GENETIC DRIFT IN ANTAGONISTIC GENES LEADS TO DIVERGENCE IN SEX‐SPECIFIC FITNESS BETWEEN EXPERIMENTAL POPULATIONS OF DROSOPHILA MELANOGASTER

Males and females differ in their reproductive roles and as a consequence are often under diverging selection pressures on shared phenotypic traits. Theory predicts that divergent selection can favor the invasion of sexually antagonistic alleles, which increase the fitness of one sex at the detriment of the other. Sexual antagonism can be subsequently resolved through the evolution of sex‐specific gene expression, allowing the sexes to diverge phenotypically. Although sexual dimorphism is very common, recent evidence also shows that antagonistic genetic variation continues to segregate in populations of many organisms. Here we present empirical data on the interaction between sexual antagonism and genetic drift in populations that have independently evolved under standardized conditions. We demonstrate that small experimental populations of Drosophila melanogaster have diverged in male and female fitness, with some populations showing high male, but low female fitness while other populations show the reverse pattern. The between‐population patterns are consistent with the differentiation in reproductive fitness being driven by genetic drift in sexually antagonistic alleles. We discuss the implications of our results with respect to the maintenance of antagonistic variation in subdivided populations and consider the wider implications of drift in fitness‐related genes.     

Antagonistic pleiotropy in species with separate sexes,and the maintenance of genetic variation in life‐history traits and fitness

Antagonistic pleiotropy (AP)—where alleles of a gene increase some components of fitness at a cost to others—can generate balancing selection, and contribute to the maintenance of genetic variation in fitness traits, such as survival, fecundity, fertility, and mate competition. Previous theory suggests that AP is unlikely to maintain variation unless antagonistic selection is strong, or AP alleles exhibit pronounced differences in genetic dominance between the affected traits. We show that conditions for balancing selection under AP expand under the likely scenario that the strength of selection on each fitness component differs between the sexes. Our model also predicts that the vast majority of balanced polymorphisms have sexually antagonistic effects on total fitness, despite the absence of sexual antagonism for individual fitness components. We conclude that AP polymorphisms are less difficult to maintain than predicted by prior theory, even under our conservative assumption that selection on components of fitness is universally sexually concordant. We discuss implications for the maintenance of genetic variation, and for inferences of sexual antagonism that are based on sex‐specific phenotypic selection estimates—many of which are based on single fitness components.     

MALE‐BIASED FITNESS EFFECTS OF SPONTANEOUS MUTATIONS IN DROSOPHILA MELANOGASTER

In populations with males and females, sexual selection may often represent a major component of overall selection. Sexual selection could act to eliminate deleterious alleles in concert with other forms of selection, thereby improving the fitness of sexual populations. Alternatively, the divergent reproductive strategies of the sexes could promote the maintenance of sexually antagonistic variation, causing sexual populations to be less fit. The net impact of sexual selection on fitness is not well understood, due in part to limited data on the sex‐specific effects of spontaneous mutations on total fitness. Using a set of mutation accumulation lines of Drosophila melanogaster, we found that mutations were deleterious in both sexes and had larger effects on fitness in males than in females. This pattern is expected to reduce the mutation load of sexual females and promote the maintenance of sexual reproduction.     

Parental sex discrimination and intralocus sexual conflict

Intralocus sexual conflict occurs when populations segregate for alleles with opposing fitness consequences in the two sexes. This form of selection is known to be capable of maintaining genetic and fitness variation in nature, the extent of which is sensitive to the underlying genetics. We present a one-locus model of a haploid maternal effect that has sexually antagonistic consequences for offspring. The evolutionary dynamics of these maternal effects are distinct from those of haploid direct effects under sexual antagonism because the relevant genes are expressed only in females. Despite this, we find the same opportunity for sexually antagonistic polymorphism at the maternal effect locus as at a direct effect locus. Thus, sexually antagonistic maternal effects may underlie some natural genetic variation. The model we present permits alternative interpretations of how the genes are expressed and how the fitness variation is assigned, which invites a theoretical comparison to models of both imprinted genes and sex allocation.     

