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doi:10.1111/j.1558-5646.2007.00254.x
THE GENETIC BASIS OF SEXUAL DIMORPHISM
IN BIRDS
Jerry A. Coyne,1,2 Emily H. Kay,1,3,4 and Stephen Pruett-Jones1,5
1 Department
of Ecology and Evolution, The University of Chicago, 1101 E. 57 Street, Chicago, Illinois 60637
2 E-mail:
j-coyne@uchicago.edu
4 E-mail:
emilyhokay@gmail.com
5 E-mail:
pruett-jones@uchicago.edu
Received July 17, 2007
Accepted August 31, 2007
The genetic basis of sexual dimorphisms is an intriguing problem of evolutionary genetics because dimorphic traits are limited to
one sex. Such traits can arise genetically in two ways. First, the alleles that cause dimorphisms could be limited in expression to only
one sex at their first appearance. Alternatively, dimorphism alleles could initially be expressed in both sexes, but subsequently
be repressed or promoted in only one sex by the evolution of modifier genes or regulatory elements. We investigated these
alternatives by looking for the expression of sexually dimorphic traits in female hybrids between bird species whose males show
different types of ornaments. If modifier alleles or regulatory elements involved in sex-limited traits are not completely dominant,
the modification should break down in female hybrids, which might then show dimorphic traits resembling those seen in males.
Of 13 interspecific hybridizations examined, we found not a single instance of the expression of male-limited ornaments in female
hybrids. This suggests that male ornaments were sex limited from the outset or that those traits became sex limited through the
evolution of dominant modifiers—possibly cis-dominant regulatory elements. Observing hybrid phenotypes is a useful approach
to studying the genetics and evolution of dimorphic traits.
KEY WORDS:
Avian evolution, evolutionary genetics, gene regulation, sex limitation, sexual selection.
A difficulty which was regarded rather seriously during the
development of the theory of sexual selection is implicit in the
limitations of many of the structures ascribable to sex-limited
selection, to the particular sex on which selection acts. The
difficulty lay in how far selection acting on only one sex ought to
be expected to affect the characters of both sexes, and whether
a mutation originally affecting the development of both sexes
could be confined to one sex only, by counterselection on the
other sex.
R. A. Fisher (1930, p. 139)
As implied by Fisher in the quotation given above, there are
two ways that genes can produce the striking sexual dimorphisms
seen in many species of animals. The first is that the alleles for
3Present address: Department of Organismic and Evolutionary Bio-
logy and the Museum of Comparative Zoology, Harvard University,
26 Oxford Street, Cambridge, Massachusetts 02138.
C
214
dimorphic traits could be male-limited from the outset, with their
expression perhaps conditioned on physiological or hormonal differences between the sexes (we assume for convenience that such
traits are seen in males but not females). Alternatively, these alleles
could be expressed initially in both sexes, but then become limited
to males by the accumulation via selection of modifier genes (the
presumption is that male-specific ornaments are sexually selected
traits that are deleterious in females). This sex limitation could
itself evolve via two routes: the accumulation of modifiers (alleles or regulatory elements) that (1) suppress expression only in
females, or (2) promote expression only in males. At the end of
all of these processes, only males would show sexually dimorphic
traits. How, then, do we determine which genetic pathway has
occurred?
Unable to see how selection could limit to a single sex a
trait originally expressed in both sexes, Darwin (1871, p. 182)
C 2007 The Society for the Study of Evolution.
2007 The Author(s). Journal compilation Evolution 62-1: 214–219
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believed that dimorphic traits were male-limited from their first
appearance:
I have endeavored . . . to shew that the arguments are not trustworthy in favour of the view that weapons, bright colours, and
various ornaments, are now confined to the males owing to the
conversion, by means of natural selection, of a tendency to the
equal transmission of characters to both sexes into transmission to the male sex alone.
