Download Condition-dependent mutation rates and sexual selection

doi:10.1111/j.1420-9101.2008.01683.x
Condition-dependent mutation rates and sexual selection
S. COTTON
Research Department of Genetics, Evolution & Environment, University College London, London, UK
Keywords:
Abstract
condition;
good genes;
mutation rate;
ornament;
sexual selection.
‘Good genes’ models of sexual selection show that females can gain indirect
benefits for their offspring if male ornaments are condition-dependent signals
of genetic quality. Recurrent deleterious mutation is viewed as a major
contributor to variance in genetic quality, and previous theoretical treatments
of ‘good genes’ processes have assumed that the influx of new mutations is
constant. I propose that this assumption is too simplistic, and that mutation
rates vary in ways that are important for sexual selection. Recent data have
shown that individuals in poor condition can have higher mutation rates, and
I argue that if both male sexual ornaments and mutation rates are conditiondependent, then females can use male ornamentation to evaluate their mate’s
mutation rate. As most mutations are deleterious, females benefit from
choosing well-ornamented mates, as they are less likely to contribute
germline-derived mutations to offspring. I discuss some of the evolutionary
ramifications of condition-dependent mutation rates and sexual selection.
Introduction
Genetic models of sexual selection show that females can
gain indirect benefits in terms of ‘good genes’ for their
offspring if they show mating preference for ornaments
that signal male genetic quality (Iwasa et al., 1991; Iwasa
& Pomiankowski, 1994, 1999; Houle & Kondrashov,
2002). The more genetic variance that exists in male
quality, the more females gain from being choosy, as
mating with genetically high-quality males endows their
offspring with better than average genotypes. A variety of
mechanisms for generating genetic variation in male
quality have been suggested, including the continual loss
of genetic adaptation as a result of co-evolution with
parasites (Hamilton & Zuk, 1982) and recurrent deleterious mutation (Houle, 1991; Burt, 1995). The latter has
featured heavily in previous models. However, these
theoretical treatments have assumed that the influx of
new mutations is constant both across generations and
between individuals within the same generation (Iwasa
et al., 1991; Iwasa & Pomiankowski, 1994; Houle &
Kondrashov, 2002). Here, I suggest that this assumption
Correspondence: Samuel Cotton, Research Department of Genetics,
Evolution & Environment, University College London, Wolfson House,
4 Stephenson Way, London NW1 2HE, UK.
Tel.: +44 20 7679 5116; fax: +44 20 7679 5052;
e-mail: [email protected]
may be too simplistic and propose that mutation rates
may vary in ways that are important for sexual
selection.
Far from being static and inflexible, mutation rates
are highly variable and responsive to selection (Baer
et al., 2007). Although mutations arise in all cell types,
the most important mutational events for evolution are
those that occur in the germline, as these are inherited
by offspring. The majority of mutations are deleterious
to fitness; so, some opposing force must maintain the
mutation rate above zero. Selection can favour the
spread of mutator alleles that elevate mutation rates, as
a result of rare beneficial mutations that they create and
hitch-hike with (e.g. Sniegowski et al., 1997; Taddei
et al., 1997). However, this is likely to occur only in
asexual populations where there is no recombination to
unlink mutator alleles and beneficial mutations (Johnson, 1999). In sexual populations, recombination drastically reduces hitch-hiking of mutator alleles (Johnson,
1999) and the alternative, more pervasive, explanation
for a nonzero mutation rate is that of a physiological
constraint, as maintaining a low mutation rate is likely
to be costly (Sniegowski et al., 2000; Agrawal & Wang,
2008). Evolved mutation rates are therefore an optimal
balance between the costs of DNA fidelity and the
predominantly deleterious consequences of mutation
(Sniegowski et al., 2000).
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If the costs of mutational repair and DNA fidelity are
evolutionarily important, then mutation rates should be
sensitive to environmental and genetic stress, as the
degree of stress will influence the relative costs of DNA
replication fidelity and repair. In this respect, mutation
rates are similar to other genomic traits that are
condition-dependent, such as recombination (Parsons,
1988; Lucht et al., 2002). Transposition rates of selfish
genetic elements, and hence mutational events that
result from their incision, increase significantly in the
presence of external stressors (McClintock, 1984;
Grandbastien, 1998) and populations maintained under
environmental stress evolve higher mutation rates in
both prokaryotes (Bjedov et al., 2003) and eukaryotes
(Goho & Bell, 2000). Goho & Bell (2000) estimated that
mutation rates were 10- to 40-fold greater in Chlamydomonas populations maintained in mildly stressful environments compared with that in controls reared under
benign conditions. Recently, Agrawal & Wang (2008)
demonstrated that such patterns also exist at the level of
the individual by showing for the first time that DNA repair
is condition-dependent in a multicellular eukaryote.
