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The dynamic relationship between
polyandry and selfish genetic elements
Nina Wedell
Biosciences, University of Exeter, Cornwall Campus, Penryn, Cornwall TR10 9EZ, UK
rstb.royalsocietypublishing.org
Review
Cite this article: Wedell N. 2013 The dynamic
relationship between polyandry and selfish
genetic elements. Phil Trans R Soc B 368:
20120049.
http://dx.doi.org/10.1098/rstb.2012.0049
One contribution of 14 to a Theme Issue
‘The polyandry revolution’.
Subject Areas:
behaviour, evolution, ecology,
microbiology, genetics
Selfish genetic elements (SGEs) are ubiquitous in eukaryotes and bacteria,
and make up a large part of the genome. They frequently target sperm to
increase their transmission success, but these manipulations are often associated with reduced male fertility. Low fertility of SGE-carrying males is
suggested to promote polyandry as a female strategy to bias paternity
against male carriers. Support for this hypothesis is found in several taxa,
where SGE-carrying males have reduced sperm competitive ability. In
contrast, when SGEs give rise to reproductive incompatibilities between
SGE-carrying males and females, polyandry is not necessarily favoured,
irrespective of the detrimental impact on male fertility. This is due to the
frequency-dependent nature of these incompatibilities, because they will
decrease in the population as the frequency of SGEs increases. However,
reduced fertility of SGE-carrying males can prevent the successful population invasion of SGEs. In addition, SGEs can directly influence male and
female mating behaviour, mating rates and reproductive traits (e.g. female
reproductive tract length and male sperm). This reveals a potent and
dynamic interaction between SGEs and polyandry highlighting the potential
to generate sexual selection and conflict, but also indicates that polyandry can
promote harmony within the genome by undermining the spread of SGEs.
1. Introduction
Keywords:
sperm competition, sexual conflict, Wolbachia,
sex-ratio distorter
Author for correspondence:
Nina Wedell
e-mail: [email protected]
The number of times a female mates during her lifetime is highly variable both
between- and within species. With the use of molecular techniques, we now
know that monogamy is the exception rather than the rule, with females of
most species mating with more than one male in their lifetime—polyandry
[1,2]. Mating can be costly in terms of time and energy expenditure [3], physical
damage [4], receipt of seminal proteins [5] and exposure to sexually transmitted
infections [6]. Multiple mating, therefore, has to confer benefits to outweigh
these costs. Females may derive direct benefits such as paternal care [7], nutrient provisioning [8], sperm replenishment [9,10] and strengthened social
cohesion [11] by mating multiply. In addition, they may gain genetic benefits
such as increased offspring diversity [12], viability [13] and attractiveness of
sons [14]. A recent meta-analysis indicated there is only weak evidence for
the genetic benefits of polyandry, largely due to insufficient data from welldesigned studies [15]. Females may also mate multiply to acquire compatible
genotypes [16,17]. Genetic compatibility is affected by male and female relatedness [18,19], and selfish genetic elements (SGEs) [20,21]. Incompatibility
stemming from relatedness is due to the exposure of deleterious recessive alleles
[22]. SGEs are a frequent source of intra-genomic conflict that can cause reproductive incompatibilities between male and female genomes [23]. It has also
been suggested that females may mate multiply to reduce the cost of male harassment. Such female harm minimization is predicted to be widespread owing
to the potential conflict between the sexes over female mating rate [24], or as a
means to obscure paternity to reduce the risk of male infanticide [25]. It is likely
that more than one benefit can be obtained by polyandry to individual females.
The frequency at which females remate is of key importance to many areas
in ecology and evolution. The frequency of polyandry can affect the level of
gene flow and effective population size [26], and, therefore, population viability
[27,28]. Polyandry also determines the level of post-copulatory sexual selection
& 2013 The Author(s) Published by the Royal Society. All rights reserved.
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also regulate the frequency of SGEs. Here, I explore the
evidence for this.
2. Selfish genetic elements and sexual selection
Phil Trans R Soc B 368: 20120049
Because SGEs are associated with a variety of costs such as
reduced fertility and production of the more common sex
in the case of sex-ratio distorters, non-carrying individuals
are expected to avoid mating with SGE-carrying mates.
There is evidence that both males and females discriminate
against SGE-carriers prior to mating in some species. For
example, in populations of stalk-eyed flies that harbour a
sex-ratio distorter, females prefer to mate with males with
long eye-stalks, as this is an indicator of a genetic suppressor
of drive ensuring females will produce both sons and daughters [46]. Similarly, some populations of house mice carry
a recessive lethal autosomal driving chromosome, the
t-complex [47]. Heterozygous individuals prefer to mate
with homozygous wild-types, and avoid other heterozygote
individuals using odour cues [47]. A recent fascinating
example comes from Drosophila paulistorum flies, where it is
demonstrated that both males and females show assortative
mating based on the strain of the endosymbiont (Wolbachia)
they carry [48]. This is favoured as crosses between males
and females carrying different strains of Wolbachia result in
reproductive incompatibilities and embryo death (cytoplasmic incompatibility—(CI)). It is as yet not clear what
the mechanism is that promotes Wolbachia-assortative mate
preferences in this fly species complex, although it is possible
the different strains of Wolbachia may be reflected in different
cuticular hydrocarbons potentially used in mate choice.
In other Drosophila species, there is evidence that different
diets cause differences in the commensal gut microbiota
that can directly affect mate preferences by changing the cuticular hydrocarbon sex pheromones [49,50]. Females of the
two-spotted spider Tetranychus urticae also show assortative
mating and oviposition preferences with respect to CIinducing Wolbachia; uninfected females prefer uninfected
males, whereas infected females aggregate their offspring,
thereby promoting mating with their infected sibs [51]. In
the isopod, Armadillidium vulgare harbouring feminizing
Wolbachia, males prefer real females to feminized males [52].
It is possible that feminized (i.e. genotypic) males lack the ability to produce female sexual pheromones and, therefore,
appear less ‘attractive’, and hence mate discrimination is not
due to the presence of Wolbachia itself. There is also evidence
that males may modify their mate preferences in response to
SGEs. For example, in Gammarus duebeni shrimp populations
infected by feminizing microsporidia, males prefer to mate
with real females and provide them with more sperm. This is
advantageous as feminized males are less fecund, and males
are severely sperm limited [53]. However, Wolbachia-based
mate preferences are not present in Drosophila melanogaster
or Drosophila simulans flies, indicating that this is far from a
universal pattern [54] (but see [55]).
There is also evidence of ‘maladaptive’ mate choice based
on SGEs. In Xiphophorus cortezi molly populations carrying a
cancerous melanoma, females prefer to mate with cancerous
males [56]. These males have a spotted caudal melanin pattern (Sc), which is associated with the Xmrk oncogene
(melanoma receptor kinase), that has been maintained for
several million years. High expression of Xmrk leads to the
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and sexual conflict, giving rise to a range of adaptations
and counter-adaptations involving reproductive manipulation
[29,30]. In addition to sexual conflict, female remating
frequency determines the within family relatedness, thus
affecting the intensity of parent–offspring conflict [31] and
the potential evolution of cooperation and sociality [32,33].
While inhibiting cooperation at the family level, recent studies
also indicate that polyandry can promote harmony within the
genome, through undermining the spread of SGEs that distort
transmission ratios [34]. It is not clear to what extent polyandry
is generally favoured as a strategy by females to reduce the
risks and costs associated with SGEs, although it is suggested
to favour evolution of female multiple mating [20]. To date,
there have been remarkably few experimental examinations
of this possibility.
The existence of genetic incompatibility is predicted to
favour polyandry as a female strategy to reduce the risk of fertilizing their eggs with sperm from genetically incompatible
males [23]. The idea initially put forward is that by mating more than once, females will reduce the risk of only
mating to males who carry incompatible genes. However,
this bet-hedging strategy only works under very restricted
circumstances [35]. Potentially of wider importance is that,
whenever females mate multiply, sperm from different
males will compete for fertilization of the female’s ova [36].
