Sexual conflict in viscous populations: The effect of the timing of dispersal

In recent years, there has been increasing theoretical and empirical examination of how sexual conflict can arise between males and females. However, much this work has implicitly assumed that interactions take place in panmictic populations with complete dispersal, where interactions are between unrelated individuals. Here, we examine the consequences of limited dispersal and population structure for the evolution of a male phenotype that is associated with the males pre- and post-copulatory reproductive success, using an inclusive-fitness based analysis applied to group-structured populations. We show that: (i) the sex-specific timing of the dispersal phase of the life cycle can drive the evolution of sexual conflict; (ii) the inclusive fitness of a female in this conflict is determined solely by direct (i.e. personal) effects on its own competitive ability. Our analysis is supported by results from individual-based simulations of multi-level selection. Our results support the suggestion that kin selection can influence the evolution of sexual conflict, but reveal that such a role might be more complex than previously appreciated when sex-specific life histories are taken into consideration. We discuss the implications of our results for sexual conflict in various species of insects, but focus primarily on dipteran flies of the family Sepsidae.     

Sexual conflict in viscous populations: the effect of the timing of dispersal

In recent years, there has been increasing theoretical and empirical examination of how sexual conflict can arise between males and females. However, much this work has implicitly assumed that interactions take place in panmictic populations with complete dispersal, where interactions are between unrelated individuals. Here, we examine the consequences of limited dispersal and population structure for the evolution of a male phenotype that is associated with the males pre- and post-copulatory reproductive success, using an inclusive-fitness based analysis applied to group-structured populations. We show that: (i) the sex-specific timing of the dispersal phase of the life cycle can drive the evolution of sexual conflict; (ii) the inclusive fitness of a female in this conflict is determined solely by direct (i.e. personal) effects on its own competitive ability. Our analysis is supported by results from individual-based simulations of multi-level selection. Our results support the suggestion that kin selection can influence the evolution of sexual conflict, but reveal that such a role might be more complex than previously appreciated when sex-specific life histories are taken into consideration. We discuss the implications of our results for sexual conflict in various species of insects, but focus primarily on dipteran flies of the family Sepsidae.     

No evidence that experimental manipulation of sexual conflict drives premating reproductive isolation in Drosophila melanogaster

Theoretical models predict that sexual conflict can drive reproductive isolation by decreasing the probability of matings between individuals from allopatric populations. A recent study in dung flies supported this prediction. To test the generality of this finding we used replicate lines of Drosophila melanogaster that had been selected under high, medium and low levels of sexual conflict, in which the females had evolved differences in their level of resistance to male-induced harm. We compared the proportion of virgin pairs that mated by set time points, for flies from the same replicate within each sexual conflict level vs. flies from different replicates within each sexual conflict level. The results did not support the prediction that, in D. melanogaster, sexual conflict drives population divergence via changes in female willingness to mate. The results were unlikely to be explained by differential inbreeding or by a lack of response to sexual conflict.     

Post-copulatory sexual selection and female fitness in Scathophaga stercoraria

Whether sexual selection increases or decreases female fitness is determined by the occurrence and relative importance of sexual-conflict processes and the ability of females to choose high-quality males. Experimentally enforced polyandry and monogamy have previously been shown to cause rapid evolution in the yellow dung fly Scathophaga stercoraria. Flies from polyandrous lines invested more in reproductive tissue, and this investment influenced paternity in sperm competition, but came at a cost to immune function. While some fitness consequences of enforced polyandry or monogamy have been examined when flies mate multiply, the consequences for female fitness when singly copulated remain unexplored. Under a good-genes scenario females from polyandrous lines should be of higher general quality and should outperform females from monogamous lines even with a single copulation. Under sexual conflict, costly adaptations will afford no advantages when females are allowed to mate only once. We investigate the lifetime reproductive success and longevity of females evolving under enforced monogamy or polyandry when mating once with males from these selection regimes. Females from polyandrous lines were found to have lower fitness than their monogamous counterparts when mating once. They died earlier and produced significantly fewer eggs and offspring. These results suggest that sexual conflict probably drove evolution under enforced polyandry as female fitness did not increase overall as expected with purely good-genes effects.     