Fisher (1930), however, with characteristic enthusiasm for the
evolution of modifier alleles (a famous aspect of his theory about
the evolution of dominance), ascribed sexual dimorphisms almost
entirely to the appearance of the trait in both sexes followed by
the accumulation of suppressors in females. Yet there was no empirical evidence for this hypothesis at the time of Fisher’s writing,
nor is there any today.
Here we suggest one approach to this question. This involves
studying hybrids between species showing different forms or degrees of sexual dimorphism. Because the different evolutionary
ways that alleles could become male-specific in expression make
different predictions about what one might see in female hybrids,
an analysis of these hybrids might help us discriminate between
the hypotheses.
We envision three scenarios. In the first, we assume that in
two closely related species, males differ in the type or degree
of their sexually dimorphic traits, and that the traits were originally expressed in both sexes but later suppressed in females
by the accumulation of modifiers. (These modifiers could be either trans-acting genes or regulatory elements, or closely linked
cis-regulatory elements). If these two species were interfertile,
their F 1 female hybrids would carry some genes for sexual dimorphisms from each parental species (except for W-linked genes,
because female birds are heterogametic), but only a haploid set of
suppressors from each species. Unless the suppressors are completely dominant, hybrid females should show some expression
of the male traits.
In the second scenario, the alleles now expressed only in
males could have originally been expressed in both sexes, but the
evolution of “modifiers” (again, trans-acting genes or trans- or cisacting regulatory elements), could have led to those alleles being
expressed only in males, perhaps by bringing their transcription
solely under hormonal control. This leads to the same prediction
as that for female suppressors: unless the male-limited modifiers
or regulatory elements are completely dominant, hybrid females
between two species differing in male-specific traits should show
some expression of those traits. Although the first and second scenarios are mechanistically different, they could presumably occur
together, with the simultaneous evolution of female suppressors
and male promoters.
It is important to stress here that although alleles may be
presently activated or suppressed by evolved sex-specific modi-
fiers (perhaps regulated by hormones), this does not mean that
male traits could not appear in female hybrids. This is because
these females resemble in genetic constitution a partial ancestral
state in which (if the genes were not sex-limited from the outset)
“dimorphism” alleles were expressed in both sexes.
The third possibility is that alleles could be male-limited from
the outset, perhaps because they arose at genes that were already
male-limited, or arose fortuitously in regions under control of
cis-dominant elements activated only in males. In such cases, female hybrids would show no expression of male traits and would
presumably resemble intermediates between the nonornamented
females of the parental species.
Hybridization between species thus offers a way to study the
genetic basis of sexual dimorphisms. Species hybrids have been
used in other studies to reconstruct ancestral genetic conditions,
for example to look for meiotic drive alleles that have been fixed
in species but whose presence is undetectable unless they are
made heterozygous in species hybrids (Coyne 1989; Coyne and
Orr 1993).
Here we examine hybrid birds to determine whether female
interspecific hybrids show reexpression of “dimorphism” alleles
that may have been originally expressed in both sexes but later
suppressed in females. Birds are an obvious group in which to
examine this question because many species show extreme sexual
dimorphisms, are easily crossed, and hybrids have been documented extensively (e.g., Gray 1958; McCarthy 2006). Mundy
(2006, p. 495) even suggested that these hybrids could be used to
study the genetics of sexual dichromatism:
Although the genetic mechanisms controlling the presence of
dichromatism are poorly understood, it seems likely that they
are distinct in avian lineages with different hormonal mechanisms underlying dichromatism . . . . Crosses between closely
related species that differ in degree of dichromatism (e.g.,
among species in the mallard complex) provide a potential
route for investigating the genetic basis of dichromatism, but
such an approach does not appear to have been attempted.
We will show that, based on the hybrids and hybrid specimens
available, we find virtually no evidence for the expression of malelimited traits in female species hybrids, suggesting that the genes
for such traits are either male-limited from the outset or controlled
by completely dominant sex-limited modifiers.
