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Sexual Selection Resolves Sexual Antagonism in
Favour of the Homogametic Sex
Arianne Y. K. Albert & Sarah P. Otto
Department of Zoology, University of British Columbia, Vancouver, B.C. V6T 1Z4,
Canada
Evolutionary biologists have long puzzled over why female preferences evolve for
exaggerated male traits. Generally, female preferences for male display traits are
thought to enhance a female’s long-term fitness by increasing her offspring’s
fitness, either directly or through linkage between preference and trait loci1, 2.
Previous models assume that male traits have no fitness effects in females.
However, recent research suggests that substantial genetic variance results from
loci that are sexually antagonistic (with different alleles favoured in each sex3).
Such loci are disproportionately located on sex chromosomes3. How female
preferences evolve for traits under sexually antagonistic selection remains
unexplored. Here we show that with a sexually antagonistic trait on the X
chromosome (males XY, females XX), females evolve to prefer mates carrying
alleles beneficial to daughters. In contrast, with a Z-linked trait (males ZZ, females
ZW), females evolve to prefer mates carrying alleles beneficial to sons. This
provides a novel explanation for why males in ZW species have flashier sexual
displays than males in XY species.
Ever since the evolution of separate sexes, alleles have arisen that are
advantageous to one sex and deleterious to the other, creating conflict. Continuous
traits, for example, may have different optima in the two sexes (e.g. hip width in
humans4); and different colouration patterns are often favoured in each sex5, 6. The
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existence of sexually antagonistic genes affects the evolution of mate preferences, as a
female must choose between maximizing the fitness of her sons or daughters.
There have been several recent theoretical examinations of the evolution of female
preferences under sex-linkage of the trait and/or preference7-10. However, all previous
models assume that sexually selected traits have male-limited expression and therefore
no fitness consequences when carried by females. Here we address the question of how
female preferences evolve for traits that have different fitness effects in each sex.
We present the results of two-locus models with either an X-linked trait or a Zlinked trait. Both models follow the fate of a newly arising preference allele p in a
population that is at a polymorphic equilibrium at a trait locus, with allele T most fit in
females and allele t most fit in males. In the X-linked model females with a tt genotype
suffer a fitness disadvantage of 1s relative to TT females, and the fitness of Tt females
is given by 1hs. Males carrying the T allele suffer a fitness disadvantage of 1z relative
to males with the t allele (Table 1). The fitness scheme in the Z-linked model is similar
(Table 1). The mating preference of a female of genotype i at the preference locus is
determined by ai, which describes the relative increase (or decrease) in the female’s
probability of mating with males carrying allele t (Table 1, after ref. 11). An additional
parameter, d, is required to describe the female preferences for heterozygous males
when the preference locus is Z-linked. When both trait and preference loci are sexlinked recombination occurs at a rate r between them; autosomal preference loci were
also considered. The analytical solutions for the polymorphic equilibria, and the
invasion of a new preference allele, p, are approximated assuming weak selection (s, z
and a are small).
There are three basic fates for sexually antagonistic genes: 1) the fixation of an
allele if, averaged over both sexes, it increases fitness, 2) the evolution of sex-specific
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expression, or 3) polymorphism4, 7. A polymorphic equilibrium for T can be maintained
by sexually antagonistic selection as long as the fitness of heterozygotes averaged
across the sexes is sufficiently high. In the X-linked model, the criteria for maintenance
of an equilibrium in a population fixed for the preference allele P is:
2hs < (aPP + z) < 2s(1-h).
(1)
For this interval to exist and be stable, the deleterious allele in females, t, must be
partially recessive (h < 1/2). A new preference allele, p, invades a population that is
polymorphic for an X-linked trait locus whenever aPp < aPP, whether the preference
locus is X-linked or autosomal. Consequently, a new preference allele invades only if it
confers a stronger preference for males bearing T: the trait allele that has the highest
fitness in females. Surprisingly, recombination between the trait and preference does not
alter the invasion conditions, although invasion is faster when r = 0. Recombination
places preference alleles on the same chromosome as the trait alleles that have been
preferred and is therefore critical to the development of genetic associations. However,
recombination also breaks apart genetic associations. These two factors balance and
cause the level of genetic associations to be fairly insensitive to the recombination rate.
