Intralocus sexual conflict for fitness: sexually antagonistic alleles for testosterone

Intralocus sexual conflict occurs when a trait encoded by the same genetic locus in the two sexes has different optima in males and females. Such conflict is widespread across taxa, however, the shared phenotypic traits that mediate the conflict are largely unknown. We examined whether the sex hormone, testosterone (T), that controls sexual differentiation, contributes to sexually antagonistic fitness variation in the bank vole, Myodes glareolus. We compared (opposite-sex) sibling reproductive fitness in the bank vole after creating divergent selection lines for T. This study shows that selection for T was differentially associated with son versus daughter reproductive success, causing a negative correlation in fitness between full siblings. Our results demonstrate the presence of intralocus sexual conflict for fitness in this small mammal and that sexually antagonistic selection is acting on T. We also found a negative correlation in fitness between parents and their opposite-sex progeny (e.g. father-daughter), highlighting a dilemma for females, as the indirect genetic benefits of selecting reproductively successful males (high T) are lost with daughters. We discuss mechanisms that may mitigate this disparity between progeny quality.     

Intralocus sexual conflict,adaptive sex allocation,and the heritability of fitness

Intralocus sexual conflict arises when selection favours alternative fitness optima in males and females. Unresolved conflict can create negative between‐sex genetic correlations for fitness, such that high‐fitness parents produce high‐fitness progeny of their same sex, but low‐fitness progeny of the opposite sex. This cost of sexual conflict could be mitigated if high‐fitness parents bias sex allocation to produce more offspring of their same sex. Previous studies of the brown anole lizard (Anolis sagrei) show that viability selection on body size is sexually antagonistic, favouring large males and smaller females. However, sexual conflict over body size may be partially mitigated by adaptive sex allocation: large males sire more sons than daughters, whereas small males sire more daughters than sons. We explored the evolutionary implications of these phenomena by assessing the additive genetic (co)variance of fitness within and between sexes in a wild population. We measured two components of fitness: viability of adults over the breeding season, and the number of their progeny that survived to sexual maturity, which includes components of parental reproductive success and offspring viability (RS^V). Viability of parents was not correlated with adult viability of their sons or daughters. RS^V was positively correlated between sires and their offspring, but not between dams and their offspring. Neither component of fitness was significantly heritable, and neither exhibited negative between‐sex genetic correlations that would indicate unresolved sexual conflict. Rather, our results are more consistent with predictions regarding adaptive sex allocation in that, as the number of sons produced by a sire increased, the adult viability of his male progeny increased.     

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.     

Intralocus sexual conflict over human height

Intralocus sexual conflict (IASC) occurs when a trait under selection in one sex constrains the other sex from achieving its sex-specific fitness optimum. Selection pressures on body size often differ between the sexes across many species, including humans: among men individuals of average height enjoy the highest reproductive success, while shorter women have the highest reproductive success. Given its high heritability, IASC over human height is likely. Using data from sibling pairs from the Wisconsin Longitudinal Study, we present evidence for IASC over height: in shorter sibling pairs (relatively) more reproductive success (number of children) was obtained through the sister than through the brother of the sibling pair. By contrast, in average height sibling pairs most reproductive success was obtained through the brother relative to the sister. In conclusion, we show that IASC over a heritable, sexually dimorphic physical trait (human height) affects Darwinian fitness in a contemporary human population.     

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.     

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.     

SEXUAL CONFLICT AND SEXUAL SELECTION: MEASURING ANTAGONISTIC COEVOLUTION

Abstract Arnqvist (2004) raises some concerns with several of the points made by Pizzari and Snook (2003) on the study of sexually antagonistic coevolution (SAC) generated by sexual conflict, arguing that: (1) sexual conflict cannot be expressed in terms of average male and female fitness; (2) our criticism of current experimental approaches, particularly interpopulation crosses, is unjustified; and (3) the alternative experimental approach we proposed is problematic. Here we discuss and respond to these criticisms by: (1) clarifying that we can distinguish between SAC and mutualistic sexual coevolution by measuring changes in the average fitness of the reproducing subsamples of males and females of a population across generations, (2) maintaining that testing SAC using interpopulation crosses is undermined by the lack of a priori knowledge of what traits mediate SAC across isolated populations, and (3) reinforcing the advantages of our experimental approach to distinguish between sexually mutualistic and antagonistic selection.     