If females mate several times, they may potentially swamp
the sperm of incompatible males with that of genetically
superior males. Of particular importance in this context is the
finding that males that carry SGEs frequently have reduced fertility [37,38] and, therefore, often poor sperm competitive
ability [39,40].
SGEs are genes that are present in the genome or cell of an
organism that ensure they are passed on at a higher frequency
than the rest of the genome to subsequent generations. This
‘selfish’ nature of SGEs ensures they will accumulate within
the genome [41]. However, the subversion of the normal pattern of inheritance by SGEs generates a conflict with the rest
of the genome [41,42]. SGEs are ubiquitous in living organisms,
can make up a large proportion of the genome [42,43], and the
intra-genomic conflicts they create are thought to have had
major impacts on the evolution of sex and reproductive systems [41–44]. For example, the scarcity of males caused by
sex-ratio distorting SGEs can have dramatic effects on mating
systems [43]. There is strong selection for suppression of
SGEs to ensure a more equitable inheritance and to restore
the sex ratio to unity. Such genetic suppression of SGEs can
have far reaching impacts. For example, it is suggested that
methylation arose to silence SGEs, and was key to the evolution
of genomic imprinting and the placenta in mammals [45].
There is also evidence that SGEs can directly affect sexual selection. Many SGEs, including meiotic drive elements, B
chromosomes, endosymbionts and some transposons, target
male gametes in order to increase their transmission rate, and
have been shown to impair male fertility through manipulation
of spermatogenesis. This often also reduces the success of male
carriers in sperm competition [37]. Polyandry is, therefore,
hypothesized to decrease the frequency of any SGEs that
reduce the sperm competitive ability of males [34] by undermining their transmission advantage [20]. Hence, there is a
dynamic link between the presence of SGEs and mating systems, with female multiple mating that promote sperm
competition being favoured when they are at risk of mating
with SGE-carrying males, and conversely that polyandry can
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Is there any evidence that the presence of SGEs favours polyandry? In D. simulans carrying the Riverside strain of
Wolbachia (wRi), crosses between uninfected females and
infected males result in greater than 90 per cent hatching failure owing to CI. This enhances the transmission of Wolbachia
as all other crosses involving infected individuals are fertile
and result in Wolbachia-infected offspring. Uninfected females
do not discriminate against infected males as mates [54].
However, infected males are poor sperm competitors relative
to uninfected males [39]. Uninfected females mating multiply
with at least one uninfected male are able to recuperate their
total offspring
3
uninfected
infected
infected
infected
uninfected
uninfected
total offspring
(b) 140
120
100
80
60
40
40
0
II
UI
IU
infected
UU
II
UI
IU
uninfected
UU
Figure 1. The mean + s.e. offspring production of (a) monandrous females
and (b) polyandrous Drosophila simulans females. Dark grey bars indicate
crosses where all males are incompatible with females. Light grey bars
indicate crosses where one of two males is incompatible. White bars indicate
entirely compatible crosses. Female infection status is described in the lower
divisions of the x-axes. Male infection status is given in the higher divisions of
the x-axes. In (b), male infection status and order of mating is described as
follows: I, infected male; U, uninfected male. The first letter indicates the
infection status of the first male to mate and the second letter the infection
status of the second male. Adapted from Champion de Crespigny et al. [64]
fitness loss caused by CI owing to the poor sperm performance of infected males, and have the same reproductive
output as infected females (figure 1a,b). As a consequence,
polyandry should be favoured by uninfected females. There
is some evidence this is indeed the case. Uninfected females
(that are at risk of reproductive incompatibilities) remate
sooner than infected females [64]. However, despite the
poor sperm competitive ability of infected males, this benefit
cannot promote polyandry in itself. The reason is the relatively low probability of uninfected females mating with
both an infected and uninfected male, which will become
increasing less likely as the frequency of Wolbachia increases
and most individuals are infected (see §4).
The situation is different when the benefit of polyandry is
not dependent on the frequency of male and female genotypes (e.g. uninfected females and infected males), but
solely linked to the magnitude of the fertility reduction of
male carriers. In Hypolimnas bolina butterflies for example,
many South Pacific populations harbour a male-killing
strain of Wolbachia [65]. Intriguingly, different populations
have different frequency of male killers that is associated
with differences in degree of female-biased sex ratio, with a
higher frequency of male killers associated with a more
severely female-biased population sex ratio [66]. As a consequence, the mating system differs in relation to the
frequency of male killers. In high prevalence populations,
males provide smaller sperm packets than in low prevalence
populations, which is likely due to their higher mating
frequency in these high prevalence populations as a consequence of the pronounced female sex-ratio bias (figure 2a).
This in turn promotes female multiple mating, likely due to
the increased severity of sperm limitation experienced in
high prevalence populations (figure 2b). This creates a cycle
Phil Trans R Soc B 368: 20120049
3. Do selfish genetic elements
promote polyandry?
(a) 80
70
60
50
40
30
20
10
0
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development of a large black spot on the fish’s side—a cancer
that destroys muscle, reduces swimming speed and causes
early death—but is also associated with bigger size and
increased aggressiveness. Females prefer black, cancerous
and bigger males. Frequency-dependent selection maintains
this gene as individuals with two copies of Xmrk have reduced
viability. However, the majority of cases examining the
potential for SGE-based mate choice have failed to find any
conclusive evidence, despite severe fitness consequences of
not discriminating against SGE-carrying individuals [54,57].
The reason for the general lack of avoidance of SGE-carriers
may be the problem of recombination breaking up any association between an ornament and the SGE, and a potential
preference allele allowing for SGE-based mate choice to
evolve [58]. Support for this suggestion is that the only
known examples that are not associated with either behavioural or pheromonal differences of SGE-carriers do indeed show
reduced recombination. There is little recombination between
the driving and non-driving X-chromosome in stalk-eye flies
[59]. The t-complex in mice is contained within a large inversion system that also contains the major histocompatibility
complex and odour preference gene(s) [60]. In the swordtail
mollies, it is suggested a pre-existing sensory bias in females
is responsible for the preference of black cancerous males, as
preference for dark males is present in populations without
the oncogene, in combination with black males being more
visible [56].
The limited evidence for the importance of SGEs in promoting pre-copulatory mate choice suggests that postcopulatory effects may be more important, thereby favouring
polyandry. Many SGEs target male spermatogenesis in order
to get transmitted to the next generation. This can be
achieved by modifying sperm during development (e.g.
Wolbachia [61,62]). Other SGEs destroy sperm that do not
pass on the selfish gene to subsequent generations by killing
non-carrying sperm during spermatogenesis (e.g. meiotic
drive [63]). However, the method of sperm killing can also
have a detrimental side effect on the surviving carrier
sperm that will compromise sperm performance (e.g.
sex-ratio drive [40]). As a consequence of such sperm
manipulation to enhance transmission of SGEs, male carriers
frequently suffer reduced fertility and sperm competitive
ability compared with non-carrier males [37,38]. This provides an important link between SGE-carrying and reduced
fertility, and sperm competitive ability in males, which is predicted to promote polyandry as a female strategy to avoid
passing on SGEs to offspring [20,37].
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mean spermatophore size
2.0
1.8
1.6
1.4
0.5
0.4
0.3
0.2
0.1
0.0
no SR
no SR
SR present
equal sex ratio female biased female biased
(n = 3)
(n = 4)
(n = 4)
(b)
Figure 3. The proportion of experimental evolution line
Drosophila pseudoobscura females remating at their first opportunity, for each
selection regime (n ¼ 11 lines), when offered standardized stock males,
showing median, interquartile range, and range (*p ¼ 0.0383; n.s., not
significant). Adapted from Price et al. [69]
2.0
female mating rate
*
n.s.