Methods and Materials
We began our search for hybrid females with the recently published book Handbook of Avian Hybrids of the World (McCarthy
2006), which describes approximately 4000 interspecific and intersubspecific hybrids. We also looked for other female hybrids
by communicating with ornithologists, bird curators, and other
researchers who study avian hybrid zones. All of these workers
had personally examined hybrids.
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We narrowed our search to female hybrids between sexually
dimorphic species whose males possess different types of ornamental traits (e.g., distribution of color patches; presence/absence
of headwires, elongated feathers, or wattles). This maximized our
chances of seeing expression of dimorphic traits in female hybrids.
Related species whose males share similar types of dimorphic
traits (i.e., species having the same area of the body pigmented,
but in different colors) may be less useful for investigating the
origin of sexual dimorphisms: such species might have inherited
both the dimorphic trait and any female suppressors (or male promoters) from a common ancestor, and the lack of expression in
female hybrids might simply reflect their homozygosity for identical suppressors or promoters from that ancestor. We thus excluded
these cases (which were not numerous) from our study. For similar
reasons, we excluded hybrids between subspecies.
We further restricted our search to female hybrids who were
adults at the time of collection or observation. Age was determined from either information on the specimen tag or the literature. In nearly all sexually dimorphic birds, males do not acquire
dimorphic traits until they reach or approach breeding age. By
eliminating female hybrids collected as juveniles or immatures,
we avoided the possibility of their not showing male traits simply
because they were too young.
Some bird species also show seasonal variation in dimorphic
traits, with males of most species molting into a plumage less
bright or less exaggerated during the nonbreeding season. Were
this the case for some of our hybrids, it is possible that they would
not display male traits simply because they were collected during the winter months. However, in nearly every case included in
our analysis, the winter plumage of male parental species differs
substantially from that of females. Thus, our results should not
be markedly affected by the season at which the hybrid individuals were collected, as some evidence of male traits in mature
individuals would be detectable year round. The only two cases
in our dataset in which male traits disappear during molting involve the two duck hybrids. In most duck species, males drop their
body feathers rapidly twice each year during a period of “eclipse
plumage,” and resemble females for a few weeks. It is possible
that if the female duck hybrids given in Table 1 were collected
during this time, we may have missed some male-like traits expressed during most of the year. Nevertheless, we consider this
fairly unlikely because the interval of eclipse plumage occupies
only a small proportion of the year.
The number of known hybrid females that meet all of the
above criteria was surprisingly small (see below), although we
did not have the resources to personally examine all known
hybrid specimens in museums. We acknowledge that our list
is incomplete. Nevertheless, it is a representative list because
it includes hybrids in a wide range of taxa collected in many
places.
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It is also likely that many female hybrids have been collected
or observed but have not been correctly identified. The reason
for this has to do with how hybrids are recognized. Excluding
cases of hybridization in captivity, where the parentage of a hybrid is known precisely, all hybrid specimens that we found were
identified as hybrids either through DNA sequencing (one case:
Lazuli × Indigo Bunting), because they were reared in captivity
and parentage was known (six cases), or because the individual
showed morphological or plumage traits intermediate between
females of parental species who themselves had nonoverlapping
distributions of these traits (six cases). This latter method has been
used in the ornithological literature for over 100 years as the standard way to identify hybrids. Table 1 shows the methods by which
each hybrid was identified.
Because in many cases males of the parental species differ in
plumage but not size, it is often quite easy to identify male hybrids
but difficult or impossible to identify female hybrids. There are,
for example, no fewer than 30 known specimens of hybrid males
between the King Bird of Paradise (Cicinnurus regius) and the
Magnificent Bird of Paradise (C. magnificus), yet not a single
description of a female hybrid. The explanation is almost certainly
that females of the two parental species are nearly identical in
plumage and morphology, making it impossible without genetic
evidence to identify female hybrids.
Results and Discussion
Table 1 summarizes the crosses, the types of traits differing between male parent species, and a description of female hybrids.