The consequences of sexual selection in well‐adapted and maladapted populations of bean beetles†

Whether sexual selection generally promotes or impedes population persistence remains an open question. Intralocus sexual conflict (IaSC) can render sexual selection in males detrimental to the population by increasing the frequency of alleles with positive effects on male reproductive success but negative effects on female fecundity. Recent modeling based on fitness landscape theory, however, indicates that the relative impact of IaSC may be reduced in maladapted populations and that sexual selection therefore might promote adaptation when it is most needed. Here, we test this prediction using bean beetles that had undergone 80 generations of experimental evolution on two alternative host plants. We isolated and assessed the effect of maladaptation on sex‐specific strengths of selection and IaSC by cross‐rearing the two experimental evolution regimes on the alternative hosts and estimating within‐population genetic (co)variance for fitness in males and females. Two key predictions were upheld: males generally experienced stronger selection compared to females and maladaptation increased selection in females. However, maladaptation consistently decreased male‐bias in the strength of selection and IaSC was not reduced in maladapted populations. These findings imply that sexual selection can be disrupted in stressful environmental conditions, thus reducing one of the potential benefits of sexual reproduction in maladapted populations.     

FITNESS CONSEQUENCES OF SEX‐SPECIFIC SELECTION

Theory suggests that sex‐specific selection can facilitate adaptation in sexually reproducing populations. However, sexual conflict theory and recent experiments indicate that sex‐specific selection is potentially costly due to sexual antagonism: alleles harmful to one sex can accumulate within a population because they are favored in the other sex. Whether sex‐specific selection provides a net fitness benefit or cost depends, in part, on the relative frequency and strength of sexually concordant versus sexually antagonistic selection throughout a species’ genome. Here, we model the net fitness consequences of sex‐specific selection while explicitly considering both sexually concordant and sexually antagonistic selection. The model shows that, even when sexual antagonism is rare, the fitness costs that it imposes will generally overwhelm fitness benefits of sexually concordant selection. Furthermore, the cost of sexual antagonism is, at best, only partially resolved by the evolution of sex‐limited gene expression. To evaluate the key parameters of the model, we analyze an extensive dataset of sex‐specific selection gradients from wild populations, along with data from the experimental evolution literature. The model and data imply that sex‐specific selection may likely impose a net cost on sexually reproducing species, although additional research will be required to confirm this conclusion.     

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.     

Sexual reproduction and diversity: Connection between sexual selection and biological communities via population dynamics

Sexual reproduction is a mysterious phenomenon. Most animals and plants invest in sexual reproduction, even though it is more costly than asexual reproduction. Theoretical studies suggest that occasional or conditional use of sexual reproduction, involving facultative switching between sexual and asexual reproduction, is the optimal reproductive strategy. However, obligate sexual reproduction is common in nature. Recent studies suggest that the evolution of facultative sexual reproduction is prevented by males that coerce females into sexual fertilization; thus, sexual reproduction has the potential to enforce costs on a given species. Here, the effect of sex on biodiversity is explored by evaluating the reproductive costs arising from sex. Sex provides atypical selection pressure that favors traits that increase fertilization success, even at the expense of population growth rates, that is, sexual selection. The strength of sexual selection depends on the density of a given species. Sexual selection often causes strong negative effects on the population growth rates of species that occur at high density. Conversely, a species that reduces its density is released from this negative effect, and so increases its growth rate. Thus, this negative density-dependent effect on population growth that arises from sexual selection could be used to rescue endangered species from extinction, prevent the overgrowth of common species and promote the coexistence of competitive species. Recent publications on sexual reproduction provide several predictions related to the evolution of reproductive strategies, which is an important step toward integrating evolutionary dynamics, demographic dynamics and community dynamics.     