1.5
1.0
0.5
0
4
5
1
2
3
sex-ratio (log2(female/male))
6
Figure 2. (a) Spermatophore size as a function of male mating rate in the
butterfly H. bolina. Negative correlation is highly significant (Spearman’s rank
correlation test, r ¼ 2 0.66, S ¼ 2206, p ¼ 0.0002). (b) Female mating
rate as a function of population sex ratio. Model comparison showed that a
regression containing both a linear and a quadratic term (dashed curve) fits
the data significantly better than a linear one (F1,17 ¼ 12.10, p ¼ 0.002) or
a purely quadratic one (F1,17 ¼ 11.34, p ¼ 0.004). Female mating rate was
estimated from the mean number of spermatophores per female. Sex ratio is
given as log of number of females per male. Adapted from Charlat et al. [66]
of male fatigue with a concomitant female sperm shortage
that will further promote polyandry. At extreme levels of
male killing, female mating becomes directly limited by
access to males [66]. Polyandry is favoured in this species
because of the limited supply of sperm owing to the shortage,
and exhaustion of the few males in high prevalence populations because of the female-biased sex ratio that in some
populations can be as high as 100 females to one male [65].
Some populations of Drosophila pseudoobscura harbour an
X-linked meiotic drive element, ‘sex ratio’ (SR) that results in
female only broods owing to the elimination of all Y-chromosome sperm during spermatogenesis [63]. In females, SR has
no consistent effect. Despite being an ancient drive system of
approximately 70 000 years, there is no genetic resistance or
suppression of SR drive in D. pseudoobscura [67], and females
cannot distinguish male carriers from normal males [57]. Moreover, there is considerable variation in the frequency of SR,
which has remained remarkably stable for more than 50 years
[68]. The loss of sperm by SR-carrying males makes them
poor sperm competitors [40]. Female multiple mating by promoting sperm competition may thus be an effective strategy
to undermine the transmission of SR by biasing paternity
towards non-carrying males. We therefore predict that females
that are at risk of SR should evolve to remate more frequently
and at a higher rate. This possibility was examined using experimental evolution in replicate populations, demonstrating that
females do indeed rapidly evolve higher remating rates in the
presence of SR (figure 3; [69]). This effect could be attributed to
the presence of SR and not due to the associated female-biased
population sex ratio, as SR alone did not result in evolution of
higher female remating rates. The reason for the rapid evolution
of higher female remating rates in SR populations may be
partially due to sperm and/or ejaculate depletion, which will
be exacerbated in sex-ratio males under a female sex-ratio bias.
In mice populations harbouring an autosomal meiotic
drive system, the t-complex, it has recently been shown that
polyandry is favoured, because female multiple mating
undermines the frequency of the t-allele by promoting
sperm competition that disfavours heterozygous t/þ males
owing to the production of reduced sperm numbers [7].
Recent theoretical work together with extensive laboratory
and field experiments also found that the dynamics of
t alleles in a natural population of house mice could only
be explained by the transmission disadvantage owing to
poor sperm competitive ability [70], which will favour polyandrous females. Similarly, in Solenopsis invicta fire ants, there
is evidence that a selfish gene (Gp-9) that determines the
social organization of the ant colony, also directly influences
the level of polyandry in queens. Workers carrying the Gp-9b
allele only tolerate sexuals that also have the Gp-9b allele, and
always reject and kill Gp-9BB queens. However, males carrying the Gp-9b allele have low sperm counts and as a
consequence suffer reduced paternity in mixed broods compared with Gp-9B males. In addition, the low sperm counts
of Gp-9b males result in increased female remating rates, presumably as a direct consequence of receiving limited amount
of sperm. Reduced paternity in sperm competition together
with an inability to suppress female receptivity represents a
dramatic reduction to the reproductive success of Gp-9b
males [71]. Polyandry in this ant species is, therefore, largely
4
Phil Trans R Soc B 368: 20120049
1.2
0.6
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proportion of females remating at
first opportunity
(a)
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4. When do selfish genetic elements
promote polyandry?
5. Impact of selfish genetic elements on
reproductive behaviours
Endosymbionts can dramatically alter the behaviour and
reproductive morphology of their host [75]. There is plenty
of evidence to suggest that the presence of SGEs more generally can have a dramatic effect on female mating patterns that
can influence the mating system, including the degree of multiple mating. For example, it can alter the reproductive
behaviour of female butterflies in populations harbouring
male-killing bacteria, resulting in sex role reversal. In Acrea
encedon butterflies, lekking is normally carried out by males
in non-female-biased populations, whereas females form
leks in populations with high frequency of male killers and
female-biased sex ratio. Female lekking is suggested to
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It was initially suggested by Zeh & Zeh [20,23] that genetic
incompatibilities have the potential to promote polyandry
as a female strategy to bias paternity against incompatible
males. While there is evidence that SGEs are a frequent
source generating genetic incompatibilities between male
and female genomes, there is remarkably little experimental
examination of this hypothesis. Despite this, there has been
an explosion of reviews examining the potency of genetic
incompatibilities to promote polyandry [15,16,21,29,72].
While there is some evidence that polyandry confers genetic
benefit to females by enabling post-copulatory female choice
(see reviews [15,16,21,29,72]), there is little experimental
support regarding the potency of SGE causing reproductive
incompatibilities to favour polyandry. The one study explicitly examining the potential for CI-inducing Wolbachia to
promote polyandry found that, although polyandrous
females have higher fitness than monogamous females, in
itself this cannot promote polyandry [64]. This is because
the benefit to females depends on the frequency with
which they encounter incompatible males. In this study,
females were equally likely to mate with an incompatible
and a compatible male, as is often the case for studies examining genetic incompatibility avoidance, where the paternity
achieved by related and non-related males is compared
[18]. However, the rate at which incompatible matings
occur has crucial implications for the reproductive benefits
obtained by polyandrous females. As the frequency of
infected females in the population increases, the probability
of an uninfected female mating with both an infected (incompatible) and an uninfected (compatible) male is reduced.
Furthermore, despite the increased reproductive success
obtained by polyandrous females, the spread of polyandry
is constrained by associated costs and the low frequency of
incompatible matings when Wolbachia has reached a stable
equilibrium. The probability of mating with an incompatible
mate in conjunction with the potential costs associated with
polyandry imposes severe restrictions on the conditions
in which incompatibilities caused by Wolbachia generate a
selective advantage for polyandry. Therefore, although
incompatibility avoidance may be a benefit of polyandry,
models based on laboratory data do not support the hypothesis that genetic incompatibilities caused by Wolbachia
promote the evolution of polyandry [64]. However, the
models show that the disadvantage in sperm competition
can inhibit or prevent the invasion of Wolbachia [64]. This is
an important finding as it shows the sperm competitive disadvantage of Wolbachia-infected males relative to uninfected
males can undermine the successful invasion and establishment of CI-inducing Wolbachia in polyandrous populations.
If the sperm of uninfected males win in competition against
sperm from infected males, polyandry may well act to inhibit
the invasion and spread of Wolbachia, and although in principle sperm competition may promote polyandry when
Wolbachia is established, the advantage is typically too weak
to resist even very minor costs of polyandry.
In contrast, polyandry can rapidly evolve when SGEs are
associated with reduced male fertility and does not result in
genetic incompatibilities based on the combination of male
and female genotypes. This situation is common as many
SGEs compromise both male fertility and sperm competitive
ability [37,38]. The impact of SGEs can either be direct or
indirect. In the fire ant, for example, males carrying the
Gp-9b allele produce few sperm, resulting in reduced capacity
to suppress remating in the queens that together with poor
sperm competitive ability undermines male reproductive success [71]. In H. bolina butterflies, male-killing Wolbachia result
in a female-biased population sex ratio, which causes females
to experience sperm limitation owing to lack of males, in turn
promoting female multiple mating to obtain more sperm [66].