Of the more than 4000 hybrids we considered, only 13 pairs met
our criteria. However, every one of these cases gives the same result: F 1 female hybrids do not show any sexually dimorphic traits
seen in males of the parental species. We note that this lack of expression is not because alleles for male-specific traits are simply
recessive in hybrids, for these traits are seen in male hybrids, which
invariably show dimorphic traits seen in males of both parental
species (see, for example, plate 15 of Frith and Beehler 1998,
showing the appearance of male interspecific hybrids in birds of
paradise).
A striking illustration of the absence of male traits in female
hybrids is given in plate 14 of Frith and Beehler (1998), depicting
hybrids in two pair of birds of paradise, each pair representing
an intergeneric cross (Table 1, see cover). Despite the fact that
males in each cross differ by diverse and elaborate characters
such as head wires, tail streamers, and iridescent colors, the female
hybrids are drab brown, lacking any trace of male ornaments, and
resembling the females of the parental species.
Because only 0.4% of all known bird hybrids are represented
in Table 1, it is possible that there is some ascertainment bias in
our table, and that our conclusions might not be general. But this
American Redhead×
Ring-necked Duck
Phasianus versicolor×
Chrysolophus amherstae
Chrysolophus amherstiae×
C. pictus
Tympanhuchus
phasianellus×T. cuipdo
Aythya americana×A. ferina
valisineria
Aythya americana×A.
collaris
Head and wing color, distribution
of body coloration
Wattles, elongated tail, coloration
of most body parts
Head, belly, and tail color;
distribution of body coloration
Eye combs, crest feathers,
coloration of throat sacs
Iris and bill color, distribution of
body coloration
Tail and breast color
Male ornamental traits
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Weller (1957), p. 32 n=1
Female “intermediate in morphological
and plumage characters between the
Redhead and Canvasback” (c)
“The female’s plumage contained more
gray than is normal for the Redhead,
and the lores and eye-ring were
whitish as in the Ring-neck” (c)
Intermediate plumage to females of
parent species (i)
Resembles female L. superba (i)
Frith and Beehler (1998),
pl. 14 n=1
Hopkinson (1926), p. 218
n=2
R. Payne (pers. comm.) n=3
S. Riplog-Peterson (pers.
comm.) n=1
M. Carling (pers. comm.)
n=2
Resembles female P. lawesii (i)
“Females are ‘exactly like’ F.
madagascariensis females.” (c)
Did not show any male traits (i)
Resembles a female Yellow Grosbeak,
did not show any male traits. (i)
One female showed plumage
intermediate to females of parent
species; the other resembled a female
P. amoena (DNA)
Short and Phillips (1966),
p. 255 n=2
Frith and Beehler (1998),
pl. 14 n=1
Weller (1957), p. 33 n=1
Deraniyagala (1953), p. 61
n=4
Hachisuka (1928), p. 77
n=1+
Danforth and Sandnes
(1939), p. 539 n=1+
R. Payne (pers. comm.) n=1
Source and sample size
Intermediate plumage to females of
parent species (c)
Intermediate plumage to females of
parent species (c)
Intermediate plumage to females of
parent species (c)
Did not show any male traits (i)
Description of female hybrid and
method of hybrid identification
Note: where samples sizes are shown as “n+1,” source did not give sample size but noted that more than one hybrid was examined.
Black-chinned Hummingbird× Crown and throat color
Costa’s Hummingbird
Superb Bird of Paradise×
Neck cape, head wires, iris color,
Carola’s Parotia
elongated breast and belly
feathers, iridescent crest and
throat
Parotia lawesii× Paradisasea Lawe’s Parotia×Blue Bird of
Head wires, tail streamers, iris
rudolphia margarita
Paradise
color, elongated flank and belly
feathers, iridescent throat and
tail
Foudia madagascariensis×
Red Fody× Vitelline
Iris color, distribution of body
Ploceus vitellinus
Masked-weaver
coloration
Uraeginthus bengalus×U.