The criteria for the maintenance of a polymorphic equilibrium in the Z-linked case
can be simplified by combining the overall fitness of males due to both natural and
sexual selection, and standardizing by the fitness of the most fit genotype (tt)
(supplementary material). Assuming weak selection, the fitness of TT males is now
given by 1-Z where Z = z + a, and the fitness of Tt males is given by 1-HZ, where H is
(hz +a – da)/(a+z). Z and H are equivalent to the selection coefficient s and the
dominance coefficient h in the X-linked case. Given these definitions for Z and H the
criteria for the maintenance of a polymorphic equilibrium at a Z-linked trait locus is:
2HZ < s < 2Z (1-H).
(2)
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The main difference from (1) is that only natural selection, s, acts on the
heterogametic females in (2), but both sexual selection, a, and natural selection, z, act
on the heterogametic males in (1). For a polymorphic equilibrium to exist and be stable,
the deleterious allele in males, T, must be partially recessive (H < 1/2). In contrast to the
X-linked case, p can invade a population monomorphic for P only when ap > aP if the
preference is Z-linked, or aPp > aPP if it is autosomal. Consequently, a new preference
allele can invade only if it confers a stronger preference for the trait allele, t, favoured in
sons. Again, recombination has a slight effect on the rate of invasion of p, but not the
condition under which invasion occurs.
The conditions for the invasion of a new preference were determined assuming
weak selection. How robust are these results to stronger selection? Simulations with
selection coefficients on the order of 10-30% were explored, and confirmed the
predictions of the model (Figure 1). Selection coefficients in this range are not
uncommon13. The simulations suggest that invasion depends more on how the new
preference allele changes female mating preferences than on the strength of selection.
Our results point to a potentially large effect of the sex determination mechanism
on how female preferences evolve for sexually antagonistic traits. Over the long term
course of evolution, as multiple preference alleles arise by mutation and are lost or
spread, the evolution of female preferences will eventually lead to the fixation of the
trait most fit in females, T, in XY systems and the trait most fit in males, t, in ZW
systems. This process can occur at once if the new allele has a strong enough effect on
preferences. Thus, sexually antagonistic selection becomes resolved in favour of
females in XY species (Fig. 1b), but in favour of males in ZW species (Fig. 2b). In
contrast, when both the trait and preference loci are autosomal, there is no longer any
selection for females to prefer traits that help only one sex. This is consistent with a
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previous model14, which found that sexual selection could resolve a T/t polymorphism
either in favour of T or t.
The resolution of sexual antagonism in favour of females in XY species when the
trait is X-linked is perhaps an explanation for the expression patterns of sex-biased
genes in Drosophila melanogaster. Many genes in D. melanogaster show sex-biased
expression, where the gene is expressed more in one sex than the other15. Genes that
have male-biased expression are significantly underrepresented on the X chromosome,
while gonad-specific female-biased genes occur on the X chromosome more often than
expected15. Our model predicts that the opposite should be true in ZW species, where
male-biased genes will be expected to accumulate on the Z chromosome.
Why exactly do opposite preferences evolve depending on the type of sexdetermination? When the trait is X-linked, our results demonstrate that female
preferences can evolve to increase the fitness of daughters at the expense of sons.
Intuitively this is because females who prefer certain XY males over others cannot
affect the fitness of her sons through her preference as her sons inherit only the Y
chromosome from their father. However, a female can improve the fitness of her
daughters through her preference because daughters inherit the X chromosome from
their father. In contrast, we have found that Z-linkage allows the evolution of
preferences that increase the fitness of sons. Now, a preference allele on the Z
chromosome is not passed on from a mother to her ZW daughters who inherit their Z
chromosome from their father, and thus does not benefit by improving the fitness of
daughters. By preferring males carrying the trait allele favourable to males, however, a
mother can improve the fitness of her ZZ sons, who also inherit their mother’s
preference allele. This difference in how female preferences are inherited and how they
evolve could explain why males in ZW species (e.g., birds and butterflies) have more
elaborate sexual displays than males in XY species. Our model predicts that female
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preferences can more easily evolve in ZW species for traits that benefit sons more than
daughters. Once these preferences have established within a species, they could cause
the further evolution of flashy male displays at loci throughout the genome11.
If sexually antagonistic traits (and genes) are as common in other organisms as
they are in Drosophila3, it is probable that they have strongly influenced the direction of
female preference evolution. Although few mutations will have sexually antagonistic
effects, those that do are more likely to remain polymorphic and make a substantial
contribution to the standing genetic variance in fitness. Therefore, the evolution of
female preferences may be driven more by traits expressed in both males and females
than has been previously appreciated.