This exacerbates the issue of sperm depletion for males (and,
therefore, also for females), as males become increasingly
sperm limited, generating a cycle of increasing female mating
demand and male fatigue. In this situation male-killing
Wolbachia favours polyandry in response to male (i.e. sperm)
limitation. In principle, any sex-ratio distorter has the potential
to promote polyandry as a female response to sperm limitation
owing to the lack of mating males. This possibility needs to
be more widely examined in species harbouring sex-ratio
distorters that cause female-biased population sex ratios.
There is also additional direct evidence that the presence
of a sex-ratio distorter with associated poor sperm competitive ability of male carriers can promote rapid evolution of
polyandry. In experimental populations of D. pseudoobscura
harbouring SR drive, females rapidly evolve increased remating rate when at risk of sex-ratio distorting males [69].
Moreover in laboratory populations, polyandry is effective
at biasing paternity against SR males by promoting sperm
competition [28], thereby undermining the transmission
advantage of SR and suppressing its frequency [28]. In two
species of stalk-eyed flies, females are found to mate more frequently in populations with higher frequency of meiotic
drive. In addition, mating rate increased as the frequency of
drive increases across species [73]. In at least one species,
males carrying the drive allele suffer reduced sperm competitive ability [74], which is likely to be the case also in the other
species. In general, polyandry is likely to be favoured whenever SGE-carrying males suffer reduced fertility and sperm
competitive ability. This situation is fulfilled for many SGEs
[37]. To date, there are few experimental examinations of
this possibility, particularly in the wild, although field data
suggest this may be the case in mice [70].
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determined by the reduced sperm production of Gp-9b males,
again corroborating the existence of a link between carrying a
SGE and reduced sperm numbers [37].
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6. Consequences of polyandry for the dynamics
of selfish genetic elements
The presence of SGEs can promote polyandry, but conversely
polyandry can also directly regulate the frequency of SGEs by
undermining their transmission advantage. An indication
that this may be the case comes from laboratory studies in
D. pseudoobscura showing that polyandry is very effective at
suppressing the frequency of SR. While the frequency of SR
was high in populations evolving under monogamy, just
one remating opportunity was sufficient to dramatically suppress the frequency of SR, with no further benefits from
additional mating in terms of increased SR suppression
[28]. In support for the hypothesis that sperm competition
per se is sufficient to effectively reduce the frequency of sexratio distorters, both theory and empirical studies have
shown that less than two sires per brood are required to
allow invasion and persistence of sex-ratio drive [28,87]. Polyandry may generally play a major role in controlling the
abundance of many SGEs in nature, although to date only
one study has examined this possibility. The population
dynamics of autosomal meiotic driving t alleles in mice
have been investigated for decades [88]. Models commonly
predict t allele frequencies much higher than those found in
natural populations [89]. Recent work using models parametrized with laboratory and field experiments shows that the
dynamics of t alleles in a natural population of house mice
could best be explained by the transmission disadvantage
owing to sperm competition [70].
The potency of polyandry to regulate the dynamics
of SGEs can have important implications for population
viability. Laboratory studies in D. pseudoobscura suggest
that polyandry may directly enhance survival of populations harbouring SR drivers. Populations evolving under
monogamy were found to have a significantly higher probability of going extinct [28]. Each extinction event was
preceded by the production of very few males, indicating
the reason that populations went extinct was due to the
lack of males stemming from a high frequency of SR. This
finding indicates that monogamy is not a viable option in
6
Phil Trans R Soc B 368: 20120049
females in the population [82]. An alternative interpretation
is that the infection is beneficial to males by enabling them
to maintain a higher mating rate than uninfected males.
Although there are benefits of Wolbachia infection in terms
of conferring protection against RNA viruses in both fly
species [84,85], this benefit is enjoyed by both sexes and
cannot explain why infected males should mate at a higher
rate than uninfected males (and endosymbiont protection
against viruses is not universal [86]). In addition, infected
D. simulans males suffer reduced sperm production [61]
and sperm competitive ability [39] relative to uninfected
males, further suggesting that Wolbachia infection is not
associated with a reproductive advantage to males. This
result taken together with the finding that uninfected
D. simulans females remate sooner (the only ones at risk of
CI), suggests that Wolbachia infection can favour both male
and female multiple mating as a strategy to avoid associated reproductive incompatibilities, but that the impact
differs depending on the infection status. The net result
is an increased level of multiple mating and polyandry in
populations harbouring Wolbachia.
rstb.royalsocietypublishing.org
increase the likelihood of mating [76], and may also increase
the likelihood of multiple mating. Changes in female mating
patterns in response to the presence of SGEs will also influence male mating behaviours and strategies. In D.
pseudoobsura, for example, non-carrier males that coevolved
with females that evolved increased remating rates in the
presence of SR males were found to evolve increased sperm
transfer at mating. This is likely a response to the higher
risk of sperm competition experienced by males in these
high polyandry populations compared with populations
evolving without the SR allele, where females did not
evolve to mate at a higher rate [77]. In addition, males evolving in the high polyandry populations were also better at
suppressing female remating, and there was a tight relationship between the level of female multiple mating and
males’ ability to suppress female remating across populations, with males from populations where females
evolved the highest remating rates being best able suppress
female remating. Despite this, females were able to maintain
high remating rates, indicating that it is variation in female
remating rate that drives male ejaculate evolution. This provides evidence for strong male– female coevolution driven
by the presence of the SR allele, even when present at a
low frequency (less than 5%). Similarly, in isopods infected
by feminizing bacteria, males may have evolved an increased
ability to inseminate more females, most likely in response to
a chronic female population sex ratio [78].
SGEs can also affect morphological traits. In the Allonemobius
socius cricket species complex, for example, Wolbachia modify
the length of the spermathecal duct of females. There is a
causal link between Wolbachia infection status and the length
of the spermathecal duct, as curing reduces the length to
resemble uninfected female tract morphology [79]. This may
have important implications for male fertilization success, as in
D. melanogaster longer reproductive tract length is associated
with greater female influence over the outcome of sperm competition and therefore exerts selection on sperm length [80].
Inspired by the finding in crickets, a recent model suggests
that endosymbiont-induced changes to female reproductive
traits can directly impact on the dynamics of sexual conflict by
directly affecting the mating rates of females. This, in turn, can
maintain the infection within the host population, even in the
absence of any reproductive manipulation such as sex-ratio
distortion or reproductive incompatibilities [81]. It is unclear to
what extent endosymbionts and other SGEs can manipulate
morphological traits important for reproduction in other species,
or indeed by what mechanism, but they clearly have the
potential to directly affect female mating rate and, therefore,
polyandry levels by manipulating reproductive traits.
There is also evidence that the presence of SGEs can
directly affect male mating strategies. In D. melanogaster and
D. simulans harbouring CI-inducing Wolbachia, infected
males have significantly higher mating rates than uninfected
males [82]. Moreover, the difference in male mating rate
covaries with the level of CI. It is more pronounced in
D. simulans where wRi induces a more severe CI, with more
than 95 per cent of crosses between uninfected females and
infected males failing to hatch compared with less than
30 per cent in similar crosses in D. melanogaster. There is evidence that the level of CI declines with both male age and
male mating frequency [83]. It is therefore possible that the
higher level of mating by infected male Drosophila may be a
strategy to regain reproductive compatibility with all the
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SGEs clearly have the potential to generate sexual selection,
sexual conflict and to promote polyandry. Sexual selection
and conflict can occur as a side effect of selection on females’
mating behaviour to avoid mating with SGE-carrying males,
which in turn can generate bouts of selection and counteradaptation by males. This possibility has been demonstrated
(e.g. increased female mating frequency in butterflies carrying male-killing bacteria [66], SR drive promoting evolution
of polyandry in flies [69]). The main cause of the impact
of SGEs on female mating patterns is driven by the association between low fertility and reduced paternity in sperm
competition of males carrying SGEs. This favours female
multiple mating, which can increase sexual conflict over
mating frequency [37,39]. A less well-studied situation
is the realization that the SGE itself can have sex-specific
effects when present in males and females, potentially
causing sexual conflict [93]. A recent example of this is
DDT-resistance alleles (DDT-R) in D. melanogaster flies.