Red-cheeked Cordon bleu×
Cap and cheek color
cyanocephalus
Blue-capped Cordon bleu
Pheucticus chrysopeplus×P. Yellow Grosbeak×
Head color, distribution of body
melanocephalus
Black-headed Grosbeak
coloration
Passerina cyanea×P. amoena Indigo Bunting×Lazuli
Wing bars, breast color,
Bunting
distribution of body coloration
Red Junglefowl×Ceylon
Junglefowl
Green pheasant×Lady
Amhersts’s Pheasant
Lady Amherst’s Pheasant×
Golden Pheasant
Sharp-tailed Grouse×Greater
Prairie Chicken
American Redhead×
Canvasback
Gallus gallus×G. lafayetti
Archilochus alexandri×
Calypte costae
Lophorina superba×Parotia
carolae
Common names
Latin names
Table 1. Adult female hybrids of bird species whose males differ in sexually dimorphic traits. Key to hybrid identification: c, hybrid reared in captivity; i, intermediate in femalerecognizable morphological traits; d, DNA haplotypes.
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possibility seems unlikely because our sampling represents four
orders and eight families of birds.
We conclude, then, that in our sample of species (and perhaps
in birds in general), male-limited dimorphic traits evolved in either
(or both) of two ways (1) The alleles responsible for such traits
were from their initial appearance expressed only in males. (2)
The alleles responsible for such traits were initially expressed in
both sexes, but then were either suppressed in females or became
limited to males by alleles or regulatory regions that are completely
dominant in hybrids.
We cannot from our data alone discriminate between these
two hypotheses. If the second hypothesis is true, the most likely
explanation for dominance would be cis-dominance, perhaps because “dimorphism” alleles have been brought under control by
a promoter region either suppressed or activated by hormones,
or by some product of genes in a pathway that is itself activated
by hormones. (One example of a cis-dominant promoter region
controlling a male-specific allele is the promoter element of the
yellow gene in Drosophila biarmipes [Gompel et al. 2005], which
is involved in creating a male-specific wing spot used in mating.)
Moreover, if the second hypothesis is true, then the absence of
male traits in any female hybrids implies that the “dimorphism”
alleles come under the control of regulatory genes fairly quickly,
before speciation is completed.
In principle, repressors or activators that are not dominant
could be identified by backcrossing hybrids to either parental
species. Some backcross females should be homozygous for suppressors or activators from one species but carrying “dimorphism”
alleles for the other, and should thus show male traits. Alternatively, one could look for male-like females in hybrid zones (which
may contain “natural” advanced intercross or backcross individuals) between two species having different dimorphisms. These
techniques will not work, however, if the dimorphism genes are
controlled by cis-dominant elements, as the genes and their regulators will not be separable in backcrosses.
We should emphasize that modifier alleles or regulatory
elements need not inevitably act in a dominant fashion. Even
cis-acting regulators need not be completely dominant (Duncan
2002). Regulators (and proteins involved in regulation, whether
linked or not) can also be trans-acting, and thus not invariably
dominant. Transcription factors, for example, are structural proteins that need not be linked to the genes they regulate, and other
proteins can act as cofactors during gene regulation; these possibilities show that gene regulation can evolve that is not cis-dominant
(Hoekstra and Coyne 2007). For example, in the study of Gompel
et al. (2005) described above, expression of the full wing spot
requires trans-acting in addition to cis-acting factors.
What traits could any male-limited genes “cue on” to limit
their expression to only one sex? The most obvious—and most
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EVOLUTION JANUARY 2008
likely—is hormones. It is well known that in birds the expression of sexually dimorphic traits is strongly affected by hormones
(Kimball 2006). In most groups of birds, plumage traits (e.g.,
feather color or elongation, appearance of color patches) appear to
be estrogen dependent, with male-specific traits expressed only in
the absence of that hormone. In the Charadriiformes and Passeriformes, however, male plumage appears to be testosterone dependent. In most groups, testosterone is also involved in inducing
nonplumage traits such as bill and leg color, presence of wattles,
spurs, and combs, as well as behavioral traits such as aggression
and male-specific sex displays (Owens and Short 1995; Kimball
2006). (In a few species, male-specific plumage traits are produced
directly by the presence of homogametic sex chromosomes.)