Populations with elevated mutation load do not benefit from the operation of sexual selection

Theory predicts that if most mutations are deleterious to both overall fitness and condition-dependent traits affecting mating success, sexual selection will purge mutation load and increase nonsexual fitness. We explored this possibility with populations of mutagenized Drosophila melanogaster exhibiting elevated levels of deleterious variation and evolving in the presence or absence of male-male competition and female choice. After 60 generations of experimental evolution, monogamous populations exhibited higher total reproductive output than polygamous populations. Parental environment also affected fitness measures - flies that evolved in the presence of sexual conflict showed reduced nonsexual fitness when their parents experienced a polygamous environment, indicating trans-generational effects of male harassment and highlighting the importance of a common garden design. This cost of parental promiscuity was nearly absent in monogamous lines, providing evidence for the evolution of reduced sexual antagonism. There was no overall difference in egg-to-adult viability between selection regimes. If mutation load was reduced by the action of sexual selection in this experiment, the resultant gain in fitness was not sufficient to overcome the costs of sexual antagonism.     

Experimental evolution exposes female and male responses to sexual selection and conflict in Tribolium castaneum

Between-individual variance in potential reproductive rate theoretically creates a load in reproducing populations by driving sexual selection of male traits for winning competitions, and female traits for resisting the costs of multiple mating. Here, using replicated experimental evolution under divergent operational sex ratios (OSR, 9:1 or 1:6 ♀:♂) we empirically identified the parallel reproductive fitness consequences for females and males in the promiscuous flour beetle Tribolium castaneum. Our results revealed clear evidence that sexual conflict resides within the T. castaneum mating system. After 20 generations of selection, females from female-biased OSRs became vulnerable to multiple mating, and showed a steep decrease in reproductive fitness with an increasing number of control males. In contrast, females from male-biased OSRs showed no change in reproductive fitness, irrespective of male numbers. The divergence in reproductive output was not explained by variation in female mortality. Parallel assays revealed that males also responded to experimental evolution: individuals from male-biased OSRs obtained 27% greater reproductive success across 7-day competition for females with a control male rival, compared to males from the female-biased lines. Subsequent assays suggest that these differences were not due to postcopulatory sperm competitiveness, but to precopulatory/copulatory competitive male mating behavior.     

No evidence for divergence in male harmfulness or female resistance in response to changes in the opportunity for dispersal

The outcome of sexual conflict can depend on the social environment, as males respond to changes in the inclusive fitness payoffs of harmfulness and harm females less when they compete with familiar relatives. Theoretical models also predict that if limited male dispersal predictably enhances local relatedness while maintaining global competition, kin selection can produce evolutionary divergences in male harmfulness among populations. Experimental tests of these predictions, however, are rare. We assessed rates of dispersal in female and male seed beetles Callosobruchus maculatus, a model species for studies of sexual conflict, in an experimental setting. Females dispersed significantly more often than males, but dispersing males travelled just as far as dispersing females. Next, we used experimental evolution to test whether limiting dispersal allowed the action of kin selection to affect divergence in male harmfulness and female resistance. Populations of C. maculatus were evolved for 20 and 25 generations under one of three dispersal regimens: completely free dispersal, limited dispersal and no dispersal. There was no divergence among treatments in female reproductive tract scarring, ejaculate size, mating behaviour, fitness of experimental females mated to stock males or fitness of stock females mated to experimental males. We suggest that this is likely due to insufficient strength of kin selection rather than a lack of genetic variation or time for selection. Limited dispersal alone is therefore not sufficient for kin selection to reduce male harmfulness in this species, consistent with general predictions that limited dispersal will only allow kin selection if local relatedness is independent of the intensity of competition among kin.     