DDT-R is caused by a SGE—a retrotransposon inserted into
the promoter region of a detoxification gene (Cyp6g1) that
7
Phil Trans R Soc B 368: 20120049
7. Summary and future prospects
upregulates this gene in both sexes. Intriguingly, DDT-resistant females are more fecund and have offspring of higher
fitness than susceptible females [94]. Despite this fitness
advantage to females, DDT-R did not spread before the use
of pesticides [95]. This implies a cost to males in order to
balance the benefits to females—the hallmark of a sexually
antagonistic allele. Remarkably, this seems to be the case.
In males, DDT-R makes them less likely to obtain matings
when competing for females with susceptible males [93].
This cost (relative fitness reduction to DDT-R males 20.28)
almost perfectly balances the fitness benefit to females
(þ0.25 [94]) when DDT-R is expressed in the same genetic
background. However, there is also evidence of extensive
epistasis between the DDT-R allele and the genetic background in which it is expressed [93], but it shows that the
sexual conflict it can generate clearly has the potential to
affect the spread of resistance alleles. It is possible that
other SGEs may function as sexually antagonistic alleles
with opposite fitness effects when expressed in males and
females. If this is the case, it indicates that SGEs may not
only generate sexual selection and sexual conflict by favouring polyandry, as this will result in increased risk of sperm
competition with potential loss of paternity for males, but
may also generate conflict by acting as a sexually antagonistic
allele with large sex-specific fitness effects. To date, the extent
to which SGEs may have such sex-specific fitness effects is
not known, but considering their prevalence throughout the
genome and their direct involvement in gene regulation, it
is likely to be an overlooked possibility.
So how important are SGEs in general for variation in
female mating frequency between species and populations?
The simple answer is that we do not know. However, seeing
the ubiquitous nature of SGEs in animals and plants, it is
likely to be a more common reason for polyandry than previously recognized, although the pervasiveness of polyandry
across taxa is likely due to more than one reason. Future studies
should focus on exploring the potential that high polyandry
populations may have arisen as a female response to the
existence of SGEs, although the feasibility of determining this
possibility may be hampered by the difficulty of identifying
the SGE within the genome of most species. One fruitful
approach may be to examine the impact of various endosymbionts known to manipulate host reproduction (there are
diagnostic tools (PCR) available for several arthropod endosymbionts—e.g. Wolbachia, Spiroplasma, Cardinium) on the
level of polyandry between females and populations with or
without endosymbionts. A caveat is that some endosymbionts
also have a beneficial role in many insects [84,85].
In nature, genetic suppressors of SGEs frequently evolve,
thereby obscuring their presence. It is therefore likely that
SGEs are more common in populations than we can appreciate at first glance. Such genetic suppressors are often
population specific; hence divergent populations may be at
risk when coming into secondary contact as they may be
exposed to a SGE without the protection of a corresponding
suppressor [90]. The impact can be pronounced by generating
severe reproductive incompatibilities and hybrid dysfunction
[96] that can contribute to species divergence and potentially
even speciation [97]. This situation is likely to occur on secondary contact of previously isolated populations, or when
a species colonizes a new habitat. The emergence of sexratio bias when populations interbreed is a strong contender
for the re-surfacing of an unsuppressed distorter [98]. It is
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populations harbouring sex-ratio distorters, further promoting polyandry. If in nature, monogamous populations
harbouring sex-ratio distorters are generally at a higher risk
of going extinct, this would further add to an association
between polyandry and the presence of SGEs. This possibility
may be difficult to quantify in the wild, because documenting
extinction events of entire populations is inherently difficult to
observe [90]. The recent discovery of a cline in polyandry that
underlies the cline in SR in D. pseudoobscura across North
America may hint at such a relationship between degree of
polyandry and the frequency of SR (T. A. R. Price, G. D. D.
Hurst & N. Weddell 2012, unpublished data).
As yet, we have no idea how important variation in
female multiple mating is for determining the frequency of
SGEs, although models predict polyandry can allow the persistence of SGEs at a stable equilibrium in the population [87].
We need more systematic surveys of populations harbouring
SGEs with clear differences in degree of polyandry to allow
us to examine if there is a corresponding variation in the
frequency of SGEs. One possible example could be the fly
Drosophila neotestacea that shows a clinal distribution in the
frequency of a meiotic driver across the USA, implicating
temperature as the regulating factor [91], although it is not
known whether there is corresponding variation also in
degree of polyandry that may regulate the frequency of meiotic drive. Another potential example may be the weevil
Curculio sikkimensis that also shows a clinal distribution in
the frequency of Wolbachia [92], but to date, there is no information regarding possible underlying variation in polyandry
along this cline. The difficulty with any association between
the frequency of an SGE and degree of polyandry is that it
may not be possible to determine the causal relationship: is
the frequency of SGEs determined by the level of polyandry,
or is the level of polyandry determined by the frequency of
the SGEs? Ideally, additional experimental manipulations
are needed to disentangle the link between the two, although
it is possible, or even likely, that both processes are operating
simultaneously, ultimately determining a stable equilibrium
of both the frequency of SGEs and the level of polyandry.
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The preparation of this article was supported by a Royal Society Wolfson
Research Merit Award and NERC (NE/I027711/1) to N W. The author
would also like to thank David Hosken, Judith Mank and Tom Pizzari
for many helpful discussions and stimulating debates, and the
anonymous referees for many excellent suggested improvements.
References
1.
Birkhead TR, Møller AP. 1998 Sperm competition
and sexual selection. London, UK: Academic Press.
2. Birkhead TR, Hosken DJ, Pitnick S. 2009 Sperm
biology: an evolutionary perspective. Burlington, MA:
Academic Press.
3. Lima SL, Dill LM. 1990 Behavioral decisions made
under the risk of predation: a review and
prospectus. Can. J. Zool. 68, 619–640. (doi:10.
1139/z90-092)
4. Crudgington HS, Siva-Jothy MT. 2000 Genital
damage, kicking and early death. Nature 407,
855–856. (doi:10.1038/35038154)
5. Chapman T, Liddle LF, Kalb JM, Wolfner MF,
Partridge L. 1995 Cost of mating in Drosophila
melanogaster females is mediated by male
accessory gland products. Nature 373, 241–244.
(doi:10.1038/373241a0)
6. Hurst GDD, Sharpe RG, Broomfield AH,
Walker LE, Majerus TMO, Zakharov IA,
Majerus MEN. 1995 Sexually transmitted disease in
a promiscuous insect, Adalia bipunctata. Ecol.
Entomol. 20, 230 –236. (doi:10.1111/j.1365-2311.
1995.tb00452.x)
7. Davies NB, Hartley IR, Hatchwell BJ, Langmore NE.
1996 Female control of copulations to maximize
male help: a comparison of polygynandrous alpine
accentors, Prunella collaris, and dunnocks,
P. modularis. Anim. Behav. 51, 27 – 47. (doi:10.
1006/anbe.1996.0003)
8. Arnqvist G, Nilsson T. 2000 The evolution of
polyandry: multiple mating and female fitness in
insects. Anim. Behav. 60, 145 –164. (doi:10.1006/
anbe.2000.1446)
9. Wedell N, Gage MJG, Parker GA. 2002 Sperm
competition, male prudence and sperm-limited
females. Trends Ecol. Evol. 17, 313–320.
