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Peabody Museum

of Natural History

Yale University

New Haven, CT 06511

Postilla number 1g7

15 February 1982

The Relationships of the
Yellow-breasted Chat (/cteria virens)
and the Alleged Slowdown in

the Rate of Macromolecular Evolution
in Birds if RY

Charles G. Sibley
Jon E. Ahiquist

(Received 14 May 1981)
Abstract

The taxonomic relationships of the Yellow-
breasted Chat (/cteria virens) have been
Uncertain since its discovery more than
200 years ago. Although usually considered
to be a New World wood warbler (Parulini)
it possesses structural and behavioral char-
acteristics that seem aberrant in compari-
Son with the typical members of that group.
The relationships of /cteria were inves-
tigated by comparing its single-copy DNA
Sequences with those of other New World
nine-primaried oscines and representatives
of other oscine families, using the technique
of DNA-DNA hybridization. The data indi-
Cate that /cteria is a paruline warbler and
'tshould continue to be included within
that group.

The study of /eteria provided the basis
for an examination of the suggestion by
Several authors that the proteins of birds
and, by extension, their DNAs, evolve more
Slowly than do those of other animals. Evi-
dence is presented indicating that the al-
leged differences are due, at least in part, to
differences in the human perception of the
boundaries of taxonomic categories in
birds versus most other organisms. Birds
are taxonomically oversplit at all supra-

Copyright 1982 by the Peabody Museum of Natu-
al History, Yale University. All rights reserved. No
Part of this publication, except brief quotations for
Scholarly purposes, may be reproduced without the
Written permission of the Director, Peabody
Museum of Natural History.

specific levels, but small, nocturnal mam-
mals and other groups are probably over-
lumped at all levels. The lack of equivalence
between the taxonomic categories of birds
and those of other animals results in an er-
roneous evaluation of their rates of macro-
molecular evolution. DNA hybridization
data indicate that the vireos (Vireoninae)
are not closely related to the wood war-
blers, or to other New World nine-primaried
oscines. We have shown elsewhere that
the vireos are members of a large, varied
“corvine assemblage.”

Key Words

DNA-DNA hybridization, birds, Yellow-
breasted Chat, macromolecular evolution,
rate slowdown, avian systematics, categori-
cal equivalence.

Introduction

The Yellow-breasted Chat (/cteria virens)
breeds from southern Canada and the
United States to central Mexico (Jalisco). It
has been included among the New World
wood warblers (Fringillidae: Emberizinae:
Parulini, cf. Sibley, 1970; Sibley and Ahl-
quist, in press, a,c) for more than a century
but its affinities repeatedly have been ques-
tioned because it is aberrant In comparison
with the other species assigned to that
group. /cteria is larger than any of the typi-
cal wood warblers and it differs from them
in several structural and behavioral charac-
ters. Although it is a New World nine-

2 Yellow-breasted Chat Relationships

Postilla 187

primaried oscine, it does not fit readily into
any of the subgroups of that large
assemblage.

Baird (1858) was the first to assign /cte-
ria to the wood warblers and (p. 248) he
noted the controversy surrounding It.

The proper position of this genus has
always been a matter of much uncertainty,
but | see no reason why it may not legiti-
mately be assigned to the Sy/vicolinae,
possessing, as it does, so many of their
characteristics. The bill is stouter and more
curved than in the rest, but the other char-
acters agree very well. It cannot properly
be placed with the vireos and shrikes on ac-
count of the absence of a spurious primary,
as well as of a notch in either mandible.

But the doubts soon returned. Coues
(1892:311) questioned whether /cteria is
“most naturally classed with the Warblers”
and Newton (1896:85) noted that /cteria
“is generally referred to the Family Mniotilti-
dae, or American Warblers, but may possi-
bly not belong to them, its stout bill being
very unlike that possessed by the rest.”
However, Baird's opinion was supported by
Ridgway (1902:426) who wrote that

The position of /eteria in the Mniotiltidae
has more than once been questioned;
indeed it had not been referred to this
family at all until 1858, when Professor
Baird formally placed it here as sole repre-
sentative of a group or section /cterieae.
That he was fully justified in doing so is
quite certain, for, however unlike other
North American Mniotiltidae /cteria may
seem, the extralimital genera Chamaeth-
/ypisand Granatellus distinctly connect it
with more typical forms, the former being,
indeed, a very near relative, its close rela-
tionship being shown even in the colora-
tion.

Bent (1953:587) noted that “Audubon
classed [/cteria] with the manakins, and
others have placed it with the vireos or
with the honeycreepers, but structurally it
seems to be most closely related to the
wood warblers...” The fifth edition of the
American Ornithologists’ Union Check-list
(1957) placed /cteria between Chamaeth-

/ypisand Euthlypis, without even a foot-
note, and its acceptance as a paruline
seemed to be settled, but not for long.

Eisenmann (1962) reopened the debate
by questioning the validity of Chamaeth-
/ypis as distinct from Geoth/ypis and sug-
gested these two genera be merged. Part of
his argument related to Ridgway’s (1902)
statement that /cteria was linked to the
typical parulines via Chamaethl/ypis and
Granatellus. Eisenmann sought, and found,
support for the idea that “Recent anatomical
studies strongly suggest that /cteria is
probably out of place in the wood-
warblers.” The evidence cited by Eisenmann
included “ /n //tt” communications from W.
J. Beecher, who noted that a reexamination
of his notes on the jaw musculature of /cte-
ria showed that it “could be a tanager’;
from William George, who reported that, in
certain aspects, the hyoid apparatus of /cte-
ria differs markedly” from that of “all conti-
nental genera traditionally included in the
Parulidae,” as well as from that of “numer-
ous genera of tanagers and other Oscines’;
and from C. G. Sibley who advised Eisen-
mann “that the electrophoretic patterns of
the egg-white proteins” of /cteria “are strik-
ingly different” from those of the “typical”
warblers and tanagers that were examined.