Sexual conflict and environmental change: trade-offs within and between the sexes during the evolution of desiccation resistance

Intralocus sexual conflict occurs when males and females experience sex-specific selection on a shared genome. With several notable exceptions, intralocus sexual conflict has been investigated in constant environments to which the study organisms have had an opportunity to adapt. However, a change in the environment can result in differential or even opposing selection pressures on males and females, creating sexual conflict. We used experimental evolution to explore the interaction between intralocus sexual conflict, sexual dimorphism and environmental variation in Drosophila melanogaster. Six populations were selected for adult desiccation resistance (D), with six matched control populations maintained in parallel (C). After 46 generations, the D populations had increased in survival time under arid conditions by 68% and in body weight by 20% compared to the C populations. The increase in size was the result of both extended development and faster growth rate of D juveniles. Adaptation to the stress came at a cost in terms of preadult viability and female fecundity. Because males are innately less tolerant of desiccation stress, very few D males survived desiccation-selection; while potentially a windfall for survivors, these conditions mean that most males’ fitness was determined posthumously. We conjectured that selection for early maturation and mating in males was in conflict with selection for survival and later reproduction in females. Consistent with this prediction, the sexes showed different patterns of age-specific desiccation resistance and resource acquisition, and there was a trend towards increasingly female-biased sexual size dimorphism. However, levels of desiccation resistance were unaffected, with D males and females increasing in parallel. Either there is a strong positive genetic correlation between the sexes that limits independent evolution of desiccation resistance, or fitness pay-offs from the strategy of riding out the stress bout are great enough to sustain concordant selection on the two sexes. We discuss the forces that mould fitness in males under a regimen where trade-offs between survival and reproduction may be considerable.     

Males' evolutionary responses to experimental removal of sexual selection

We evaluated the influence of pre- and post-copulatory sexual selection upon male reproductive traits in a naturally promiscuous species, Drosophila melanogaster. Sexual selection was removed in two replicate populations through enforced monogamous mating with random mate assignment or retained in polyandrous controls. Monogamous mating eliminates all opportunities for mate competition, mate discrimination, sperm competition, cryptic female choice and, hence, sexual conflict. Levels of divergence between lines in sperm production and male fitness traits were quantified after 38-81 generations of selection. Three a priori predictions were tested: (i) male investment in spermatogenesis will be lower in monogamy-line males due to the absence of sperm competition selection, (ii) due to the evolution of increased male benevolence, the fitness of females paired with monogamy-line males will be higher than that of females paired with control-line males, and (iii) monogamy-line males will exhibit decreased competitive reproductive success relative to control-line males. The first two predictions were supported, whereas the third prediction was not. Monogamy males evolved a smaller body size and the size of their testes and the number of sperm within the testes were disproportionately further reduced. In contrast, the fitness of monogamous males (and their mates) was greater when reproducing in a non-competitive context: females mated once with monogamous males produced offspring at a faster rate and produced a greater total number of surviving progeny than did females mated to control males. The results indicate that sexual selection favours the production of increased numbers of sperm in D. melanogaster and that sexual selection favours some male traits conferring a direct cost to the fecundity of females.     

Sexual conflict and cooperation under naturally occurring male enforced monogamy

An evolutionary conflict often exists between the sexes in regard to female mating patterns. Females can benefit from polyandry, whereas males mating with polyandrous females lose reproductive opportunities because of sperm competition. Where this conflict occurs, the evolution of mechanisms whereby males can control female remating, often at a fitness cost to the female, are expected to evolve. The fitness cost to the female will be increased in systems where a few high status males monopolise mating opportunities and thus have limited sperm supplies. Here we show that in the cockroach Nauphoeta cinerea, a species where males enforce female monogamy in the first reproductive cycle, males that have become sperm depleted continue to be able to manipulate female remating behaviour. Although the manipulation severely decreases fecundity in females mated to sperm-depleted males, males benefit, increasing their relative fitness by preventing other males from reproducing. Our results suggest that there is selection on maintaining the mechanism of manipulation rather than maintaining sperm numbers. Taken with previous research on sexual conflict in N. cinerea, this study suggests that the causes and consequences of sexual conflict are complex and can change across the life history of an individual.     

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.     