Sexual selection and the evolution of secondary sexual traits: sex comb evolution in Drosophila

Sexual selection can drive rapid evolutionary change in reproductive behaviour, morphology and physiology. This often leads to the evolution of sexual dimorphism, and continued exaggerated expression of dimorphic sexual characteristics, although a variety of other alternative selection scenarios exist. Here, we examined the evolutionary significance of a rapidly evolving, sexually dimorphic trait, sex comb tooth number, in two Drosophila species. The presence of the sex comb in both D. melanogaster and D. pseudoobscura is known to be positively related to mating success, although little is yet known about the sexually selected benefits of sex comb structure. In this study, we used experimental evolution to test the idea that enhancing or eliminating sexual selection would lead to variation in sex comb tooth number. However, the results showed no effect of either enforced monogamy or elevated promiscuity on this trait. We discuss several hypotheses to explain the lack of divergence, focussing on sexually antagonistic coevolution, stabilizing selection via species recognition and nonlinear selection. We discuss how these are important, but relatively ignored, alternatives in understanding the evolution of rapidly evolving sexually dimorphic traits.     

Does reproductive isolation evolve faster in larger populations via sexually antagonistic coevolution?

Sexual conflict over reproductive investment can lead to sexually antagonistic coevolution and reproductive isolation. It has been suggested that, unlike most models of allopatric speciation, the evolution of reproductive isolation through sexually antagonistic coevolution will occur faster in large populations as these harbour greater levels of standing genetic variation, receive larger numbers of mutations and experience more intense sexual selection. We tested this in bruchid beetle populations (Callosobruchus maculatus) by manipulating population size and standing genetic variability in replicated lines derived from founders that had been released from sexual conflict for 90 generations. We found that after 19 generations of reintroduced sexual conflict, none of our treatments had evolved significant overall reproductive isolation among replicate lines. However, as predicted, measures of reproductive isolation tended to be greater among larger populations. We discuss our methodology, arguing that reproductive isolation is best examined by performing a matrix of allopatric and sympatric crosses whereas measurement of divergence requires crosses with a tester line.     

The sexually-selected sperm hypothesis: sex-biased inheritance and sexual antagonism

When females are inseminated by more than one male (polyandry) sexual selection continues after insemination in the form of sperm competition and cryptic female choice. The sexually-selected sperm hypothesis proposes that, under the risk of sperm competition, additive variation in male traits determining fertilising efficiency will select for female propensity to be polyandrous in order to increase the probability of producing sons with superior fertilising efficiency. Two factors complicate this prediction: sex-biased transmission of male fertilising efficiency traits and sexual antagonism of sex-limited traits, fostered by sex-biased inheritance. Here, we (i) review the evidence that male traits contributing towards fertilising efficiency are heritable through sex-biased mechanisms, and (ii) explore the evolutionary implications for male and female reproductive strategies caused by both sex-biased transmission and sexual antagonism of fertilising efficiency traits. Many male fertilising efficiency traits are heritable through sex-biased mechanisms and may not necessarily increase female fitness. The predictions of the sexually-selected sperm hypothesis change dramatically under these different mechanisms of inheritance of fertilising efficiency traits, and different fitness pay-offs derived by females from the expression of such traits. Both sex-biased control of fertilising efficiency and sexual antagonism may also be important in explaining the maintenance of the genetic variance and selection potential of fertilising efficiency. We propose that a useful approach to test the sexually-selected sperm hypothesis is to combine studies which identify behavioural and physiological mechanisms explaining variation in reproductive success with artificial selection experiments to infer the underlying evolutionary patterns.     