Eisenmann’s paper stimulated Ficken
and Ficken (1962) to add to the evidence
that “the Yellow-breasted Chat is not prop-
erly classified as a parulid.” They cited as
“aberrant characters” of /cteria its nest
structure, eggs, lack of natal down, com-
plete post-juvenal molt (“which also occurs
in Geothlypis trichas, but not in most other
warblers”), color of mouth lining, song char-
acteristics, nocturnal singing, courtship dis-
play, lack of a distraction display, and the
habit of holding food with its feet. They
concluded that “the Chat is not a parulid,
but that its true relationships remain
obscure.”

These observations served to reopen the
debate about the relationships of /cteria, al-
though it now seems clear that the senior
author provided Eisenmann with erroneous
information in 1962. We do not now recall
the basis for the statement quoted by Eisen-

3 Yellow-breasted Chat Relationships

Postilla 187

mann (1962) but an examination of the
electrophoretic patterns of the groups in
question (Sibley, 1970, fig. 28), reveals that
those of /cteria match those of the paruline
Warblers and other New World nine-
primaried oscines, rather than being “strik-
ingly different” from them.

New data on this problem have been
presented by Avise et al. (1980a) from elec-
trophoretic comparisons of 16 proteins in
28 species representing 12 genera of paru-
line warblers (including /cteria), a thrush
(Catharus ustulatus), and a vireo ( Vireo
olivaceus). They found that /cter/a, al-
though the most distinctive of the wood
warblers, is closer to them than to the
thrush or the vireo.

In this paper we report the results of
Comparisons among the homologous nu-
cleotide sequences of the single-copy
DNAs of /eteria virens and representative
genera of the wood warblers (Parulini), the
tanagers (Thraupini), the buntings (Emberi-
Zini), the New World blackbirds (icterini),
the cardueline finches (Carduelini), the
Vireos (Vireonidae), the mimic thrushes
(Muscicapidae: Mimini) and the wrens
(Troglodytidae). These taxonomic alloca-
tions follow Sibley (1970) and Sibley and
Ahlquist (1980; in press, a,b,c,e,f).

In addition, we doubt the interpretation
of the evidence that has been presented
purporting to show that the proteins, and
Presumably also the DNAs, of birds evolve
More slowly than do those of mammals
and reptiles.

Methods

The genetic material, DNA (deoxyribonu-
Cleic acid), is composed of two linear
Chains of four kinds of subunits called nu-
Cleotides. The four types of nucleotides
differ in the structures of their “bases,”
Which are adenine (A), guanine (G), thymine
(T), and cytosine (C). In double-stranded
DNA the four bases occur as complemen-
tary pairs, an adenine in one chain can pair
Only with a thymine in the other, a guanine
Can pair only with a cytosine. This A-T and

G-C base pairing results in the two single
strands being complementary nucleotide
sequences of one another. Genetic informa-
tion is encoded in the sequence of the
bases in the DNA strands.

In this paper the word “homologous” is
used with two meanings. As applied to nu-
cleotide sequences it means that two se-
quences, or genes, are the descendants of
the same sequence In the common ances-
tral species. This equals the “orthologous”
type of homology of Fitch (1976:161),
defined as two different genes “whose dif-
ference is a consequence of independence
arising from speciation... because there is
an exact phyletic correspondence between
the history of the genes and the history of
the taxa from which they derive.” Homolo-
gous, as applied to DNA-DNA hybrids,
means a homoduplex hybrid composed of
labeled and unlabeled DNA of the same
species. Heterologous (or heteroduplex) hy-
brids are composed of DNAs from two dif-
ferent species.

The DNA hybridization technique takes
advantage of the complementary structure
of the double-stranded DNA molecule.
When double-stranded DNA in solution is
heated to ca. 100°C the hydrogen bonds be-
tween A-T and G-C base pairs dissociate
and the two strands separate. Under proper
conditions of temperature and salt concen-
tration the two single strands will reassoci-
ate as the solution cools because the
complementary bases “recognize” one
another. If the temperature is maintained at
a high enough level, e.g., 60°C, complemen-
tary base pairing will occur only between
long homologous sequences of nucleotides.
This is because only long sequences of
complementary bases will have sufficient
bonding strength to form stable duplexes
at that temperature, and only homologous
sequences possess the necessary degree of
complementarity. Thus, under appropriate
conditions of temperature and salt concen-
tration, conspecific double-stranded DNA
may be thermally dissociated and, because
of their inherent properties, the single
strands will reassociate only with their
homologous partners.

4 Yellow-breasted Chat Relationships

Postilla 187

Similarly, if the single-stranded DNAs of
two different species are combined under
conditions favoring reassociation hybrid
double-stranded molecules will form be-
tween homologous sequences. These se-
quences will contain mismatched bases as
a result of the nucleotide sequence dif-
ferences that have evolved since the two
species diverged from their most recent
common ancestor. The lower bonding
strength of such hybrid duplexes will cause
them to dissociate at a temperature lower
than that required to melt conspecific
double-stranded DNA. Thus the property of
sequence recognition exhibited by homolo-
gous sequences and the decreased thermal
stability of imperfectly matched hybrid se-
quences form the basis of the DNA-DNA
hybridization technique.