Sexual selection and speciation in mammals,butterflies and spiders

Recently refined evolutionary theories propose that sexual selection and reproductive conflict could be drivers of speciation. Male and female reproductive optima invariably differ because the potential reproductive rate of males almost always exceeds that of females: females are selected to maximize mate 'quality', while males can increase fitness through mate 'quantity'. A dynamic, sexually selected conflict therefore exists in which 'competitive' males are selected to override the preference tactics evolved by 'choosy' females. The wide variation across taxa in mating systems therefore generates variance in the outcome of intrasexual conflict and the strength of sexual selection: monandry constrains reproductive heterozygosity and allows female choice to select and maintain particular (preferred) genes; polyandry promotes reproductive heterozygosity and will more likely override female choice. Two different theories predict how sexual selection might influence speciation. Traditional ideas indicate that increased sexual selection (and hence conflict) generates a greater diversity of male reproductive strategies to be counteracted by female mate preferences, thus providing elevated potentials for speciation as more evolutionary avenues of male-female interaction are created. A less intuitively obvious theory proposes that increased sexual selection and conflict constrains speciation by reducing the opportunities for female mate choice under polyandry. We use a comparative approach to test these theories by investigating whether two general measures of sexual selection and the potential for sexual conflict have influenced speciation. Sexual size dimorphism (across 480 mammalian genera, 105 butterfly genera and 148 spider genera) and degree of polyandry (measured as relative testes size in mammals (72 genera) and mating frequency in female butterflies (54 genera)) showed no associations with the variance in speciosity. Our results therefore show that speciation occurs independently of sexual selection.     

Family feuds: social competition and sexual conflict in complex societies

Darwin was initially puzzled by the processes that led to ornamentation in males-what he termed sexual selection-and those that led to extreme cooperation and altruism in complex animal societies-what was later termed kin selection. Here, I explore the relationships between sexual and kin selection theory by examining how social competition for reproductive opportunities-particularly in females-and sexual conflict over mating partners are inherent and critical parts of complex altruistic societies. I argue that (i) patterns of reproductive sharing within complex societies can drive levels of social competition and reproductive conflict not only in males but also in females living in social groups, and ultimately the evolution of female traits such as ornaments and armaments; (ii) mating conflict over female choice of sexual partners can influence kin structure within groups and drive the evolution of complex societies; and (iii) patterns of reproductive sharing and conflict among females may also drive the evolution of complex societies by influencing kin structure within groups. Ultimately, complex societies exhibiting altruistic behaviour appear to have only arisen in taxa where social competition over reproductive opportunities and sexual conflict over mating partners were low. Once such societies evolved, there were important selective feedbacks on traits used to regulate and mediate intra-sexual competition over reproductive opportunities, particularly in females.     

Evolution of male and female genitalia following release from sexual selection

Despite the key functions of the genitalia in sexual interactions and fertilization, the role of sexual selection and conflict in shaping genital traits remains poorly understood. Seed beetle (Callosobruchus maculatus) males possess spines on the intromittent organ, and females possess a thickened reproductive tract wall that also bears spines. We investigated the role of sexual selection and conflict by imposing monogamous mating on eight replicate populations of this naturally polygamous insect, while maintaining eight other populations under polygamy. To establish whether responses to mating system manipulation were robust to ecological context, we simultaneously manipulated life-history selection (early/late reproduction). Over 18-21 generations, male genital spines evolved relatively reduced length in large males (i.e., shallower static allometry) in monogamous populations. Two nonintromittent male genital appendages also evolved in response to the interaction of mating system and ecology. In contrast, no detectable evolution occurred in female genitalia, consistent with the expectation of a delayed response in defensive traits. Our results support a sexually antagonistic role for the male genital spines, and demonstrate the evolution of static allometry in response to variation in sexual selection opportunity. We argue that further advances in the study of genital coevolution will require a much more detailed understanding of the functions of male and female genital traits.     

Male genotype influences female reproductive investment in Drosophila melanogaster

In many species, males can influence the amount of resources their mates invest in reproduction. Two favoured hypotheses for this observation are that females assess male quality during courtship or copulation and alter their investment in offspring accordingly, or that males manipulate females to invest heavily in offspring produced soon after mating. Here, we examined whether there is genetic variation for males to influence female short-term reproductive investment in Drosophila melanogaster, a species with strong sexual selection and substantial sexual conflict. We measured the fecundity and egg size of females mated to males from multiple isofemale lines collected from populations around the globe. Although these traits were not strongly influenced by the male's population of origin, we found that 22 per cent of the variation in female short-term reproductive investment was attributable to the genotype of her mate. This is the first direct evidence that male D. melanogaster vary genetically in their proximate influence on female fecundity, egg size and overall reproductive investment.     