In Drosophila melanogaster, maternal DNA repair mechanisms can repair damaged DNA in sperm after fertilization. Females were mated to mutagenized males and
the daughters were screened for recessive lethals on the
paternally inherited X chromosome. Females maintained on a low-quality diet transmitted significantly
more (!30%) sex-linked recessive lethals to their
offspring than did females reared on a high-quality diet
(Agrawal & Wang, 2008). Together, these results support the hypothesis that individuals in poor condition
(as a result of detrimental internal or external factors)
have higher mutation rates, through either increased
incidences of DNA damage and ⁄ or reduced ability to
repair such damage.
If mutation rates scale negatively with individual
quality, then they are expected to covary with other
condition-dependent traits. There is a large body of
evidence demonstrating that male sexual ornaments are
expressed in a condition-dependent fashion, with the
highest quality individuals in the best condition displaying the largest and most extravagant ornaments
(Andersson, 1994; Johnstone, 1995; Cotton et al.,
2004a). For example, in stalk-eyed flies the male ornament (elongated eye-stalks) becomes proportionately
smaller as phenotypic condition is reduced by nutritional
stress (David et al., 1998; Cotton et al., 2004b), dessication and heat shock (Bjorksten et al., 2001). Similarly,
plumage ornaments are condition dependent in many
avian species, becoming less gaudy or elaborate as the
bearer’s phenotypic quality declines (e.g. Hill, 2000), and
the frequency and complexity of many bird and
orthopteran songs are reduced when individuals are
stressed (e.g. Scheuber et al., 2003; Spencer et al., 2003).
Sexual ornaments also reflect variation in genetic quality. For instance, male carotenoid colouration and sexual
displays exhibit marked inbreeding depression in guppies
(Sheridan & Pomiankowski, 1997; Van Oosterhout et al.,
2003), consistent with being sensitive to deleterious
mutation loads.
Here, I propose, with the aid of a simple simulation,
that, if both male sexual ornaments and mutation rates
are condition-dependent, then the degree of ornament
exaggeration will be revealing of the mutation rate of
the bearer. Females may therefore be able to exploit
male ornamentation to evaluate their mate’s germline
mutation rate. As most mutations are deleterious,
females will benefit indirectly from choosing wellornamented males as mates because they are less likely
to contribute germline-derived mutations to offspring.
So, in conjunction with additional genetic benefits of
mate choice that result from pre-existing standing
genetic variance in male quality (Iwasa et al., 1991;
Iwasa & Pomiankowski, 1994, 1999; Houle & Kondrashov, 2002), condition-dependent mutation rates may
elevate the overall level of heritable quality variation in
males and lead to stronger selection on both male
ornaments and female mate preferences.
The model
To demonstrate the potential for variation in phenotypic
condition to create variation in the germline mutation
rate, I use a simple simulation in which I follow
Blumenstiel’s (2007) proposal that germline mutation
rates are sensitive to investment into, and efficiency of,
DNA replication and repair, such that
! "1=k
E
li ¼
;
ð1Þ
Ii
where li is the mean genome-wide deleterious mutation
rate per haploid gamete in individual i. Under this model,
the cost of maintaining l close to zero becomes prohibitively high and approaches infinity (Sniegowski et al.,
2000). Ii reflects the investment by individual i into
maintaining DNA fidelity. E and k are linear and
exponential scaling parameters, respectively, that determine the cost of maintaining a particular mutation rate
for individual i. As E (and ⁄ or k) increase(s) in magnitude,
the greater is the cost of maintaining a given mutation
rate. E (and ⁄ or k) can also be viewed as parameter(s)
describing the efficiency of DNA replication fidelity and
repair. The consequences of variation in Ii and E on li are
shown in Fig. 1.