The extent of base pair matching be-
tween the homologous nucleotide se-
quences of any two DNAs can be deter-
mined by measuring (1) the percentage of
hybridization and (2) the thermal stability of
the reassociated duplex molecules. Follow-
ing is a synopsis of the technique which is
described in more detail by Sibley and Ahl-
quist (1981).

Nuclear DNAs from avian erythrocytes
were purified (Marmur 1961, Shields and
Straus 1975), sheared to an average frag-
ment length of ca. 500 nucleotides by soni-
cation, and sized by electrophoretic com-
parison with DNA fragments of known size
produced by the digestion of bacteriophage
DNA with bacterial restriction endonuc-
leases (Nathans and Smith 1975). Single-
copy DNA was prepared consisting of one
copy per genome of each single-copy se-
quence, plus at /east one copy per
genome of each repeated sequence. Such a
preparation contains more than 98% of the
“complexity” of the genome, i.e., the total
length of a/fferent DNA sequences (Britten
1971). Kohne (1970:333-347) discussed
the method and reasons for removing the
extra copies of repeated sequences in stud-
ies designed to determine “the extent of nu-
cleotide change since the divergence of
two species” (p. 347). We removed the
excess repetitive sequences by reassociat-

ing the single-stranded DNA of the species
to be “labeled” with radioiodine to a Cot
value of 1000 at 50°C in 0.48M sodium
phosphate buffer (Cot = the initial concen-
tration of DNA in moles per liter times the
time of incubation in seconds). (Kohne
1970:334).

The single-copy sequences were labeled
with radioactive iodine ('*°l) according to the
procedures of Commorford (1971) and
Prensky (1976). DNA-DNA hybrids were
formed from a mixture composed of one
part (=250 ng) '°l-labeled single-copy
DNA and 1000 parts (=250 jg) of sheared,
whole DNA at a concentration of 2 mg/ml
in 0.48 M sodium phosphate buffer. The
hybrid combinations were heated to 100°C
for 10 min to dissociate the double-
stranded molecules into single strands,
then incubated for at least 120 h (=Cot
16,000) at 60°C to permit the single strands
to form double-stranded hybrid molecules.

The hybrids were bound to hydroxyapa-
tite columns immersed in a temperature-
controlled water bath at 55°C and the tem-
perature was then raised in 2.5°C incre-
ments from 55°C to 95°C. At each of the 17
temperatures the single-stranded DNA was
eluted in 20 ml of 0.12M sodium phosphate
buffer.

The radioactivity in each eluted sample
was counted in a Packard Model 5220
Auto-Gamma Scintillation Spectrometer,
optimized for '°|. A teletype unit connected
to the gamma counter printed out the data
and punched a paper tape which is the
entry to the computer program.

The computer program used a nonlinear
regression least squares procedure to deter-
mine the best fit of the experimental data to
one of four functions: 1) the Normal, 2) the
dual-Normal, 3) the “skewed” Normal, or 4)
a modified form of the Fermi-Dirac equa-
tion. The modal temperatures for each
hybrid were calculated from the fitted
curves. The differences (in °C) between the
mode of the homologous hybrid, and that
of a heterologous hybrid is the delta mode.

5 Yellow-breasted Chat Relationships

Postilla 187

Results

Table 1 contains the delta mode values and
Figure 1 is adiagram constructed from
them. The delta mode values are measure-
ments between the labeled species and the
other species in Table 1, but not among the
other species. However, two species that
have the same delta mode value are
equidistant from the labeled taxon, but
they can be any distance from one another
Which is equal to, or less than, their
common distance from the labeled species.

The data indicate that /cteria is most
Closely related to the wood warblers
(Geothlypis, Vermivora, Dendroica), and
that the tanagers ( Tangara, Ramphocelus),
the bunting (Zonotrichia), the grackle
(Quiscalus), and the cardueline (Carpo-
dacus) are progressively more distant.
These genera are members of the Fringilli-
dae as defined by Sibley (1970), and Sibley
and Ahlquist (in press, a, c, e, f). The vireo,
the catbird, and the wren are still more dis-
tant from /cteria. Because /cteria is a vocal
mimic it has been proposed that it might be
related to the mockingbirds (Miminae), but
the /cteria:Dumetella delta mode value of
11.0 indicates that the two taxa are as dis-
tant from one another as /cteria is from the
wrens (11.9) or, as reported by Sibley and
Ahiquist (in press, a), as Himatione is from
Sturnus, Monarcha, Turdus, Sylvia, Vireo,
and Corvus, which differ from Himatione
by delta modes from 10.2 to 11.0 (average
== HO} 7A).

The DNA hybridization data indicate
that /cteria is a wood warbler, although it
Must represent an early branch in the phy-
logeny of the group. Its atypical anatomical
and behavioral characters should be
Viewed as adaptive specializations, not as
evidence that /cteria is more closely related
to some group other than the Parulini.

The vireos have been thought to be
Closely related to the New World nine-
Primaried oscines at least since 1930,
when Wetmore placed them next to the
New World nine-primaried groups. Table 1
Includes a DNA hybrid between /cteria and

the Red-eyed Vireo ( Vireo olivaceus)
which has a delta mode value of.10.4.
Similarly, in our study of the Hawaiian
honeycreepers (Fringillidae:Carduelinae:
Drepaninini) a DNA hybrid between the
Apapane (Himatione sanguinea) and the
Red-eyed Vireo had a delta mode of 11.3
(Sibley and Ahiquist, in press, a). These
data indicate that Vireo is not closely relat-
ed to the New World nine-primaried assem-
blage. Avise et al. (1980a) presented evi-
dence that Vireo is even more distant from
the paruline warblers than are the turdine
thrushes, represented by the Swainson’s
Thrush (Catharus ustulatus).