Self‐fertilization and inbreeding limit the scope for sexually antagonistic polymorphism

Sexual antagonism occurs when there is a positive intersexual genetic correlation in trait expression but opposite fitness effects of the trait(s) in males and females. As such, it constrains the evolution of sexual dimorphism and may therefore have implications for adaptive evolution. There is currently considerable evidence for the existence of sexually antagonistic genetic variation in laboratory and natural populations, but how sexual antagonism interacts with other evolutionary phenomena is still poorly understood in many cases. Here, we explore how self‐fertilization and inbreeding affect the maintenance of polymorphism for sexually antagonistic loci. We expected a priori that selfing should reduce the region of polymorphism, as inbreeding reduces the frequency of heterozygotes and speeds fixation. This expectation was supported, but although previous results suggest that the more an allele that is deleterious to one sex is dominant in that sex, the smaller the region of parameter space that will admit polymorphism, we found that this effect is weakened by self‐fertilization. However, the effect of inbreeding is not strong enough to completely cancel out the effect of dominance: For a given frequency of inbreeding, it will still be the case that the more dominant the alleles are in their deleterious context, the smaller the region of parameter space in which they can exist at polymorphism.     

Genetic correlations and sex‐specific adaptation in changing environments

Females and males have conflicting evolutionary interests. Selection favors the evolution of different phenotypes within each sex, yet divergence between the sexes is constrained by the shared genetic basis of female and male traits. Current theory predicts that such “sexual antagonism” should be common: manifesting rapidly during the process of adaptation, and slow in its resolution. However, these predictions apply in temporally stable environments. Environmental change has been shown empirically to realign the direction of selection acting on shared traits and thereby alleviate signals of sexually antagonistic selection. Yet there remains no theory for how common sexual antagonism should be in changing environments. Here, we analyze models of sex‐specific evolutionary divergence under directional and cyclic environmental change, and consider the impact of genetic correlations on long‐run patterns of sex‐specific adaptation. We find that environmental change often aligns directional selection between the sexes, even when they have divergent phenotypic optima. Nevertheless, some forms of environmental change generate persistent sexually antagonistic selection that is difficult to resolve. Our results reinforce recent empirical observations that changing environmental conditions alleviate conflict between males and females. They also generate new predictions regarding the scope for sexually antagonistic selection and its resolution in changing environments.     

INTRALOCUS SEXUAL CONFLICT OVER IMMUNE DEFENSE,GENDER LOAD,AND SEX‐SPECIFIC SIGNALING IN A NATURAL LIZARD POPULATION

In species with separate sexes, antagonistic selection on males and females (intralocus sexual conflict) can result in a gender load that can be resolved through the evolution of sexual dimorphism. We present data on intralocus sexual conflict over immune defense in a natural population of free‐ranging lizards (Uta stansburiana) and discuss the resolution of this conflict. Intralocus sexual conflict arises from correlational selection between immune defense and orange throat coloration in these lizards. Males with orange throats and high antibody responses had enhanced survival, but the same trait combination reduced female fitness. This sexual antagonism persisted across the life cycle and was concordant between the juvenile and adult life stages. The opposing selective pressure on males and females is ameliorated by a negative intersexual genetic correlation (r_m,f=?0.86) for immune defense. Throat coloration was also genetically correlated with immune defense, but the sign of this genetic correlation differed between the sexes. This resulted in sex‐specific signaling of immunological condition. We also found evidence for a sex‐specific maternal effect on sons with potential to additionally reduce the gender load. These results have implications for signaling evolution, genetic integration between adaptive traits, sex allocation, and mutual mate choice for indirect fitness benefits.     