If mutation rates are condition-dependent, then I is
expected to increase in proportion with individual
condition. Let us assume that Ii increases in an exponential fashion with condition, Ci,
Ii ¼ ðImax % Imin ÞCia ;
ð2Þ
where Imax and Imin are the maximum and minimum
levels of investment into mutation repair, respectively,
and a is the scaling exponent. When a = 1, investment
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0.5
0.1
0.05
sire’s genetic quality through its ability to provide a
female with mutation-free gametes. If mutations are rare,
distributed randomly across gametes and not subject to
haploid selection, then the probability of syngamy and
fertilization involving a mutation-free gamete from
individual i (P[0]i) can be given by the first term in the
Poisson series,
0.01
0.005
0.001
P½0(i ¼
Fig. 1 The consequences of variation in investment in DNA replication fidelity (Ii) across different values of E on the mean genomewide deleterious mutation rate per haploid gamete in individual
i (li), as expected if li ¼ ðE=Ii Þ1=k ; k = 1.0.
into DNA repair and replication fidelity increases linearly
with condition, whereas when a > 1or a < 1, the rate of
investment increases or decreases, respectively, with
condition.
To investigate the effect of condition-dependent mutation rates on any genetic benefits of mate choice, I use a
series of simple simulations. Males were assigned a
condition value (Ci) drawn at random from a normal
distribution and standardized within the range
0.01 £ Ci £ 1. A male i also possesses a sexual ornament,
whose size (Si) is determined by a condition-dependent
exaggeration away from a natural selection optimum
trait value (t),
Si ¼ ðt þ t 0 Ci Þ þ e;
ð3Þ
where t ¢ is the degree of condition dependence and e is a
normally distributed error with a mean of zero and a
standard deviation of 1. Biologically, ! reflects sexual
signalling inefficiency either through imperfect signalling
of condition by ornaments or through perceptual errors
made by females in their assessment of male ornaments.
Females in the population exhibit an open-ended psychophysical mate preference function (Lande, 1981); the
probability of a male i being chosen as a mate (Pmate,i) is
contingent on its ornamental phenotype and the strength
of female preference (y),
eySi
Pmate;i ¼ Pn yS
i
i¼1 e
901
ð4Þ
where n is the number of males (here arbitrarily
n = 100). Females mate at random when y = 0 and show
stronger mating preferences for males with large ornaments when y increases above zero.
I consider offspring fitness to be a function of the
number of deleterious mutations, with mutation-free
zygotes having the highest potential fitness. In order to
keep the model as general as possible, I ignore the fitness
effects of mutated gametes and instead define a potential
1
:
eli
ð5Þ
The greatest genetic benefits will be obtained by mating
with males bearing the highest values of P[0]i. This
definition of P[0]i only represents a male’s true genetic
quality if all new mutations are dominant lethals.
Nonetheless, given that P[0]i scales negatively with
overall gametic mutation load, then it is likely to be a
useful proxy of a male’s gametic quality under more
relaxed assumptions about mutation selection coefficients and dominance. Note that P[0]i is also a conservative index of male genetic quality, precisely because it
does not account for the (magnitude of the) deleterious
fitness consequences of gametes containing one or
multiple mutations, which are increasingly likely in
individuals with higher l. The probability (P[0]mating) of
a female receiving a mutation-free sperm from a mating,
given its preference function is,
P½0(mating ¼
n
X
i¼1
ðPmate;i P½0(i Þ:
ð6Þ
Females with the highest P[0]mating values produce
offspring with the fewest deleterious mutations.
To explore whether sexual selection can favour males
that produce the fewest mutations, I compared the
populations with no sexual selection [random mating
(y = 0) and no condition-dependent ornaments (t¢ = 0)],
with those in which females preferred well-ornamented
males (e.g. y = 0.5) and ornaments were revealing of
male condition (e.g. t¢ = 5). To explore variation in the
form of condition dependence of mutation rates I ran
simulations under different scaling exponents that
reflected an increasing, unchanging and decreasing rate
of investment into mutational repair processes with
increasing condition (a = 0.5, 1 and 2 respectively).
Similarly, simulations were repeated over two values of
E that reflected weakly and strongly declining mutation
rates with increasing investment (E = 0.05 and 0.005
respectively). Each set of simulations was repeated 10
times and P[0]mating values from the different mating
regimes were compared using Wilcoxon tests.
Results
If both male sexual ornaments and mutation rates are
condition-dependent, then we observe that high-quality
males with large ornaments have the lowest mutation
rates and the greatest probability of delivering mutationfree gametes to females (Fig. 2a). Poor quality males have
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high mutation rates, small ornaments and produce fewer
mutation-free sperm. By contrast, if male sexual traits are
not condition-dependent (t¢ = 0), then ornament size
does not reveal the underlying mutation rate and thus
cannot be used to predict the probability of receiving
mutation-free gametes (Fig. 2b).