A DNA hybridization study in which
Vireo olivaceus was the radioiodine-
labeled taxon has shown that the typical
vireos ( Vireo, Hylophilus), the pepper-
shrikes (Cyc/arhis) and, presumably, the
shrike-vireos ( Vireo/anius) are closely relat-
ed to one another, and are not closely relat-
ed to the American nine-primaried groups.
Instead, they are members of a large,
varied, “corvine assemblage” that includes
the corvids, monarch flycatchers, cuckoo-
shrikes, oriolids, birds-of-paradise, wood
swallows, cracticids, drongos, and shrikes.
The DNA hybrids between Vireo and mem-
bers of these groups have delta values be-
tween 7.5 and 9.4 (Sibley and Ahlquist, in
press, c). Additional data pertaining to the
“corvine assemblage” are included in Sibley
and Ahlquist (in press,d, g, h, i).

6 Yellow-breasted Chat Relationships Postilla 187
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o 5 Wn
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a Po es gs oS a ° oO
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ete 5 eect eee Soe ieee
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14

Fig. 1

Diagram based on the delta mode values given in
Table 1. Because only the DNA of the Yellow-
breasted Chat was labeled with radioactive iodine,
the diagram depicts only the distances between it
and the other taxa and not among those taxa.

7 Yellow-breasted Chat Relationships Postilla 187

Table 1.
Modal and delta modal values for DNA-DNA hybrids between the
radioiodine (1251)-labeled DNA of the Yellow-breasted Chat

and the DNAs of some other passerine birds.

COMMON NAME SCIENTIFIC NAME MODE AMODE
Yellow-breasted Chat Ieterta virens 3c, O50)
Common Yellow-throat Geothlypts trtchas 80.5 B55)
Tennessee Warbler Vermtvora peregrina 80.0 SPAA5)
Magnolia Warbler Dendrotea magnolia UD 52) 6.0
Scrub Tanager Tangara vitrtolina So 5)
Silver-beaked Tanager Ramphocelus carbo Uae 6.6
Song Sparrow Zonotrtchta melodta 78.4 7.4
Common Grackle Qutscalus qutscula LSS Ss
Purple Finch Carpodacus purpureus TESS, hs)
Red-eyed Vireo Vireo oltvaceus 75.4 10.4
Gray Catbird Dumetella carolinensis 74.8 IEE)
Bewick's Wren Thryomanes bewtektt W329 JIS)

8 Yellow-breasted Chat Relationships

Postilla 187

Discussion

/cteria is but one of many avian genera
whose relationships have been unclear.
The Wrenthrush, Ze/edonia coronata, was
considered to be a turdine thrush until the
electrophoretic pattern of its egg white pro-
teins revealed its relationship to the wood
warblers (Sibley, 1968), and the Swallow-
tanager, 7ersina viridis, often placed in a
monotypic family, is clearly a somewhat
modified tanager (Sibley, 1973). The Hoat-
zin (Opisthocomus) was placed in the Gal-
liformes because of its superficial similarity
to the chachalacas (Orta/is), but its egg
white proteins (Sibley and Ahiquist, 1973)
revealed its cuculiform affinities. There are
many additional examples of morphologi-
cally distinctive species of birds which
have been viewed as taxonomically distant
from their closest relatives. The discrepancy
between our perception of taxonomic rela-
tionships based upon visible morphological
characters, and evidence of relationships
derived from comparisons of proteins
and/or DNAs, deserves careful scrutiny, for
it has important implications for systematic
and evolutionary biology. One of the mani-
festations of this problem is the debate as
to whether or not avian protein molecules
evolve more slowly than do those of other
animals.

One of the most interesting and contro-
versial discoveries in recent years has been
evidence that the amino acid sequences of
proteins and the nucleotide sequences of
DNA evolve at remarkably uniform average
rates. The concept of the “molecular clock,”
first proposed by Zuckerkandl and Pauling
(1962), has been discussed by many au-
thors, including Fitch (1976), Wilson et al.
(1977), and Doolittle (1979). We have found
evidence for a uniform average rate of
DNA evolution (i.e., nucleotide substitution)
in our studies of the ratites (Sibley and Ahl-
quist, 1981), the Hawaiian honeycreepers
(Sibley and Ahlquist, in press, a), the New
Zealand Wrens (Sibley, Williams, and Ahl-
quist, in press), the vireos (Sibley and AhI-
quist, in press, c) and the Australian fairy-
wrens (Sibley and Ahlquist, in press, h).

Although there is considerable evidence
that DNA and proteins evolve at constant
or uniform average rates, several studies
have led their authors to suggest that the
proteins of birds may evolve more slowly
than do those of other animals (Prager et
al., 1974; Prager and Wilson, 1975; Barrow-
clough and Corbin, 1978; Avise et al.,
1980a, b).

Prager et al. (1974) first suggested that
avian proteins evolve more slowly than do
those of other organisms. They used the
technique of microcomplement fixation
and concluded that the ovotransferrins and
serum albumins of birds have evolved more
slowly than those of mammals, reptiles, or
frogs.