The molecular-genetic basis of sexually dimorphic morphological traits in birds is unknown, but much is known about the
molecular basis of sex-specific gene expression in other taxa.
In some cases, hormones such as androgen or estrogen bind to
transcription factors, and these complexes then interact with target sequences such as enhancers, causing sex limitation of gene
expression—and of the traits affected (e.g., Ning and Robins 1999;
Claessens 2001). This raises the possibility that evolution of the
transcription factors or cofactors, rather than of regulatory sequences themselves, may be involved in the sex-limitation of avian
dimorphic traits.
It seems likely, then, that any male-specific genes somehow
cue their expression on the absence of estrogen or the presence
of testosterone. This is supported by two anecdotal reports that
female hybrids in pheasants and ducks develop partial male-like
plumage when they are old or diseased, conditions that can reduce
the amount of estrogen (White 1900; Thomas 1914), a hormone
whose absence is known to induce male traits in Galliformes and
Anseriformes (Kimball 2006).
A supplemental approach to studying the genetics of sexual
dimorphism could involve manipulations, such as ovarectomies
or testosterone injections, which change the hormone titer in female hybrids of reciprocal crosses. The consequent expression
of male plumage in the reciprocal-hybrid heterogametic females
(assuming that such plumage is hormone dependent) could indicate whether interspecific differences in such traits reside largely
on the X chromosome. Such manipulations in backcross females
could further elucidate the genetics of dimorphic traits, including
whether any modifiers are dominant and always cosegregate with
the male trait (implying cis-dominant regulation).
We should note that our approach was limited to plumage
colors and ornaments in birds, but in principle could be extended
to behavioral traits. For example, the behavior of hybrid females
might also be examined in crosses between species whose males
show different mating displays. Our approach could, of course,
also be used in species other than birds.
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Finally, there is evidence that some alleles involved in some
sexual dimorphisms have not been male-limited from the outset.
These are cases in which females display some exaggerated malelike traits, but traits less extreme than seen in males. In the birds
of paradise, for example, male astrapias have very long tails (Frith
and Beehler 1998, plate 6); females have tails shorter than those
of conspecific males, but clearly longer than those of females
from related species. It is not clear whether in such cases the
exaggerated female trait may actually have an adaptive function
(e.g., social signaling or species recognition). Rudimentary female
versions of male traits might also function in both attracting mates
and in female–female contest competitions (Amundsen 2000).
Nevertheless, the presence of similar traits in both sexes, with the
males showing a more exaggerated form, suggests (but does not
prove) that such traits are based on the same alleles in males and
females.
In sum, we reinforce the suggestion of Mundy (2006) that
the study of hybrids can illuminate, in part, the genetic basis of
important morphological evolution. Because sexually dimorphic
traits are involved in processes as critical as mate choice and reproductive isolation, this approach may ultimately help us understand sexual selection in general, and speciation in particular. If
our results are general, they suggest that the origin of sexually
dimorphic traits in birds has followed a consistent pathway in all
taxa.
ACKNOWLEDGMENTS
This work was supported NIH grant GM058260 to JAC and NSF grant
IOB0516967 to SPJ. We are grateful for the assistance and correspondence of M. Braun, R. Brumfield, M. Carling, J. Confer, E. McCarthy,
D. McDonald, J. Hinshaw, R. Payne, S. Riplog-Peterson, S. Rohwer, G
Saetre, and A. Uy. H. Hoekstra, T. Price, J. True, and two anonymous
reviewers made helpful comments on the manuscript.
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Associate Editor: J. True
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