Relative to random-mating females, females that
preferred well-ornamented males gained significant
genetic benefits in terms of their offspring acquiring
fewer mutations (higher P[0]mating values; Fig. 3).
Although the benefits of sexual selection were small –
but nonetheless significant – when investment into
mutational repair increased with condition at a
diminishing rate (e.g. when a = 0.5) and ⁄ or when
mutation rates declined strongly with increasing
investment (e.g. E = 0.005; Fig. 3b), they became quite
large when investment into mutational repair increased
with condition at an unchanging or increasing rate (e.g.
when a ‡ 1; Fig. 3a). These results arose primarily
because females showing preference avoid mating with
the few very low quality males with very high mutation
rates.
Fig. 2 Sample simulations showing (a) condition-dependent ornaments (t¢ = 5, upper panel) can reveal condition-dependent mutation
rates (li, central panel) and can be used to predict the probability of receiving a mutation-free gamete during a mating (P[0]i, lower panel).
Removing the condition dependence of ornaments (b; t¢ = 0, upper panel) eliminates their utility as signals of mutation rate (central panel) and
hence P[0]i (lower panel). Additional parameter values: E = 0.05, k = 1.0, Imax = 1.0, Imin = 0.001, a = 1.0, t = 4, n = 100.
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(a)
(b)
Fig. 3 The probability of a female receiving male gametes with no
mutations (P[0]mating) under random mating (open bars; y = 0) and
sexual selection via female mating preference for well-ornamented
males (shaded bars; y = 0.5), when the decline in mutation rate
with increasing investment was weak (a; E = 0.05) or strong (b;
E = 0.005). Results are given for three values of a, the exponent
relating investment to mutational repair with condition. Bars
represent median values (±interquartile ranges) from 10 simulations. Asterisks denote the significance of Wilcoxon tests;
***P < 0.001, **P < 0.01, *P < 0.05. Additional parameter values:
k = 1.0, Imax = 1.0, Imin = 0.001, t = 4, n = 100.
Discussion
Previous genetic models demonstrating that the handicap
principle can work have assumed that the rate of influx
of new mutations is constant (e.g. Iwasa et al., 1991;
Iwasa & Pomiankowski, 1994; Houle & Kondrashov,
2002). Here I suggest, with reference to recent experimental evidence, that this assumption is too simplistic
and propose an additional factor favouring sexual selection. Mutation rates are highly variable (Baer et al., 2007)
and variation in individual condition has been shown to
explain significant levels of intraspecific variation in
mutation rates, with poor quality individuals having
higher mutation rates than individuals in good phenotypic condition (Agrawal & Wang, 2008). Male sexual
ornaments also covary with phenotypic condition in
most systems studied (Andersson, 1994; Johnstone,
1995; Cotton et al., 2004a). The common reliance of
903
these two traits (mutation rates and ornamentation) on
condition means that a male’s sexual trait size may be
revealing of its propensity for generating new mutations.
If mutations are predominantly deleterious and occur
with increasing frequency in low condition individuals,
then in addition to signalling any pre-existing genetic
variance in quality, ornaments will also reflect the risk of
endowing the offspring with recently acquired mutations.
Given the relative infancy of investigations into condition-dependent mutation rates, it is currently
unknown how widespread the phenomenon is, but the
available evidence is from diverse taxa suggesting that it
could be near ubiquitous (Goho & Bell, 2000; Agrawal &
Wang, 2008). Likewise, it is not clear what proportion of
intraspecific variance in mutation rates is explained by
condition, although Agrawal & Wang (2008) report that
a 30% increase in mutation in low condition individuals
is accompanied by a 30% reduction in female fecundity,
suggesting that the proportion may be quite high. It is
also difficult to make specific predictions or conclusions,
as most parameters in my simulations are unknown for
real biological systems. However, a few general remarks
can be made. The form of the relationships between:
(i) investment into DNA repair and condition and
(ii) investment and realized mutation rate, have large
effects on the degree of potential benefits to be gained by
females. The benefits are the greatest when the rate of
investment into DNA repair increases with condition and
when mutation rates decline more slowly with increasing
investment. As with previous ‘good genes’ models (Iwasa
et al., 1991; Iwasa & Pomiankowski, 1994), the reliability
of signalling of such genetic benefits is the greatest when
the degree of ornament condition dependence is high.