The average rate of transferrin evolution
in birds was calculated as 1.2 “immunologi-
cal distance” (I.D.) units per million years,
compared with 2.6 |.D units in mammals
and 4.7 in snakes. The authors concluded
that the rate of transferrin evolution in
mammals is “about twice as great as in
birds” and that in snakes it “appears to be
nearly 4 times as great as in birds” (p. 253).
But the authors did not comment on their
evidence showing that snake transferrins
apparently evolve 1.8 times as fast as do
those of mammals. Thus mammalian trans-
ferrins appear to evolve faster than those of
birds, but slower than those of snakes.

Prager et al. (1974) used the 27 “orders”
of birds recognized by some contemporary
avian systematists (e.g., Wetmore, 1960)
and an estimate of fossil datings to arrive at
an average interordinal divergence time of
100 million years (MY; MYA, million years
ago).

It is not easy to refute some aspects of
the study by Prager et al. but we do not be-
lieve that the fossil datings are accurate nor
that the 27 “orders” are equivalent to one
another. From our admittedly preliminary
and incomplete DNA comparisons it seems
clear that some of these “orders” diverged
more recently than 85 MY ago. At least
one, the “Apterygiformes” of Wetmore
(1960), diverged from the “Casuariiformes”
not more than 50 MYA (Sibley and Ahiquist.
1981) and few of the living groups diverged

9 Yellow-breasted Chat Relationships

Postilla 187

more than 100 MYA (Sibley and Ahlquist,
unpublished).

We also doubt that the “orders” of birds,
mammals, and reptiles represent equivalent
degrees of evolutionary divergence. Instead,
we believe that avian orders are excessively
“split” and that those of mammals, and per-
haps also of reptiles, are overly “lumped.”
The lack of equivalence between the
boundaries of taxonomic categories within
and between birds and mammals is
demonstrated by the study of Avise et al.
(1980a) who defined the problem by stating

that protein evolution in birds appears con-
servative relative to that of many inverte-
brate and nonavian vertebrate groups. By
conservative we mean only that at equiva-
lent levels of taxonomic recognition many
birds appear to exhibit smaller genetic dis-
tances at protein-coding loci than of most
other kinds of organisms that have been
Surveyed. The reason for this conservative
pattern remains unknown. One possibility
is that protein evolution is decelerated in
birds; the protein “clock” may tick ata
slower pace.

Barrowclough and Corbin (1978:699,
table 5) summarized the data from several
Studies and compared the genetic dis-
tances (D) of Nei (1972) for Drosophila,
fish, salamanders, and mammals with
those for birds. For local populations the
nonavian average Nei distance (D) was
0.037, for birds 0.003; for subspecies the
Values were 0.199 and 0.008; for species
0.609 and 0.100, and for genera 0.783
and 0.213. Thus, compared with the
Values for birds, the nonavian distances
average nearly 12 times as large for local
Populations, 25 times for subspecies, six
times for species and 3.7 times for
genera. If these differences were due only
to a slowdown in the rate of avian protein
€volution, these ratios should be equal.

Avise et al. (1980a, fig. 1) compared
the Nei genetic distances for 27 species
Of wood warblers (excluding /cteria), a
thrush (Catharus), and a vireo ( Vireo)
with those of 14 species of New World
Cricetine rodents. For congeneric species

the rodents had an average Nei distance
of 0.40, the wood warblers 0.056: for dif-
ferent genera the rodents averaged 1.256,
the wood warblers 0.175. In both of these
cases the mammalian distances were
more than seven times the corresponding
values for the birds. /cteria, with a D value
of 0.48 from other parulines is considered
to be an aberrant wood warbler, but the
grasshopper mice (Onychomys) and the
white-footed mice (Peromyscus), at aD
of 0.56 from one another are considered
to be closely related by mammalian sys-
tematists. Thus, on the scale used for the
cricetines, there would be only two
genera of wood warblers for the 28 spe-
cies examined by Avise et al. (1980a), viz.,
/cteria, plus one other genus for the other
27 species which currently are distributed
among 11 genera!

The discrepancy is further demonstrat-
ed by the Nei distances among 11 species
of Dendroica plus those for Wi/son/a,
Setophaga, and Sejurus noveboracensis
which are less (ca. 0.09 maximum) than
the distance (0.11) between two closely
related species of mice, Peromyscus
maniculatus and P. polionotus. Eleven of
the 12 genera of wood warblers examined
by Avise et al. (1980a), cluster within a
Nei distance of 0.28, which is less than
the distance (0.34) between Peromyscus
/Jeucopusand P. maniculatus.

Avise et al. (1980b) have provided
another example by comparing the Nei
genetic distance values among 13 species
of North American sparrows and finches
with those among 13 species of sunfishes
(Centrarchidae). The 13 avian species are
usually placed in eight genera and two
families, Fringillidae and Emberizidae. The
123 sunfish species are divided among
six genera.

The 13 species of birds have a maxi-
mum Nei D value of 0.795 (Carpoda-
cus.Calcarius) and among six of the
eight genera the maximum D value is
0.327. Species placed in different genera
have D distances as low as 0.032 (Ammo-
dramus sandwichensis.:Zonotrichia albi-
collis).

10 Yellow-breasted Chat Relationships

Postilla 187

The D distances among the sunfishes
are much larger. The seven species of
Lepomis have a maximum D value of ca.
0.70 and the greatest distance between
two of the sunfishes is D=ca. 1.7. The
smallest D value among the sunfishes is
ca. 0.16, between Lepomis marginatus
and L. megalotis. The six genera are well
separated from one another and all inter-
generic D values are 0.7 or larger.