The geography of sex‐specific selection,local adaptation,and sexual dimorphism

Local adaptation and sexual dimorphism are iconic evolutionary scenarios of intraspecific adaptive differentiation in the face of gene flow. Although theory has traditionally considered local adaptation and sexual dimorphism as conceptually distinct processes, emerging data suggest that they often act concurrently during evolutionary diversification. Here, I merge theories of local adaptation in space and sex‐specific adaptation over time, and show that their confluence yields several new predictions about the roles of context‐specific selection, migration, and genetic correlations, in adaptive diversification. I specifically revisit two influential predictions from classical studies of clinal adaptation and sexual dimorphism: (1) that local adaptation should decrease with distance from the species’ range center and (2) that opposing directional selection between the sexes (sexual antagonism) should inevitably accompany the evolution of sexual dimorphism. I show that both predictions can break down under clinally varying selection. First, the geography of local adaptation can be sexually dimorphic, with locations of relatively high local adaptation differing profoundly between the sexes. Second, the intensity of sexual antagonism varies across the species’ range, with subpopulations near the range center representing hotspots for antagonistic selection. The results highlight the context‐dependent roles of migration versus sexual conflict as primary constraints to adaptive diversification.     

Meiotic drive influences the outcome of sexually antagonistic selection at a linked locus

Most meiotic drivers, such as the t‐haplotype in Mus and the segregation distorter (SD) in Drosophila, act in a sex‐specific manner, gaining a transmission advantage through one sex although suffering only the fitness costs associated with the driver in the other. Their inheritance is thus more likely through one of the two sexes, a property they share with sexually antagonistic alleles. Previous theory has shown that pairs of linked loci segregating for sexually antagonistic alleles are more likely to remain polymorphic and that linkage disequilibrium accrues between them. I probe this similarity between drive and sexual antagonism and examine the evolution of chromosomes experiencing these selection pressures simultaneously. Reminiscent of previous theory, I find that: the opportunity for polymorphism increases for a sexually antagonistic locus that is physically linked to a driving locus; the opportunity for polymorphism at a driving locus also increases when linked to a sexually antagonistic locus; and stable linkage disequilibrium accompanies any polymorphic equilibrium. Additionally, I find that drive at a linked locus favours the fixation of sexually antagonistic alleles that benefit the sex in which drive occurs. Further, I show that under certain conditions reduced recombination between these two loci is selectively favoured. These theoretical results provide clear, testable predictions about the nature of sexually antagonistic variation on driving chromosomes and have implications for the evolution of genomic architecture.     

Multivariate intralocus sexual conflict in seed beetles

Intralocus sexual conflict (IaSC) is pervasive because males and females experience differences in selection but share much of the same genome. Traits with integrated genetic architecture should be reservoirs of sexually antagonistic genetic variation for fitness, but explorations of multivariate IaSC are scarce. Previously, we showed that upward artificial selection on male life span decreased male fitness but increased female fitness compared with downward selection in the seed beetle Callosobruchus maculatus. Here, we use these selection lines to investigate sex‐specific evolution of four functionally integrated traits (metabolic rate, locomotor activity, body mass, and life span) that collectively define a sexually dimorphic life‐history syndrome in many species. Male‐limited selection for short life span led to correlated evolution in females toward a more male‐like multivariate phenotype. Conversely, males selected for long life span became more female‐like, implying that IaSC results from genetic integration of this suite of traits. However, while life span, metabolism, and body mass showed correlated evolution in the sexes, activity did not evolve in males but, surprisingly, did so in females. This led to sexual monomorphism in locomotor activity in short‐life lines associated with detrimental effects in females. Our results thus support the general tenet that widespread pleiotropy generates IaSC despite sex‐specific genetic architecture.     

Sex‐specific recombination rates and allele frequencies affect the invasion of sexually antagonistic variation on autosomes

The introduction and persistence of novel, sexually antagonistic alleles can depend upon factors that differ between males and females. Understanding the conditions for invasion in a two‐locus model can elucidate these processes. For instance, selection can act differently upon the sexes, or sex linkage can facilitate the invasion of genetic variation with opposing fitness effects between the sexes. Two factors that deserve further attention are recombination rates and allele frequencies – both of which can vary substantially between the sexes. We find that sex‐specific recombination rates in a two‐locus diploid model can affect the invasion outcome of sexually antagonistic alleles and that the sex‐averaged recombination rate is not necessarily sufficient to predict invasion. We confirm that the range of permissible recombination rates is smaller in the sex benefitting from invasion and larger in the sex harmed by invasion. However, within the invasion space, male recombination rate can be greater than, equal to or less than female recombination rate in order for a male‐benefit, female‐detriment allele to invade (and similarly for a female‐benefit, male‐detriment allele). We further show that a novel, sexually antagonistic allele that is also associated with a lowered recombination rate can invade more easily when present in the double heterozygote genotype. Finally, we find that sexual dimorphism in resident allele frequencies can impact the invasion of new sexually antagonistic alleles at a second locus. Our results suggest that accounting for sex‐specific recombination rates and allele frequencies can determine the difference between invasion and non‐invasion of novel, sexually antagonistic alleles in a two‐locus model.     