(doi:10.1016/S0169-5347(02)02533-8)
10. Parker GA, Pizzari T. 2010 Sperm competition and
ejaculate economics. Biol. Rev. 85, 897 –934.
(doi:10.1111/j.1469-185X.2010.00140.x)
11. Clutton-Brock TH. 1989 Review lecture: mammalian
mating systems. Proc. R. Soc. Lond. B 236,
339 –372. (doi:10.1098/rspb.1989.0027)
12. Baer B, Schmid-Hempel P. 1999 Experimental
variation in polyandry affects parasite loads and
fitness in a bumble-bee. Nature 397, 151–154.
(doi:10.1038/16451)
13. Fisher DO, Double MC, Blomberg SP, Jennions MD,
Cockburn A. 2006 Post-mating sexual selection
increases lifetime fitness of polyandrous females in
the wild. Nature 444, 89 –92. (doi:10.1038/
nature05206)
14. Hosken DJ, Taylor ML, Hoyle K, Higgins S, Wedell N.
2008 Attractive males have greater success in sperm
competition. Curr. Biol. 18, R553 –R554. (doi:10.
1016/j.cub.2008.04.028)
15. Slatyer RA, Mautz BS, Backwell PRY, Jennions MD.
2012 Estimating genetic benefits of polyandry from
experimental studies: a meta-analysis. Biol. Rev. 87,
1 –33. (doi:10.1111/j.1469-185X.2011.00182.x)
16. Jennions MD, Petrie M. 2000 Why do females mate
multiply? A review of the genetic benefits. Biol. Rev.
75, 21 –64. (doi:10.1017/S0006323199005423)
17. Pryke SR, Rollins LA, Griffith SC. 2010 Females use
multiple mating and genetically loaded sperm
competition to target compatible genes. Science
329, 964 –967. (doi:10.1126/science.1192407)
18. Tregenza T, Wedell N. 2002 Polyandrous females
avoid costs of inbreeding. Nature 415, 71 –73.
(doi:10.1038/415071a)
19. Michalczyk L, Millard AL, Martin OY, Lumley AJ,
Emerson BC, Chapman T, Gage MJG. 2011
Inbreeding promotes female promiscuity. Science
333, 1739–1742. (doi:10.1126/science.1207314)
20. Zeh JA, Zeh DW. 1997 The evolution of
polyandry. II. Post-copulatory defences against
genetic incompatibility. Proc. R. Soc. Lond. B 264,
69 –75. (doi:10.1098/rspb.1997.0010)
21. Tregenza T, Wedell N. 2000 Genetic compatibility,
mate choice, and patterns of parentage. Mol. Ecol.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
9, 1013 –1027. (doi:10.1046/j.1365-294x.2000.
00964.x)
Ayroles JF, Hughes KA, Rowe KC, Reedy MM,
Rodriguez-Zas SL, Drnevich JM, Cáceres CE, Paige
KN. 2009 A genomewide assessment of inbreeding
depression: gene number, function, and mode of
action. Conserv. Biol. 23, 920–930. (doi:10.1111/j.
1523-1739.2009.01186.x)
Zeh JA, Zeh DW. 1996 The evolution of polyandry. I.
Intra-genomic conflict and genetic incompatibility.
Proc. R. Soc. Lond. B 263, 1711– 1717. (doi:10.
1098/rspb.1996.0250)
Arnqvist G, Rowe L. 2005 Sexual conflict. Princeton,
NJ: Princeton University Press.
Hrdy SB. 1979 Infanticide among animals: a review,
classification, and examination of the implications
for the reproductive strategies of females. Ethol.
Sociobiol. 1, 13 –40. (doi:10.1016/0162-3095(79)
90004-9)
Jaffe R, Moritz RFA, Kraus FB. 2009 Gene
flow is maintained by polyandry and male
dispersal in the army ant Eciton burchellii.
Popul. Ecol. 51, 227– 236. (doi:10.1007/s10144008-0133-1)
Rankin D, Dieckmann U, Kokko H. 2011 Sexual
conflict and the tragedy of the commons. Am. Nat.
177, 780–791. (doi:10.1086/659947)
Price TAR, Hurst GDD, Wedell N. 2010 Polyandry
prevents extinction. Curr. Biol. 20, 471– 475.
(doi:10.1016/j.cub.2010.01.050)
Simmons LW. 2005 The evolution of polyandry: an
examination of the genetic incompatibility and
good-sperm hypotheses. J. Evol. Biol 14, 585 –594.
(doi:10.1046/j.1420-9101.2001.00309.x)
Hosken DJ, Stockley P, Tregenza T, Wedell N. 2009
Monogamy and the battle of the sexes. Ann. Rev.
Entomol. 54, 361– 378. (doi:10.1146/annurev.ento.
54.110807.090608)
Trivers RL. 1974 Parent-offspring conflict. Am. Zool.
14, 249 –264. (doi:10.1093/icb/14.1.249)
8
Phil Trans R Soc B 368: 20120049
polyandrous do indeed suffer a lower burden of deleterious
sex-ratio distorters [102]. Hence, in this species, variation in
polyandry could potentially determine the frequency of an
SGE and therefore the population sex ratio in natural populations. Because SGEs are ubiquitous in living organisms
and frequently compromise male fertility and sperm competitive ability, they may provide a generally overlooked
explanation for why polyandry is widespread. Conversely,
although polyandry can be a potent determinant of the intensity of sexual selection, sexual conflict, parent–offspring
conflict, and the evolution of cooperation and sociality,
there is growing evidence that polyandry may also protect
a population against the invasion and spread of SGEs.
rstb.royalsocietypublishing.org
possible that polyandry under such circumstances is
favoured if it provides protection to females by reducing
the risk of siring offspring by males with a novel and unsuppressed SGE. This may provide an additional explanation for
the observation that colonizing females appear to be less
choosy [99,100]. Theory shows that polyandry is favoured
during colonization events by reducing the risk of inbreeding
[101]. A similar argument could be made for dispersing
females at risk of encountering males with novel SGEs without the protection of corresponding suppressors.
The wide range of SGEs can provide the key combination
of low sperm competitive ability and low fitness that in many
circumstances will favour polyandry. As a corollary that
SGEs can promote polyandry, theory and laboratory experimental evolution studies indicate that high levels of
polyandry can aid genomic cohesion by protecting a population against the invasion of SGEs: for example, natural
populations of D. pseudoobscura where females are more
Downloaded from http://rstb.royalsocietypublishing.org/ on June 18, 2017
65.
66.
67.
68.
69.
70.
71.
72.
73.
74.
75.
76.
77.
78.
promote polyandry? Evolution 62, 107–122.
(doi:10.1111/j.1558-5646.2007.00274.x)
Dyson EA, Hurst GDD. 2004 Persistence of an
extreme sex-ratio bias in a natural population.
Proc. Natl Acad. Sci. USA 101, 6520–6523. (doi:10.
1073/pnas.0304068101)
Charlat S, Reuter M, Dyson EA, Hornett EA, Duplouy
AMR, Davies N, Roderick GK, Wedell N, Hurst GDD.
2007 Male killing bacteria trigger a cycle of
increasing male fatigue and female promiscuity.
Curr. Biol. 17, 273–277. (doi:10.1016/j.cub.
2006.11.068)
Policansky D, Dempsey B. 1978 Modifiers and ‘sexratio’ in Drosophila pseudoobscura. Evolution 32,
922–924. (doi:10.2307/2407507)
Powell J. 1997 Progress and prospects in
evolutionary biology: the Drosophila model. Oxford,
UK: Oxford University Press.