These examples illustrate the nature of
the evidence. If it is assumed that avian
taxonomic categories are equivalent to
those of nonavian taxa, it does indeed
appear that avian proteins diverge more
slowly than do those of other animals. But
if this assumption is wrong, the apparent
slowdown in the rates of change in avian
proteins may be an artifact resulting from
the different taxonomic evaluations ap-
plied to birds which are the result of cer-
tain aspects of their biology in which they
differ from many other animals.

Birds depend primarily, perhaps entire-
ly, upon vision and hearing to identify
conspecifics and to determine their sex.
As a result, they have evolved plumage
colors and structures, behavior patterns,
and vocalizations which function as
species-specific and sexual-recognition
signals. Conversely, most mammals,
salamanders, and invertebrates probably
utilize the chemical senses, especially ol-
faction, for the same purposes. Odors are
known to influence reproductive activities
in mammals (Bronson, 1974; Stoddart,
1980), and laboratory mice (Mus mus-
culus) can distinguish between the odors
of conspecific individuals belonging to
different histocompatibility groups
(Yamazaki et al., 1976, 1979).

Because humans, like birds, are visual-
auditory animals, we are able to detect
the actual signal characters used by birds
for species and sexual recognition. To our
eyes and ears the species of birds appear
distinct, but we often erect genera based
upon the secondary sexual characters of
males, especially in those groups in
which sexual dimorphism is pronounced.
Sibley (1957) discussed this problem,

cited examples from several groups of
birds, and concluded that excessive
generic splitting by avian taxonomists “is
due to erroneous human evaluation of the
taxonomic value of the signal characters.”

Some diurnal mammals use visual sig-
nals and have evolved visible species
specific external characters, but most
small mammals are nocturnal and even
distantly related species and genera tend
to look much alike to our eyes. The New
World cricetine rodents (Avise et al.,
1980a), although differing widely among
themselves on the Nei genetic distance
scale (up to D=1.8), are similar in color
and general appearence. We perceive
them as similar in external morphology
and emphasize their similarities by plac-
ing them in the same subfamily and in
large genera composed of genetically di-
verse species. Birds are certainly too
finely “split” at the generic and familial
levels, but small nocturnal mammals may
be too “lumped” at these levels.

Some ornithologists have long been
aware of these problems which exist
even within the Class Aves in which there
is a lack of equivalence between passe-
rines and nonpasserines in the taxonomic
ranking of Supraspecific categories. Scla-
ter (1880:345-6) noted that “the Oscines
are all very closely related to one another,
and, in reality, form little more than one
group, equivalent to other so-called fami-
lies of birds.” Similarly, Gadow (1891:252)
suggested that “strictly speaking, all of
the Oscines together are of the rank of
one family only.” Lucas (1894) also
emphasized that the passerines have usu-
ally been split into too many families, and
Furbringer (1888) recognized only two
families of passerines. However, Sharpe
et al. (1877-90) used 29 families for the
oscines (including Menuridae and Atri-
chornithidae) and more recent classifica-
tions divide the same group into 51 (Stre-
semann, 1934), 52 (Mayr and Amadon,
1951), or 72 families (Wetmore, 1960).
From our preliminary DNA hybridization
data we suspect that the oscines
(Passeres) are composed of between 10

11 Yellow-breasted Chat Relationships

Postilla 187

and 20 clusters that may be approximate-
ly equivalent to most of the families of
nonpasserines.

The range of opinion about the classifi-
Cation of the Passeres is exemplified by the
cluster of taxa known as the “New World
nine-primaried oscines.” Mayr and Amadon
(1951) divided them into five families with
seven subfamilies, Wetmore (1960) into
eight families, and Wolters (1980) used 12
families and 11 subfamilies. We have pro-
posed that the same groups should be
included in a single family
(Fringillidae) with two (or three) subfamilies,
and eight tribes (Sibley, 1970:99; Sibley
and Ahlquist, in press, a, e, f). Sibley
(1970:100) suggested that this “should be
accompanied by a correlated reduction in
the number of genera to be recognized.”
When Martin and Selander (1975), Martin
(1980), and Smith and Zimmerman (1976)
found biochemical evidence of close rela-
tionships they recommended that certain
passerine genera should be merged.

The number of orders into which birds
have been divided has also varied widely.
Huxley (1867) used only two orders, four
Suborders, and 24 “groups” the latter appar-
ently equivalent to superfamilies. Sclater
(1880) made 26 orders for living birds but
Furbringer (1888) used only seven orders,
21 suborders, 39 “gens,” and 76 families,
while Seebohm (1890) divided the birds
into six subclasses, 14 orders, and 36
Suborders.

Among the current classifications, Mayr
and Amadon (1951) used 28 orders and
Wetmore (1960) used 27, but Wolters
(1975:4) divided the living birds into 49
orders. Again, from our preliminary DNA hy-
bridization data, we suspect that living
birds can be divided into approximately 20
groups that will merit ordinal rank.

The discrepancy between avian and
Mammalian orders was apparent to Romer
(1962:67) who suggested that “apart from
the ratites, most birds... are rather uniform
in basic anatomic features, with differences
between orders no greater than those
which distinguish the smaller groups,
termed families, among mammals.” This

could also mean that the mammalian
orders are overly large.

If the number of avian genera is reduced
in proportion to the reduction in other
categories the discrepancy between avian
and mammalian taxa will also be reduced.
Bock and Farrand (1980) suggested that
the ca. 2945 genera of birds currently
recognized could be reduced to ca. 1000.
They note that “avian genera are too finely
divided and that the genus... has limited
meaning in avian classification.”