Field estimates of parentage reveal sexually antagonistic selection on body size in a population of Anolis lizards

Sexual dimorphism evolves when selection favors different phenotypic optima between the sexes. Such sexually antagonistic selection creates intralocus sexual conflict when traits are genetically correlated between the sexes and have sex‐specific optima. Brown anoles are highly sexually dimorphic: Males are on average 30% longer than females and 150% heavier in our study population. Viability selection on body size is known to be sexually antagonistic, and directional selection favors large male size whereas stabilizing selection constrains females to remain small. We build on previous studies of viability selection by measuring sexually antagonistic selection using reproductive components of fitness over three generations in a natural population of brown anoles. We estimated the number of offspring produced by an individual that survived to sexual maturity (termed RS^V), a measure of individual fitness that includes aspects of both individual reproductive success and offspring survival. We found directional selection on male body size, consistent with previous studies of viability selection. However, selection on female body size varied among years, and included periods of positive directional selection, quadratic stabilizing selection, and no selection. Selection acts differently in the sexes based on both survival and reproduction and sexual conflict appears to be a persistent force in this species.     

FITNESS VARIATION DUE TO SEXUAL ANTAGONISM AND LINKAGE DISEQUILIBRIUM

Extensive fitness variation for sexually antagonistic characters has been detected in nature. However, current population genetic theory suggests that sexual antagonism is unlikely to play a major role in the maintenance of variation. We present a two‐locus model of sexual antagonism that is capable of explaining greater fitness variance at equilibrium than previous single‐locus models. The second genetic locus provides additional fitness variance in two complementary ways. First, linked loci can maintain gene variants that are lost in single‐locus models of evolution, expanding the opportunity for polymorphism. Second, linkage disequilibrium results between any two sexually antagonistic genes, producing an excess of high‐ and low‐fitness haplotypes. Our results uncover a unique contribution of conflicting selection pressures to the maintenance of variation, which simpler models that neglect genetic architecture overlook.     

Partitioning of resources: the evolutionary genetics of sexual conflict over resource acquisition and allocation

Fitness depends on both the resources that individuals acquire and the allocation of those resources to traits that influence survival and reproduction. Optimal resource allocation differs between females and males as a consequence of their fundamentally different reproductive strategies. However, because most traits have a common genetic basis between the sexes, conflicting selection between the sexes over resource allocation can constrain the evolution of optimal allocation within each sex, and generate trade‐offs for fitness between them (i.e. ‘sexual antagonism’ or ‘intralocus sexual conflict’). The theory of resource acquisition and allocation provides an influential framework for linking genetic variation in acquisition and allocation to empirical evidence of trade‐offs between distinct life‐history traits. However, these models have not considered the emergence of trade‐offs within the context of sexual dimorphism, where they are expected to be particularly common. Here, we extend acquisition–allocation theory and develop a quantitative genetic framework for predicting genetically based trade‐offs between life‐history traits within sexes and between female and male fitness. Our models demonstrate that empirically measurable evidence of sexually antagonistic fitness variation should depend upon three interacting factors that may vary between populations: (1) the genetic variances and between‐sex covariances for resource acquisition and allocation traits, (2) condition‐dependent expression of resource allocation traits and (3) sex differences in selection on the allocation of resource to different fitness components.     