Price TAR, Hodgson DJ, Lewis Z, Hurst GDD, Wedell
N. 2008 Selfish genetic elements promote polyandry
in a fly. Science 322, 1241 –1243. (doi:10.1126/
science.1163766)
Manser A, Lindholm A, König B, Bagheri H. 2011
Polyandry and the decrease of a selfish genetic
element in a wild house mouse population.
Evolution 65, 2435– 2447. (doi:10.1111/
j.1558-5646.2011.01336.x)
Lawson LP, Vander Meer RK, Shoemaker D.
2012 Male reproductive fitness and queen
polyandry are linked to variation in the
supergene Gp-9 in the fire ant Solenopsis invicta.
Proc. R. Soc. B 279, 3217 –3222. (doi:10.1098/
rspb.2012.0315)
Zeh JA, Zeh DW. 2003 Toward a new sexual
selection paradigm: polyandry, conflict and
incompatibility. Ethology 109, 929–950.
(doi:10.1046/j.1439-0310.2003.00945.x)
Wilkinson GS, Swallow JG, Christensen SJ,
Madden K. 2003 Phylogeography of sex ratio
and multiple mating in stalk-eyed flies from
Southeast Asia. Genetica 117, 37– 46. (doi:10.1023/
A:1022360531703)
Fry CL, Wilkinson GS. 2004 Sperm survival in female
stalkeyed flies depends on seminal fluid and meiotic
drive. Evolution 58, 1622–1626.
Goodacre SL, Martin OY. 2012 Modification of insect
and arachnid behaviours by vertically transmitted
endosymbionts: infections as drivers of behavioural
change and evolutionary novelty. Insects 3,
246–261. (doi:10.3390/insects3010246)
Jiggins FM, Hurst GDD, Majerus MEN. 2000 Sexratio-distorting Wolbachia causes sex-role reversal in
its butterfly host. Proc. R. Soc. Lond. B 267, 69 –73.
(doi:10.1098/rspb.2000.0968)
Price TAR, Lewis Z, Smith DT, Hurst GDD, Wedell N.
2010 Sex ratio drive promotes sexual conflict and
sexual coevolution in the fly Drosophila
pseudoobscura. Evolution 64, 1504–1509.
Moreau J, Bertin A, Caubet Y, Rigaud T. 2001 Sexual
selection in an isopod with Wolbachia-induced
sexual reversal: males prefer real females. J. Evol.
Biol. 14, 388–394. (doi:10.1046/j.1420-9101.2001.
00292.x)
9
Phil Trans R Soc B 368: 20120049
49. Sharon G, Segal D, Ringo JM, Hefetz A, ZilberRosenberg I, Rosenberg E. 2010 Commensal bacteria
play a role in mating preference of Drosophila
melanogaster. Proc. Natl Acad. Sci. USA 107,
20 051– 20 056. (doi:10.1073/pnas.1009906107)
50. Ringo J, Sharon G, Segal D. 2011 Bacteria-induced
sexual isolation in Drosophila. Fly 5, 310–315.
(doi:10.4161/fly.5.4.15835)
51. Vala F, Breeuwer JAJ, Sabelis MW. 2004
Endosymbiont associated assortative mating in a
spider mite. J. Evol. Biol. 17, 692–700. (doi:10.
1046/j.1420-9101.2003.00679.x)
52. Moureau J, Rigaut T. 2003 Variable male potential
rate of reproduction: high male mating capacity as
an adaptation to parasite-induced excess of
females? Proc. R. Soc. Lond. B 270, 1535–1540.
(doi:10.1098/rspb.2003.2402)
53. Dunn AM, Andrews T, Ingrey H, Riley J, Wedell N.
2006 Strategic sperm allocation under parasitic sexratio distortion. Biol. Lett. 2, 78 –80. (doi:10.1098/
rsbl.2005.0402)
54. Champion de Crespigny FE, Wedell N. 2007 Mate
preferences in Drosophila infected with Wolbachia?
Behav. Ecol. Sociolbiol. 61, 1229–1235.
(doi:10.1007/s00265-007-0353-y)
55. Markov AV, Lazebny OE, Goryacheva II, Antipin MI,
Kulikov AM. 2009 Symbiotic bacteria affect mating
choice in Drosophila melanogaster. Anim. Behav. 77,
1011 –1017. (doi:10.1016/j.anbehav.2009.01.011)
56. Fernandez AA, Morris MR. 2008 Mate choice for
more melanin as a mechanism to maintain a
functional oncogene. Proc. Natl Acad. Sci. USA 105,
13 503– 13 507. (doi:10.1073/pnas.0803851105)
57. Price TAR, Lewis Z, Smith DT, Hurst GDD, Wedell N.
2012 No evidence of mate discrimination against
males carrying a sex ratio distorter in Drosophila
pseudoobscura. Behav. Ecol. Sociobiol. 66, 561–568.
(doi:10.1007/s00265-011-1304-1)
58. Nichols RA, Butlin RK. 1989 Does runaway sexual
selection work in finite populations. J. Evol. Biol. 2,
299–313. (doi:10.1046/j.1420-9101.1989.2040299.x)
59. Johns PM, Wolfenbarger LL, Wilkinson GS. 2005
Genetic linkage between a sexually selected trait
and X chromosome meiotic drive. Proc. R. Soc. B
272, 2097–2103. (doi:10.1098/rspb.2005.3183)
60. Lenington S, Coopersmith C, Williams J. 1992
Genetic basis of mating preferences in wild house
mice. Am. Zool. 32, 40 –47. (doi:10.1093/
icb/32.1.40)
61. Snook RR, Cleland SY, Wolfner MF, Karr TL. 2000
Offsetting effects of Wolbachia infection and heat
shock on sperm production in Drosophila simulans:
analyses of fecundity, fertility and accessory gland
proteins. Genetics 155, 167–178.
62. Lewis Z, Champion de Crespigny FE, Sait SM,
Tregenza T, Wedell N. 2011 Wolbachia infection
lowers fertile sperm transfer in a moth. Biol. Lett. 7,
187 –189. (doi:10.1098/rsbl.2010.0605)
63. Policansky D, Ellison J. 1970 ‘Sex ratio’ in Drosophila
pseudoobscura: spermiogenic failure. Science 169,
888 –889. (doi:10.1126/science.169.3948.888)
64. Champion de Crespigny FE, Hurst LD, Wedell N.
2008 Do Wolbachia-associated incompatibilities
rstb.royalsocietypublishing.org
32. Hughes WO, Oldroyd BP, Beekman M, Ratnieks LW.
2008 Ancestral monogamy shows kin selection is
key to the evolution of eusociality. Science 320,
1213–1216. (doi:10.1126/science.1156108)
33. Cornwallis CK, West SA, Davis KE, Griffin AS. 2010
Promiscuity and the evolutionary transition to
complex societies. Nature 466, 969–972.
(doi:10.1038/nature09335)
34. Haig D, Bergstrom CT. 1995 Multiple mating, sperm
competition and meiotic drive. J. Evol. Biol. 8,
265–282. (doi:10.1046/j.1420-9101.1995.8030265.x)
35. Yasui Y. 1998 The ‘genetic benefits’ of female
multiple mating reconsidered. Trends Ecol. Evol. 13,
246–250. (doi:10.1016/S0169-5347(98)01383-4)
36. Parker GA. 1970 Sperm competition and its
evolutionary consequences in the insects. Biol. Rev.
45, 525–567. (doi:10.1111/j.1469-185X.
1970.tb01176.x)
37. Price TAR, Wedell N. 2008 Selfish genetic elements
and sexual selection: their impact on male fertility.
Genetica 132, 295–307. (doi:10.1007/s10709-0079173-2)
38. Lewis Z, Price TAR, Wedell N. 2008 Review: sperm
competition, immunity, selfish genes and cancer.