I used a simplified measure of gamete quality, P[0]i, the
probability of syngamy and fertilization involving a
mutation-free gamete. However, if mutations are rare
and occur at random in the genome, then the probability
of receiving a heavily mutated gamete will be proportionately greater for poorly ornamented, low-quality
mates with a higher mean genome-wide deleterious
mutation rates. Even if loci act independently, offspring
fitness (xm) is expected to decline rapidly with increasing
numbers of mutations (m) because xm ¼ ð1 % sÞm
(Agrawal, 2002). So P[0]i is also likely to be a highly
conservative index of gamete quality. Interaction among
alleles and loci will also have large influences on
offspring fitness. For example, synergistic epistasis will
lead to greater than additive reductions in offspring
fitness if multiple mutations occur in the same gamete, as
is more likely in individuals with higher average mutation rates. So, condition dependence of mutation rates, in
conjunction with additive and nonadditive allelic and
locus effects, may generate more genetic variance in
quality than previously thought.
Condition-dependent mutation may also contribute to
solving the paradox of the lek (Borgia, 1979; Taylor &
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Williams, 1982). Theory predicts that directional selection will deplete genetic variation in fitness, as favoured
alleles quickly spread to fixation (Maynard Smith, 1978;
Charlesworth, 1987), and indirect selection on female
preference as a result of ‘good genes’ is predicted to be
rather low (!3.5%; Kirkpatrick & Barton, 1997). So why
do females, which receive only genes during mating,
continue to discriminate between males if there are so few
genetic benefits of choice (Borgia, 1979; Taylor & Williams,
1982; Kirkpatrick & Ryan, 1991)? The dominant
resolution to this paradox has been the hypothesis that,
although the loss of adaptation per locus (for example,
through recurrent deleterious mutation) is low, many
genes underlie the condition so that the total amount
of genetic variance introduced into the population across
all loci is sufficient to drive ‘good genes’ sexual
selection (Pomiankowski & Møller, 1995; Rowe & Houle,
1996). Under the assumptions that surround eqn (1),
condition-dependent mutation results in poor quality
individuals harbouring proportionately more mutations
in their germline (Fig. 1). This (nonlinear) covariation in
the influx of new mutations with condition elevates the
overall level of genetic variance in offspring quality, and
may therefore provide a stronger basis for ‘good genes’
sexual selection.
Handicap theory requires that ornaments are costly, as
this maintains signal honesty (Grafen, 1990; Iwasa et al.,
1991; Iwasa & Pomiankowski, 1994, 1999). However,
the cost of having a large ornament may impinge on
viability so that well-ornamented individuals have lower
phenotypic condition than those with small ornaments,
despite having overall higher fitness (sensu Kokko,
2001). Under such circumstances well-ornamented
males might be expected to have higher germline
mutation rates than those with smaller ornaments, and
thus females may weaken their preference for wellornamented males if they provide a higher complement
of mutated gametes. Although some studies suggest that
well-ornamented males may have lower phenotypic
condition, the majority have shown that individuals in
good phenotypic condition have the largest ornaments
(reviewed in Andersson, 1994; Johnstone, 1995; Jennions et al., 2001; Cotton et al., 2004a) suggesting that
the positive relationship assumed in this paper is
common in nature.
The signalling of condition-dependent mutation rates
by male ornaments is a unique hypothesis because,
whereas previous theory has suggested that ornaments
reflect genotype quality of the bearer, the one presented
in this paper suggests that ornaments may signal the
genotypic quality of offspring. ‘Good genes’ models of
sexual selection traditionally require that there is a
genetic basis to condition-dependent ornament expression (Pomiankowski & Møller, 1995; Rowe & Houle,
1996; Cotton et al., 2004a; Hunt et al., 2004; Tomkins
et al., 2004); the absence of genetic variance in the trait is
usually taken to mean that ‘good genes’ effects are not
important. However, if mutation rates are phenotypically
condition-dependent (Agrawal & Wang, 2008), then
females will still obtain genetic benefits for their offspring
even if ornament expression does not have a genetic
basis (i.e. when their expression is contingent only on
phenotypic rather than genetic quality variation). So,
‘good genes’ sexual selection may be more cryptic than
previously thought. Moreover, although conditiondependent mutations may influence ‘good genes’ to the
extent that they are inherited by progeny, they may also
lead to reduced sperm viability and ⁄ or fertilization ability
leading to direct fitness consequences. So, a low sperm
mutation load can also be classified as a direct benefit to
the female as it improves the likelihood of successful
fertilization, an important consideration if females are
sperm limited (Sheldon, 1994; Arnqvist & Nilsson, 2000;
Wedell et al., 2002). The traditional distinction between
direct (material) and indirect (genetic) benefits of mate
choice may therefore be rather more blurred than
previously thought.