The evolution of harm--effect of sexual conflicts and population size

Conflicts of interest between mates can promote the evolution of male traits that reduce female fitness and that drive coevolution between the sexes. The rate of adaptation depends on the intensity of selection and its efficiency, which depends on drift and genetic variability. This leads to the largely untested prediction that coevolutionary adaptations such as those driven by sexual conflict should evolve faster in large populations. We tested this using the bruchid beetle Callosobruchus maculatus, a species where harm inflicted by males is well documented. Although most experimental evolution studies remove sexual conflict, we reintroduced it in populations in which it had been experimentally removed. Both population size and standing genetic variability were manipulated in a factorial experimental design. After 90 generations of relaxed conflict (monogamy), the reintroduction of sexual conflicts for 30 generations favored males that harmed females and females that were more resistant to the genital damage inflicted by males. Males evolved to become more harmful when population size was large rather than when initial genetic variation was enriched. Our study shows that sexual selection can create conditions in which males can benefit from harming females and that selection may tend to be more intense and effective in larger populations.     

Sexual selection shapes development and maturation rates in Drosophila

Explanations for the evolution of delayed maturity usually invoke trade‐offs mediated by growth, but processes of reproductive maturation continue long after growth has ceased. Here, we tested whether sexual selection shapes the rate of posteclosion maturation in the fruit fly Drosophila melanogaster. We found that populations maintained for more than 100 generations under a short generation time and polygamous mating system evolved faster posteclosion maturation and faster egg‐to‐adult development of males, when compared to populations kept under short generations and randomized monogamy that eliminated sexual selection. An independent assay demonstrated that more mature males have higher fitness under polygamy, but this advantage disappears under monogamy. In contrast, for females greater maturity was equally advantageous under polygamy and monogamy. Furthermore, monogamous populations evolved faster development and maturation of females relative to polygamous populations, with no detectable trade‐offs with adult size or egg‐to‐adult survival. These results suggest that a major aspect of male maturation involves developing traits that increase success in sexual competition, whereas female maturation is not limited by investment in traits involved in mate choice or defense against male antagonism. Moreover, rates of juvenile development and adult maturation can readily evolve in opposite directions in the two sexes, possibly implicating polymorphisms with sexually antagonistic pleiotropy.     

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.     

Receptive females mitigate costs of sexual conflict

Males typically gain fitness from multiple mating, whereas females often lose fitness from numerous mating, potentially leading to sexual conflict over mating. This conflict is expected to favour the evolution of female resistance to mating. However, females may incur male harassment if they refuse to copulate; thus, greater female resistance may increase costs imposed by males. Here, I show that the evolution of resistance to mating raises fitness disadvantages of interacting with males when mating is harmful in female adzuki bean beetles, Callosobruchus chinensis. Females that were artificially selected for higher and lower remating propensity evolved to accept and resist remating, respectively. Compared with females that evolved to accept remating, females that evolved to resist it suffered higher fitness costs from continuous exposure to males. The costs of a single mating measured by the effect on longevity did not differ among selection line females. This study indicates that receptive rather than resistant females mitigate the fitness loss resulting from sexual conflict, suggesting that even though mating is harmful, females can evolve to accept additional mating.     

Testing for local adaptation in adult male and female fitness among populations evolved under different mate competition regimes

Mating/fertilization success and fecundity are influenced by sexual interactions among individuals, the nature and frequency of which can vary among different environments. The extent of local adaptation for such adult fitness components is poorly understood. We allowed 63 populations of Drosophila melanogaster to independently evolve in one of three mating environments that alter sexual interactions: one involved enforced monogamy, while the other two permitted polygamy in either structurally simple standard fly vials or in larger “cages” with added complexity. Adult male and female reproductive fitness were measured after 16 and 28 generations, respectively, via full reciprocal transplants. In males, reciprocal local adaptation was observed between the monogamy and simple polygamy treatments, consistent with the evolution of reproductively competitive males under polygamy that perform poorly under monogamy because they harm their only mate. However, males evolved in the complex polygamy treatment performed similarly or better than all other males in all mating environments, consistent with previous results showing higher genetic quality in this treatment. Differences in female fitness were more muted, suggesting selection on females was less divergent across the mating treatments and echoing a common pattern of greater phenotypic and expression divergence in males than females.