Cell Mol. Life Sci. 65, 3241 –3254. (doi:10.1007/
s00018-008-8238-4)
39. Champion de Crespigny FE, Wedell N. 2006
Wolbachia infection reduces sperm competitive
ability in an insect. Proc. R. Soc. B 273,
1455–1458. (doi:10.1098/rspb.2006.3478)
40. Price TAR, Bretman AJ, Avent TD, Snook RR, Hurst
GDD, Wedell N. 2008 Sex ratio distorter reduces sperm
competitive ability in an insect. Evolution 62,
1644–1652. (doi:10.1111/j.1558-5646.2008.00386.x)
41. Burt A, Trivers RL. 2006 Genes in conflict: the
biology of selfish genetic elements. Harvard, MA:
Harvard University Press.
42. Hurst GDD, Werren JH. 2001 The role of selfish
genetic elements in eukaryotic evolution. Nat. Rev.
Genet. 2, 597–606. (doi:10.1038/35084545)
43. Werren JH. 2011 Selfish genetic elements, genetic
conflict, and evolutionary innovation. Proc. Natl
Acad. Sci. USA 108(Suppl. 2), 10 863– 10 870.
(doi:10.1073/pnas.1102343108)
44. Jaenike J. 2001 Sex chromosome meiotic drive. Ann.
Rev. Ecol. Syst. 32, 25 –49. (doi:10.1146/annurev.
ecolsys.32.081501.113958)
45. Haig D. 2012 Retroviruses and the placenta.
Curr. Biol. 22, R609 –R613. (doi:10.1016/j.cub.
2012.06.002)
46. Wilkinson GS, Presgraves DC, Crymes L. 1998 Male
eye span in stalk-eyed flies indicates genetic quality
by meiotic drive suppression. Nature 391,
276–279. (doi:10.1038/34640)
47. Lenington S. 1991 The t-complex: a story
of genes, behavior, and populations. Adv. Stud.
Behav. 20, 51 –86. (doi:10.1016/S0065-3454
(08)60319-8)
48. Miller W, Ehrman L, Schneider D. 2010 Infection
speciation revisited: impact of symbiont-depletion
on female fitness and mating behavior of Drosophila
paulistorum. PLoS Path. 6, 1001214. (doi:10.1371/
journal.ppat.1001214)
Downloaded from http://rstb.royalsocietypublishing.org/ on June 18, 2017
95. Catania F, Kauer MO, Daborn PJ, Yen JL, ffrenchConstant RH, Schlotterer C. 2004 World wide survey of
an Accord insertion and its association with DDT
resistance in Drosophila melanogaster. Mol. Ecol. 13,
2491–2504. (doi:10.1111/j.1365-294X.2004.02263.x)
96. Presgraves DC. 2010 The molecular evolutionary
basis of species formation. Nat. Rev. Gen. 11,
175–180. (doi:10.1038/nrg2718)
97. Phadnis N, Orr HAA. 2008 A single gene causes
both male sterility and segregation distortion in
Drosophila hybrids. Science 323, 376 –379. (doi:10.
1126/science.1163934)
98. Taylor DR, Ingvarson PK. 2003 Common features
of segregation distortion in plants and animals.
Genetica 117, 27 –35. (doi:10.1023/A:102230
8414864)
99. Kaneshiro KY. 2006 Sexual selection in the
Hawaiian Drosophillidae. Proc. Hawaiian Entomol.
Soc. 38, 1 –19.
100. Tinghitella RM, Zuk M. 2009 Asymmetric mating
preferences accommodated the rapid evolutionary
loss of a sexual signal. Evolution 63, 2087–2098.
(doi:10.1111/j.1558-5646.2009.00698.x)
101. Cornell SJ, Tregenza T. 2007 A new theory for the
evolution of polyandry as a means of inbreeding
avoidance. Proc. R. Soc. B 274, 2873– 2879. (doi:10.
1098/rspb.2007.0926)
102. Price TAR, Lewis Z, Smith DT, Hurst GDD, Wedell N.
2011 Remating in the laboratory reflects rates of
polyandry in the wild. Anim. Behav. 82,
1381– 1386. (doi:10.1016/j.anbehav.2011.09.022)
10
Phil Trans R Soc B 368: 20120049
87. Taylor DR, Jaenike J. 2002 Sperm competition and
the dynamics of X chromosome drive: stability and
extinction. Genetics 160, 1721–1751.
88. Silver LM. 1993 The peculiar journey of a selfish
chromosome: mouse t haplotypes and meiotic
drive. Trends Genet. 9, 250– 254. (doi:10.1016/
0168-9525(93)90090-5)
89. Carroll L, Meagher S, Morrison L, Penn D, Potts W.
2004 Fitness effects of a selfish gene (the Mus t
complex) are revealed in an ecological context.
Evolution 58, 1318–1328.
90. Carvalho AB, Vaz CS. 1999 Are Drosophila SR drive
chromosomes always balanced? Heredity 83,
221 –228. (doi:10.1038/sj.hdy.6886100)
91. Dyer K. 2011 Local selection underlies the
geographic distribution of sex-ratio drive in
Drosophila neotestacea. Evolution 66, 973–984.
(doi:10.1111/j.1558-5646.2011.01497.x)
92. Toju H, Fukatsu T. 2011 Diversity and infection
prevalence of endosymbionts in natural populations
of the chestnut weevil: relevance of local climate
and host plants. Mol. Ecol. 20, 853– 868. (doi:10.
1111/j.1365-294X.2010.04980.x)
93. Smith DT, Hosken DJ, Rostant WG, Griffin RM,
Bretman A, Price TAR, ffrench-Constant RH,
Wedell N. 2011 DDT resistance, epistasis and male
fitness in flies. J. Evol. Biol. 24, 1351–1362.
(doi:10.1111/j.1420-9101.2011.02271.x)
94. McCart C, Buckling A, ffrench-Constant RH. 2005
DDT resistance in flies carries no cost. Curr. Biol. 15,
R587 –R589. (doi:10.1016/j.cub.2005.07.054)
rstb.royalsocietypublishing.org
79. Marshall JL. 2007 Rapid evolution of spermathecal duct
length in the Allonemobius socius complex of crickets:
species, population and Wolbachia effects. PLoS ONE 2,
e720. (doi:10.1371/journal.pone.0000720)
80. Miller GT, Pinick S. 2002 Sperm-female coevolution
in Drosophila. Science 298, 1230 –1233. (doi:10.
1126/science.1076968)
81. Hayashi TI, Marshall JL, Gavrilets S. 2007 The
dynamics of sexual conflict over mating rate with
endosymbiont infection that affects reproductive
phenotypes. J. Evol. Biol. 20, 2154–2164. (doi:10.
1111/j.1420-9101.2007.01429.x)
82. Champion de Crespigny FE, Pitt T, Wedell N. 2006
Increased male mating rate in Drosophila is associated
with Wolbachia infection. J. Evol. Biol. 19,
1964–1972. (doi:10.1111/j.1420-9101.2006.01143.x)
83. Karr TL, Yang W, Feder ME. 1998 Overcoming
cytoplasmic incompatibility in Drosophila.
Proc. R. Soc. Lond. B 265, 391–395. (doi:10.1098/
rspb.1998.0307)
84. Hedges LM, Brownlie JC, O’Neill SL, Johnson KN.
2008 Wolbachia and virus protection in insects.
Science 322, 702. (doi:10.1126/science.1162418)
85. Teixeira L, Ferreira A, Ashburner M. 2008 The bacterial
symbiont Wolbachia induces resistance to RNA viral
infections in Drosophila melanogaster. PLoS Biol. 6,
2753–2763. (doi:10.1371/journal.pbio.1000002)
86. Longdon B, Fabian DK, Hurst GDD, Jiggins FM. 2012
Male-killing Wolbachia do not protect Drosophila
bifasciata against viral infection. BMC Microbiol. 12,
S8. (doi:10.1186/1471-2180-12-S1-S8)