Throughout this paper, I have concentrated on
germline mutation rates, as these are the most important for evolution and ‘good genes’ sexual selection.
However, condition-dependent mutations will also
occur at a higher frequency in the soma of poor quality
individuals. Although themselves being evolutionary
‘dead-ends’, mutations in the soma may still play an
important role in sexual selection if they affect the
fitness of their bearer, an extreme example being the
heightened progression of cancers associated with elevated somatic mutation rates (Frank & Nowak, 2004). If
somatic mutations reduce male health and vigour then
such individuals will have lower condition and hence
lower attractiveness, as a result of condition-dependent
ornamentation. Moreover, an increased somatic mutation load may inhibit the performance of poor quality
males still further, rendering them less able to provide
females with resources, such as parental care, providing
an additional advantage to females preferring wellornamented males.
Condition- or fitness-dependent mutation rates have
been suggested to increase the twofold cost of sex, with
sexual populations having a greater number of mutations at equilibrium (Agrawal, 2002). In asexual populations, equilibrium mean fitness is contingent only
on the mutation rate of the least mutationally loaded
class, and as these individuals are of high fitness they
also have low mutation rates. Hence, asexuals are
expected to have higher equilibrium fitness than sexual
populations (Agrawal, 2002). However, if conditiondependent male ornamentation, or male mating success, reflects male mutation rates, then sexual selection
will result in preferred males transmitting the fewest
mutations to their offspring, thereby lowering the
mutational load. So, it seems plausible that any
disadvantages to sex that arise from condition-dependent mutation rates may be overcome by sexual
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selection, in much the same way that Agrawal (2001)
and Siller (2001) argued that the twofold cost of sex
can be overcome by sexual selection purging existing
mutations in the (male) population.
Some similarities may be drawn between the current
hypothesis and that of female preference based on agedependent male germline mutation (e.g. Radwan, 2003).
Germline mutation rates are expected to increase with
male age as a result of the higher number of sperm cell
divisions (Ellegren, 2007); so, females should decrease
the mutation load of their progeny by avoiding matings
with older males. Current tests of this hypothesis are
equivocal, suggesting that female choice for low (agedependent) germline mutation loads is weak (Radwan,
2003 and references therein). However, considerable
variation in condition is likely to exist within and
between male age classes and thus condition-dependent
mutation variation may obscure any age-dependent
mutation effects in natural populations. For example,
older males are often in a better condition as a result of
viability selection (Kokko, 1998) and negative correlations between age and condition will have contrasting
consequences on mutation rates, rendering age or condition, in isolation, as poor indicators of germline
mutation load. Studies of condition- and age-dependent
mutation rates are in their infancy; so, future work
should attempt to determine the relative importance of
these two forces.
Finally, condition-dependent DNA repair processes
may also contribute towards the elevated male-biased
mutation rates observed in sexually selected species
(Bartosch-Härlid et al., 2003; Ellegren, 2007). Such
biases are thought to arise because the greater number
of cell divisions in the male germline increases the
likelihood of DNA replication errors occurring during the
production of sperm, relative to ova (Ellegren, 2007;
Hedrick, 2007). Male-biased mutation rates tend to be
higher in sexually selected species, as sperm competition
increases the production of sperm, and therefore the
propensity for mutation (Bartosch-Härlid et al., 2003;
Blumenstiel, 2007; Ellegren, 2007). However, similar
patterns may arise in species with sexual ornaments.
Although an evolutionary relationship between ornaments and overall mutation rates has been proposed
before (Petrie & Roberts, 2006; but see Cotton &
Pomiankowski, 2007), I suggest that condition dependence of DNA repair will lead to an association between
ornaments and the degree of male bias in mutation rate.
Ornaments are costly (Kotiaho, 2001) and hence are
likely to reduce condition in males relative to females,
which lack such costly structures ⁄ displays. If this were
so, then we would expect males, on average, to suffer
higher mutation rates than females, leading to maledriven evolution. Relationships between ornaments and
male-biased mutation rates have yet to be studied
empirically; so, future work would profit from addressing this expectation.
905
Acknowledgments
This work was supported by a NERC (UK) Fellowship.
The author thanks K. Fowler and A. Pomiankowski for
useful discussion and two anonymous reviewers for
constructive comments on a previous version of the
manuscript.
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Received 24 September 2008; revised 18 November 2008; accepted 25
November 2008
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JOURNAL COMPILATION ª 2009 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY