of heredity. In these principles are found "the basis of our 


present attempt to explain heredity in terms of the cell/' for upon them 
is founded the Factorial Hypothesis, now supported by a large mass of 
experimental evidence. 

In our conception of the nature of the heredity units or factors we 
have departed widely from Weismann. For him each of the ids arranged 
in a series in the chromosome represented the sum of the characters of a 
complete organism; the smaller parts were represented by the smaller 
units (determinants) composing the id, and these units in turn were made 
up of biophores, which were ultimate and independent living particles. 
According to our modern hypothesis each of the serially arranged factors 
or genes exerts an influence on the development of one or more characters, 
but does not stand for a complete organism as did the id, or for a part 
of it as did the determinant. Moreover, it is generally regarded as a mass 
of some complex chemical substance whose activities are due to its defi- 
nite though imperfectly known physico-chemical properties, rather than 
to forces exerted by hypothetical vital units. 

In justice to Weismann it should be pointed out that the frequently 
made criticism that his theory was a vitalistic one is warranted only to a 
limited extent. Although his ultimate hereditary units, the biophores, 
were regarded as actually living particles, Weismann stated that " they 
are not composed in their turn of living particles, but only of molecules, 
whose chemical constitution, combination, and arrangement are such as 
to give rise to the phenomena of life." He was careful to point out that 
in spite of the fact that it cannot be proved that no peculiar vitalistic 
principle exists, we should hold fast to a purely physico-chemical basis 
of life " until it is shown that it is not sufficient to explain the facts, thus 
following the fundamental rule that natural science must not assume 
unknown forces until the known ones are proved insufficient . . . We 
can quite well believe that an organic substance of exactly proportioned 
composition exists, in which the fundamental phenomena of all life 
combustion with simultaneous renewal must take place under certain 
conditions by virtue of its composition" (1902, lecture 36). 

The manner in which hereditary factors are segregated at gameto- 
genesis has been found to be different from that conjectured by Weismann. 
As indicated in the chapter on reduction, he supposed it to occur through 
a transverse division of the chromosome, whereas it is now known that 
it is accomplished by the disjunction of pairs of entire chromosomes, 
the separating members of each pair being qualitatively different. The 
" reduction" predicted by Weismann was found to occur, but not in the 
manner he supposed. As shown above, his idea of a further qualitative 
segregation of units of a lower order in the somatic divisions has not 
been substantiated. Notwithstanding the abandonment of his theory 
of development and the changes made in his theory of heredity, Weis- 
mann's influence on both cytology and genetics was enormous, largely 


because of his emphasis upon the need for careful studies of the cell 
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 great service to place the keystone 
between the work of the evolutionists and that of the cytologists, and 
thus bring the cell-theory and the evolution-theory into organic con- 
nection " (Wilson 1900, p. 13). 

We may further point out, with Morgan (1915), that the factorial 
hypothesis assumes only three things about the factors : they are constant, 
they are usually in duplicate in each body cell and immature germ cell, 
and they usually segregate in the maturing germ cells. The hypothesis, 
and the Mendelian theory in general, therefore have to do only with 
heredity : they do not attempt to explain the causes of development. They 
seek rather to account for the initial resemblances or differences in here- 
ditary potentiality which are observed to exist between the germ cells 
from which successive generations arise. Between the materials com- 
posing the initial factors and the fully expressed characters of the or- 
ganism "lies the whole world of embryonic development," to which the 
application of the theories under consideration has not yet been extended 
in any systematic or satisfactory manner. Nevertheless many investi- 
gators, though realizing the failure of Weismann's attempt to explain 
development in terms of representative particles, are strongly inclined 
to the view that since the Mendelian characters appearing toward ma- 
turity behave as though associated with discrete units in the germ, the 
course of ontogenetic development in its earlier stages must also be due in 
large part to the activity of factors carried by the nucleus. Development 
is thus held to be predetermined or controlled by an internal mechanism : 
external agencies act only by affecting the operation of this mechanism. 
The factors control the character and behavior of the cells, and upon 
these in turn the organism, which is a cell aggregate, is alone dependent 
for its characters and activities. In place of the early hypothesis on 
which it was supposed that the development of characters is controlled 
by: the migration of determiners or pangens from the nucleus into the 
cytoplasm at precisely the right times and places, we now haVe the tlieory 
that the factors in the nucleus probably produce their effects by initiating 
series of chemical reactions which involve all parts of the cell. As Mor- 
gan (1920) states, " Granting that differences may exist in the nuclei of 
different species, different end products are expected. The evidence 
that such differences may be related to specific substances in the nucleus 
is no longer a speculation but rests on the analytical evidence from Men- 
delian heredity. In what way and a