Sexual selection on spontaneous mutations strengthens the between‐sex genetic correlation for fitness

A proposed benefit to sexual selection is that it promotes purging of deleterious mutations from populations. For this benefit to be realized, sexual selection, which is usually stronger on males, must purge mutations deleterious to both sexes. Here, we experimentally test the hypothesis that sexual selection on males purges deleterious mutations that affect both male and female fitness. We measured male and female fitness in two panels of spontaneous mutation‐accumulation lines of the fly, Drosophila serrata, each established from a common ancestor. One panel of mutation accumulation lines limited both natural and sexual selection (LS lines), whereas the other panel limited natural selection, but allowed sexual selection to operate (SS lines). Although mutation accumulation caused a significant reduction in male and female fitness in both the LS and SS lines, sexual selection had no detectable effect on the extent of the fitness reduction. Similarly, despite evidence of mutational variance for fitness in males and females of both treatments, sexual selection had no significant impact on the amount of mutational genetic variance for fitness. However, sexual selection did reshape the between‐sex correlation for fitness: significantly strengthening it in the SS lines. After 25 generations, the between‐sex correlation for fitness was positive but considerably less than one in the LS lines, suggesting that, although most mutations had sexually concordant fitness effects, sex‐limited, and/or sex‐biased mutations contributed substantially to the mutational variance. In the SS lines this correlation was strong and could not be distinguished from unity. Individual‐based simulations that mimick the experimental setup reveal two conditions that may drive our results: (1) a modest‐to‐large fraction of mutations have sex‐limited (or highly sex‐biased) fitness effects, and (2) the average fitness effect of sex‐limited mutations is larger than the average fitness effect of mutations that affect both sexes similarly.     

The consequences of facultative sex in a prey adapting to predation

A species reproductive mode, along with its associated costs and benefits, can play a significant role in its evolution and survival. Facultative sexuality, being able to reproduce both sexually and asexually, has been deemed evolutionary favourable as the benefits of either mode may be fully realized. In fact, many studies have focused on identifying the benefits of sex and/or the forces selecting for increased rates of sex using facultative sexual species. The costs of either mode, however, can also have a profound impact on a population's evolutionary trajectory. Here, we used experimental evolution and fitness assays to investigate the consequences of facultative sexuality in prey adapting to predation. Specifically, we compared the adaptive response of algal prey populations exposed to constant rotifer predation and which had alternating cycles of asexual and sexual reproduction where sexual episodes were either facultative (sexual and asexual progeny simultaneously propagated) or obligate (only sexual progeny propagated). We found that prey populations with facultative sexual episodes reached a lower final relative fitness and suffered a greater trade‐off in traits under selection, that is defence and competitive ability, as compared to prey populations with obligate sexual episodes. Our results suggest that costs associated with sexual reproduction (germination time) and asexual reproduction (selection interference) were amplified in the facultative sexual prey populations, leading to a reduction in the net advantage of sexuality. Additionally, we found evidence that the cost of sex was reduced in the obligate sexual prey populations because increased selection for sex was observed via the spontaneous production of sexual cells. These results show that certain costs associated with facultative sexuality can affect an organism's evolutionary trajectory.     

Perspective: sexual conflict and sexual selection: chasing away paradigm shifts

Abstract.— Traditional models of sexual selection propose that partner choice increases both average male and average female fitness in a population. Recent theoretical and empirical work, however, has stressed that sexual conflict may be a potent broker of sexual selection. When the fitness interests of males and females diverge, a reproductive strategy that increases the fitness of one sex may decrease the fitness of the other sex. The chase-away hypothesis proposes that sexual conflict promotes sexually antagonistic, rather than mutualistic, coevolution, whereby manipulative reproductive strategies in one sex are counteracted by the evolution of resistance to such strategies in the other sex. In this paper, we consider the criteria necessary to demonstrate the chase-away hypothesis. Specifically, we review sexual conflict with particular emphasis on the chase-away hypothesis; discuss the problems associated with testing the predictions of the chase-away hypothesis and the extent to which these predictions and the predictions of traditional models of sexual selection are mutually exclusive; discuss misconceptions and mismeasures of sexual conflict; and suggest an alternative approach to demonstrate sexual conflict, measure the intensity of sexually antagonistic selection in a population, and elucidate the coevolutionary trajectories of the sexes.     