1. Andersson, M. Sexual Selection (Princeton Univ. Press, Princeton, 1994).
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mating biases. Proc. Roy. Soc. Lond. B. 270, 653-664 (2003).
3. Gibson, J. R., Chippindale, A. K. & Rice, W. R. The X chromosome is a hot spot for
sexually antagonistic fitness variation. Proc. R. Soc. Lond. B. 269, 499-505 (2002).
4. Rice, W. R. & Chippindale, A. K. Intersexual ontogenetic conflict. J. Evol. Biol. 14,
685-693 (2001).
5. Forsman, A. Opposing fitness consequences of colour pattern in male and female
snakes. J. Evol. Biol. 8, 53-70 (1995).
6. Endler, J. A. Natural selection on color patterns in Poecilia reticulata. Evolution 34,
76-91 (1980).
7. Hastings, I. M. Manifestations of sexual selection may depend on the genetic basis of
sex determination. Proc. R. Soc. Lond. B. 258, 83-87 (1994).
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8. Keene, H. K. & Pfennig, D. W. Genetic biases for showy males: are some genetic
systems especially conducive to sexual selection? Proc. Natl. Acad. Sci. USA 100,
1089-1094 (2003).
9. Andrés, J. A. & Morrow, E. H. The origin of interlocus sexual conflict: is sex-linkage
important? J. Evol. Biol. 16, 219-223 (2003).
10. Kirkpatrick, M. & Hall, D. W. Sexual selection and sex linkage. Evolution 58, 683691 (2004).
11. Kirkpatrick, M. Sexual selection and the evolution of female choice. Evolution 36,
1-12 (1982).
12. Rice, W. R. Sex chromosomes and the evolution of sexual dimorphism. Evolution
38, 735-742 (1984).
13. Kingsolver, J. G. et al. The strength of phenotypic selection in natural populations.
Am. Nat. 157, 245-261 (2001).
14. Otto, S. P. On evolution under sexual and viability selection: a two-locus diploid
model. Evolution 45, 1443-1457 (1991).
15. Parisi, M. et al. Paucity of genes on the Drosophila X chromosome showing malebiased expression. Science 299, 697-700 (2003).
The authors are indebted to Tony Long, whose unpublished data inspired this model. We thank Tim
Vines and YOUR NAME HERE for comments and discussions. AYKA was supported by an NSERC
postgraduate scholarship (Canada) and SPO was supported by an NSERC discovery grant (Canada).
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Figure 1. Simulation results for the evolution of female preferences in male
heterogametic species (XY). All simulations were started under conditions
allowing a polymorphic equilibrium at an X-linked trait locus with P fixed, and
track the change in frequency of a newly introduced p allele. a) A new allele that
prefers males carrying the T allele sweeps to fixation leaving T polymorphic at a
higher frequency and improving the fitness of daughters. r = 0.5 for all
simulations. The frequency of T is in blue, and males are shown with a dashed
line. The frequency of p is in red (the frequencies in males and females were
not distinguishable). b) A preference allele favouring the T allele in an XY
species sweeps to high frequency, driving T to fixation. Sexual antagonism is
thus completely resolved in favour of females.
Figure 2. Simulation results for the evolution of female preferences in female
heterogametic species (ZW). a) A new allele that prefers males carrying the t
allele at a Z-linked trait locus sweeps to fixation, driving T to low frequency and
improving the fitness of sons. The colours are the same as in Figure 1. b) A
preference allele favouring the t allele in a ZW species sweeps to high
frequency, driving t to fixation. Sexual antagonism is thus completely resolved in
favour of males.
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Table 1. Male and female fitness components in (a) male heterogametic
(XY) and (b) female heterogametic (ZW) species.
(a) X-linked trait
(b) Z-linked trait
Male Trait
Female
Male Trait
T
t
PP
1
1+aPP
Pp
1
1+aPp
pp
1
1+app
1-z
1
preference:
Female
TT
Tt
tt
P
1
1+daP
1+aP
p
1
1+dap
1+ap
1-z
1-hz
1
preference:
Male
Male
viability:
viability:
Female Trait
Female
viability:
Female trait
TT
Tt
tt
1
1-hs
1-s
Female viability:
T
t
1
1-s
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Figure 1.
Figure 2.