Although birds are apparently too finely
divided at the generic, familial, and ordinal
levels, there is no reason to believe that
they are equally oversplit at the species
level. In fact, the human perception of avian
species is probably more nearly correct
than is our perception of species in many
other groups of animals. If this is true we
should expect to discover cryptic species in
some groups whose true distinctiveness
can be detected only by comparisons of
their proteins, their DNAs, or their actual
species recognition signals —for example,
odors or pheromones. This expectation has
been realized in a few cases as follows.

In an electrophoretic study of 22 protein
loci Patton et al. (1976), found that the
Heermann Kangaroo Rat (Dipodomys heer-
manni) of southern Oregon and California
is actually composed of two well-separated
species which had been considered con-
specific although one has five toes on the
hind feet, the other only four. The two spe-
cies also differ in the diploid number of
chromosomes. Similarly, Highton (1979)
discovered a cryptic species of lungless
salamander, Plethodon websteri, which is
morphologically indistinguishable from P.
dorsalis, but electrophoretically different
at 80% of 26 genetic loci. The two species
are sympatric at one locality in Alabama.

Manwell and Baker (1963) discovered a
sibling species of sea cucumber (Echinoder-
mata: Holothuroidea) when they found two
distinct electrophoretic patterns in a popu-
lation supposedly representing a single spe-
cies. After the two species were character-
ized electrophoretically the authors found
correlated morphological differences

7 Yellow-breasted Chat Relationships

Postilla 187

which had been attributed to individual
variation.

In birds there are valid species that are
difficult to distinguish visually but whose
vocalizations are species specific. Examples
include the tyrannid genera Empidonax
(Stein, 1963; Johnson, 1963), Myiarchus
(Lanyon, 1978), and Contopus (Rising and
Schueler 1980). Conversely, some avian
subspecies are so different in external mor-
phological characters that they were long
considered to be separate species — for
example, the eastern, western, and south-
western races of the Common Flicker
(Colaptes auratus) (Short, 1966), the eas-
tern and western races of the Rufous-sided
Towhee (Pipilo erythrophthalmus)
(Sibley, 1950; Sibley and West, 1959), and
the eastern and western races of the
Yellow-rumped Warbler (Dendroica
coronata) (Hubbard, 1969; Barrowclough,
1980).

It is also clear that closely related species
of birds can exist in sympatry without hy-
bridizing. The visible and audible species-
specific recognition signals of birds are
detectable at a considerable distance and
function as premating isolating mecha-
nisms which prevent pair formation. Evi-
dence for this comes from the occasional
hybrids between congeners that are widely
sympatric but which hybridize only where
one of them is uncommon and, therefore,
the choice of mates is limited. Examples in-
clude the woodpeckers Pico/des pubes-
censand P. nutta/lii (Short, 1969) and the
bulbuls Pycnonotus caferand P. /eucoge-
nys (Sibley and Short, 1959).

However, even if hybrids do occur be-
tween closely related species of small
mammals, salamanders, or other groups of
visibly similar species, they would be diffi-
cult to detect by the examination of stan-
dard museum specimens. The detection of
avian hybrids is much easier because the
plumage characters of most closely related
species are visibly different and the hybrids
are distinctive.

There are probably other factors perti-
nent to this problem but we believe that the
evidence for an alternative explanation for

the suggested slowdown in the evolution
of avian proteins is sufficient to render it
doubtful. We suggest that the alleged slow-
down is primarily the result of the limita-
tions of human perception, not of some un-
known difference between the genomes of
birds and other animals.

The problem of the equivalence of
taxonomic categories is not confined to the
genera and families of vertebrates. Van
Valen (1973) questioned the equivalence of
the categories in different phyla and it
seems clear that the nonequivalence we
have noted among birds, fishes, and mam-
mals begins with the lack of equivalence
between the groups usually designated as
“Classes” in the vertebrates. These are the
Agnatha (jawless fishes), Placodermi
(jawed, armored fishes), Chondrichthyes
(sharks, rays), Osteichthyes (bony fishes),
Amphibia, Reptilia, Mammalia, and Aves.
These groups are traditionally treated as
categorical equivalents, but the Agnatha
appear in the fossil record as the jawless os-
tracoderms in the Ordovician (ca. 450
MYA), the placoderms, Chondrichthyes
and Osteichthyes in the late Silurian or
early Devonian (ca. 400 MYA), the Amphib-
ia in the late Devonian (ca. 350 MYA), the
Reptilia in the Carboniferous (ca. 300 MYA),
the Mammalia in the Triassic (ca. 195
MYA), and the Aves in the Jurassic (ca. 130
MYA). The oldest “Class” is nearly three
times as old as the youngest. Furthermore,
it is apparent that the later groups diverged
from the earlier ones and we therefore have
Classes evolving from Classes, a logical
non sequitur Each so-called Class of verte-
brates is subdivided into orders, families,
etc., using intraclass characters and the in-
evitable result is categorical nonequival-
ence throughout the system.

The idea that categorical levels might be
based upon times of divergence was reject-
ed by Simpson (1937) and Mayr
(1969:72,230) because it seems apparent
that we perceive morphological change as
proceeding at many different rates, and
there is no way known to quantify the de-
grees of difference among morphological
characters to reflect degrees of evolutionary

iis Yellow-breasted Chat Relationships

Postilla 187

divergence. However, Simpson (1944:3)
Stated that “Rate of evolution might most
desirably be defined as amount of genetic
change in a population per year, century, or
other unit of absolute time.” But, in 1944,
there was no way to measure such a rate of
genetic change so Simpson defined the
rate of evolution as the “amount of mor-
phological change relative to a standard”
and assumed that phenotypic evolution im-
plies genetic change and that rates of mor-
phological evolution “are similar to, al-
though not identical with, rates of genetic
modification.” This assumption has been
implicit (and often explicit) in all
morphologically-based classifications of
recent years. Unfortunately, it is not true
(e.g., Wilson, 1976).