Direct benefits of choosing a high‐fitness mate can offset the indirect costs associated with intralocus sexual conflict

Intralocus sexual conflict generates a cost to mate choice: high‐fitness partners transmit genetic variation that confers lower fitness to offspring of the opposite sex. Our earlier work in the fruit fly, Drosophila melanogaster, revealed that these indirect genetic costs were sufficient to reverse potential “good genes” benefits of sexual selection. However, mate choice can also confer direct fitness benefits by inducing larger numbers of progeny. Here, we consider whether direct benefits through enhanced fertility could offset the costs associated with intralocus sexual conflict in D. melanogaster. Using hemiclonal analysis, we found that females mated to high‐fitness males produced 11% more offspring compared to those mated to low‐fitness males, and high‐fitness females produced 34% more offspring than low‐fitness females. These direct benefits more than offset the reduction in offspring fitness caused by intralocus sexual conflict, creating a net fitness benefit for each sex to pairing with a high‐fitness partner. Our findings highlight the need to consider both direct and indirect effects when investigating the fitness impacts of mate choice. Direct fitness benefits may shelter sexually antagonistic alleles from selection, suggesting a novel mechanism for the maintenance of fitness variation.     

SEXUAL SELECTION AND THE EVOLUTION OF SEXUAL SIZE DIMORPHISM IN THE WATER STRIDER,AQUARIUS REMIGIS

Sexual size dimorphism (SSD) is often attributed to sexual selection, particularly when males are the larger sex. However, sexual selection favoring large males is common even in taxa where females are the larger sex, and is therefore not a sufficient explanation of patterns of SSD. As part of a more extensive study of the evolution of SSD in water striders (Heteroptera, Gerridae), we examine patterns of sexual selection and SSD in 12 populations of Aquarius remigis. We calculate univariate and multivariate selection gradients from samples of mating and single males, for two sexually dimorphic traits (total length and profemoral width) and two sexually monomorphic traits (mesofemoral length and wing form). The multivariate analyses reveal strong selection favoring larger males, in spite of the female-biased SSD for this trait, and weaker selection favoring aptery and reduced mesofemoral length. Selection is weakest on the most dimorphic trait, profemoral width, and is stabilizing rather than directional. The pattern of sexual selection on morphological traits is therefore not concordant with the pattern of SSD. The univariate selection gradients reveal little net selection (direct + indirect) on any of the traits, and suggest that evolution away from the plesiomorphic pattern of SSD is constrained by antagonistic patterns of selection acting on this suite of positively correlated morphological traits. We hypothesize that SSD in A. remigis is not in equilibrium, a hypothesis that is consistent with both theoretical models of the evolution of SSD and our previous studies of allometry for SSD. A negative interpopulation correlation between the intensity of sexual selection and the operational sex ratio supports the hypothesis that, as in several other water strider species, sexual selection in A. remigis occurs through generalized female reluctance rather than active female choice. The implications of this for patterns of sexual selection are discussed.     

The microevolutionary response to male‐limited X‐chromosome evolution in Drosophila melanogaster reflects macroevolutionary patterns

Due to its hemizygous inheritance and role in sex determination, the X‐chromosome is expected to play an important role in the evolution of sexual dimorphism and to be enriched for sexually antagonistic genetic variation. By forcing the X‐chromosome to only be expressed in males over >40 generations, we changed the selection pressures on the X to become similar to those experienced by the Y. This releases the X from any constraints arising from selection in females and should lead to specialization for male fitness, which could occur either via direct effects of X‐linked loci or trans‐regulation of autosomal loci by the X. We found evidence of masculinization via up‐regulation of male‐benefit sexually antagonistic genes and down‐regulation of X‐linked female‐benefit genes. Potential artefacts of the experimental evolution protocol are discussed and cannot be wholly discounted, leading to several caveats. Interestingly, we could detect evidence of microevolutionary changes consistent with previously documented macroevolutionary patterns, such as changes in expression consistent with previously established patterns of sexual dimorphism, an increase in the expression of metabolic genes related to mito‐nuclear conflict and evidence that dosage compensation effects can be rapidly altered. These results confirm the importance of the X in the evolution of sexual dimorphism and as a source for sexually antagonistic genetic variation and demonstrate that experimental evolution can be a fruitful method for testing theories of sex chromosome evolution.