The resolution of sexual antagonism by gene duplication

Disruptive selection between males and females can generate sexual antagonism, where alleles improving fitness in one sex reduce fitness in the other. This type of genetic conflict arises because males and females carry nearly identical sets of genes: opposing selection, followed by genetic mixing during reproduction, generates a population genetic "tug-of-war" that constrains adaptation in either sex. Recent verbal models suggest that gene duplication and sex-specific cooption of paralogs might resolve sexual antagonism and facilitate evolutionary divergence between the sexes. However, this intuitive proximal solution for sexual dimorphism potentially belies a complex interaction between mutation, genetic drift, and positive selection during duplicate fixation and sex-specific paralog differentiation. The interaction of these processes--within the explicit context of duplication and sexual antagonism--has yet to be formally described by population genetics theory. Here, we develop and analyze models of gene duplication and sex-specific differentiation between paralogs. We show that sexual antagonism can favor the fixation and maintenance of gene duplicates, eventually leading to the evolution of sexually dimorphic genetic architectures for male and female traits. The timescale for these evolutionary transitions is sensitive to a suite of genetic and demographic variables, including allelic dominance, recombination, sex linkage, and population size. Interestingly, we find that female-beneficial duplicates preferentially accumulate on the X chromosome, whereas male-beneficial duplicates are biased toward autosomes, independent of the dominance parameters of sexually antagonistic alleles. Although this result differs from previous models of sexual antagonism, it is consistent with several findings from the empirical genomics literature.     

Intra-locus sexual conflict and sexually antagonistic genetic variation in hermaphroditic animals

Intra-locus sexual conflict results when sex-specific selection pressures for a given trait act against the intra-sexual genetic correlation for that trait. It has been found in a wide variety of taxa in both laboratory and natural populations, but the importance of intra-locus sexual conflict and sexually antagonistic genetic variation in hermaphroditic organisms has rarely been considered. This is not so surprising given the conceptual and theoretical association of intra-locus sexual conflict with sexual dimorphism, but there is no a priori reason why intra-locus sexual conflict cannot occur in hermaphroditic organisms as well. Here, I discuss the potential for intra-locus sexual conflict in hermaphroditic animals and review the available evidence for such conflict, and for the existence of sexually antagonistic genetic variation in hermaphrodites. I argue that mutations with asymmetric effects are particularly likely to be important in mediating sexual antagonism in hermaphroditic organisms. Moreover, sexually antagonistic genetic variation is likely to play an important role in inter-individual variation in sex allocation and in transitions to and from gonochorism (separate sexes) in simultaneous hermaphrodites. I also describe how sequential hermaphrodites may experience a unique form of intra-locus sexual conflict via antagonistic pleiotropy. Finally, I conclude with some suggestions for further research.     

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.     

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.     

Assessing the extent of genome-wide intralocus sexual conflict via experimentally enforced gender-limited selection

Intralocus sexual conflict, which occurs when a trait is selected in opposite directions in the two sexes, is a taxonomically widespread phenomenon. The strongest genetic evidence for a gender load due to intralocus sexual conflict comes from the Drosophila melanogaster laboratory model system, in which a negative genetic correlation between male and female lifetime fitness has been observed. Here, using a D. melanogaster model system, we utilize a novel modification of the 'middle class neighbourhood' design to relax selection in one sex, while maintaining selection in the other. After 26 generations of asymmetrical selection, we observed the expected drop in fitness of the non-selected sex compared to that of the selected sex, consistent with previous studies of intralocus sexual conflict in this species. However, the fitness of the selected sex also dropped compared to the base population. The overall decline in fitness of both the selected and the unselected sex indicates that most new mutations are harmful to both sexes, causing recurrent mutation to build a positive genetic correlation for fitness between the sexes. However, the steeper decay in the fitness of the unselected sex indicates that a substantial number of mutations are gender-limited in expression or sexually antagonistic. Our experiment cannot definitively resolve these two possibilities, but we use recent genomic data and results from previous studies to argue that sexually antagonistic alleles are the more likely explanation.