Hennig (1966) has been the principal, if
not the only, proponent of the age of origin
as the basis for the absolute ranking of taxa.
He considered the equivalence of ranking
to be a serious and important problem, the
lack of which is an enormous burden upon
systematics that prevents the development
of a consistent and maximally useful
Classification. Hennig (1966:84, 146, 156,
160) recognized the limitations of morphol-
Ogy as the basis for determining the abso-
lute rank order of taxonomic groups; so he
proposed (pp. 180-182) that the relative
rank be determined from morphology and
that, where possible, fossil datings and
other evidence be used to establish refer-
€nce points in the system. He suggested
that “there is no single method with which
the age of origin can be determined accu-
rately” and that only minimal and maximal
limits can be recognized.

As a compromise, Hennig (p. 191) sug-
gested that the present absolute ranking be
retained in most groups and that a “conver-
Sion chart” be developed to show the
€quivalent categories in different groups.

Hennig’s reason for favoring such a com-
Promise identifies one source of the prob-
lem, and what will surely be a barrier to the
general acceptance of a time-based ranking
of categories. He wrote (p. 191),

... taxonomists are essentially specialists
—entomologists, arachnologists, ornitholo-
gists, etc.—who... usually work only in cer-
tain sections of these extensive areas. All
these specialists work as if only their group
of animals existed. Consequently each spe-
cialist can erect a consistent phylogenetic
system for his group without any necessity
for correspondence on the basis of equiva-
lent age between the absolute rank order of
his categories and the absolute rank order
of other groups of animals. Presumably
even the most convincingly presented ob-
jective reasons will not bring these special-
ists to the point of giving up life-long habits
and speaking of classes and orders where
they are accustomed to speaking of families
and vice versa.

We agree with Hennig that the absolute
ranking of taxonomic categories should be
based upon the age of origin, and that sister
groups should be of equivalent rank. But
our reasons for supporting this position are
based upon evidence from DNA compari-
sons which indicate that the average rate
of DNA evolution (i.e., nucleotide substitu-
tion) is the same in all lineages. This un/-
form average rate of genetic change
meets Simpson's (1944:3) criterion for the
most desirable definition of the rate of evo-
lution and is concordant with Hennig’s
arguments in favor of a time-based ranking
of taxa.

We have presented the arguments and
evidence for the uniform average rate else-
where (Sibley and Ahlquist, 1981; in
press,a; Sibley, Williams, and Ahliquist, in
press). The essential points are that DNA
hybridization measures the net divergence
between the homologous nucleotide se-
quences of different taxa and that the uni-
form average rate of change is a Statistical
result of the large number of nucleotides in
the eukaryotic genome, e.g.,ca.2 X 10% in
mammals and birds. Each nucleotide
evolves at its own rate, and different se-
quences evolve at different rates at different
times, but when averaged over the
genome and over time, the uniform average
rate is the inevitable result because there
are upper and lower bounds to the rates

Yellow-breasted Chat Relationships Postilla 187

and the frequency distribution of rates is
narrow relative to the number of nucleo-
tides. Thus the rates are not constant, but
the average rates in all lineages are
uniform.

This means that the DNA hybridization
data provide the relative time of divergence
for any two taxa that are compared. When
the DNA values are calibrated against
geological or fossil dates the DNA data pro-
vide the absolute times of branching and
may, therefore, be used to develop a time-
based absolute ranking of taxa which Is
equivalent to genetic divergence. Because
of technical limitations the DNA hybridiza-
tion data can be used only for taxa that di-
verged during approximately the past 150
MY. However, there are other techniques
that can extend the time to the earliest peri-
ods of life on Earth. For example, the se-
quences of the 16S ribosomal RNAs have
been used to determine phylogenetic rela-
tionships among bacteria, including diver-
gences that occurred as much as three bil-
lion years ago (Fox, et al., 1980; Woese,
1981).

We therefore propose that the major,
and especially the older, dichotomies be
dated by the best available fossil and/or nu-
cleic acid sequence evidence and that DNA
hybridization data be used to develop a
genetic divergence-based, and hence time-
based, system of taxonomic categories rep-
resenting the dichotomies of the last 150
MY. This can largely solve the rank equival-
ence problem although, as Hennig so
pessimistically predicted, it may take a gen-
eration or two of systematists to win
acceptance.

Acknowledgments

For assistance in the laboratory we thank C.
Barkan, M. Pitcher, N. Snow, and F.C. Sibley.
The computer program was written by TF.
Smith. For advice we are indebted to R.J.
Britten, D.E. Kohne, R. Holmquist, G.F.
Shields, W.F. Thompson, H.E. Burr, and
W.M. Fitch.

For assistance in the field we thank F.C.
Sibley, J. Spendelow, J. O'Neill, R. Semba, J.
duPont, and N. and E. Wheelwright.

The laboratory work was supported by
Yale University and the National Science
Foundation (DEB-77-02594 and
DEB-79-26746).

15 Yellow-breasted Chat Relationships Postilla 187

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17 Yellow-breasted Chat Relationships Postilla 187

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19 Yellow-breasted Chat Relationships Postilla 187

The Authors

Charles G. Sibley and Jon E. Ahiquist.
Department of Biology and Peabody
Museum of Natural History, Yale University,
170 Whitney Avenue, P.O. Box 6666,

New Haven, CT 06511