The cost of mating rises nonlinearly with copulation frequency in a laboratory population of Drosophila melanogaster

Previous studies of Drosophila melanogaster have demonstrated a cost to females from male courtship and mating, but two critically important parameters remain unresolved: (i) the degree to which harm from multiple-mating reduces lifetime fitness and (ii) how harm from mating might change with successive matings (rematings). Here we use 'laboratory island analysis' to quantify the costs that females incur with each remating, in the currency of lifetime fitness and under conditions that closely match those to which the flies have adapted for hundreds of generations. We experimentally manipulated the number of female matings by varying the order of daily 2-h exposures of females to either sperm-less males (XO) or intact males (XY). Females that mated more often had substantially reduced lifetime fecundity, and importantly, the fitness cost from remating rapidly accelerated.     

Fitness effects of female mate choice: preferred males are detrimental for Drosophila melanogaster females

The evolution of female mate choice, broadly defined to include any female behaviour or morphology which biases matings towards certain male phenotypes, is traditionally thought to result from direct or indirect benefits which females acquire when mating with preferred males. In contrast, new models have shown that female mate choice can be generated by sexual conflict, where preferred males may cause a fitness depression in females. Several studies have shown that female Drosophila melanogaster bias matings towards large males. Here, we use male size as a proxy for male attractiveness and test how female fitness is affected by reproducing with large or small males, under two different male densities. Females housed with large males had reduced lifespan and aged at an accelerated rate compared with females housed with small males, and increased male density depressed female fitness further. These fitness differences were due to effects on several different fitness components. Female fitness covaried negatively with male courtship rate, which suggests a cost of courtship. Mating rate increased with male size, whereas female fitness peaked at an intermediate mating rate. Our results suggest that female mate choice in D. melanogaster is, at least in part, a by-product of sexual conflict over the mating rate.     

Natural selection and genetic variation for female resistance to harm from males

The sexual conflict hypothesis predicts that males evolve traits that exploit the higher parental investment of females, which generates selection for females to counter-evolve resistance. In Drosophila melanogaster it is now established that males harm females and that there is genetic variation among males for the degree of this harm. Genetic variation among females for resistance to harm from males, and the corresponding strength of selection on this variation, however, have not been quantified previously. Here we carryout a genome-wide screen for female resistance to harm from males. We estimate that the cost of interactions with males depresses lifetime fecundity of females by 15% (95% CI: 8.2-22.0), that genetic variation for female resistance constitutes 17% of total genetic variation for female adult fitness, and that propensity to remate in response to persistent male courtship is a major factor contributing to genetic variation for female resistance.     

FUNCTIONAL EQUIVALENCE OF GRASPING CERCI AND NUPTIAL FOOD GIFTS IN PROMOTING EJACULATE TRANSFER IN KATYDIDS

The function of nuptial gifts has generated longstanding debate. Nuptial gifts consumed during ejaculate transfer may allow males to transfer more ejaculate than is optimal for females. However, gifts may simultaneously represent male investment in offspring. Evolutionary loss of nuptial gifts can help elucidate pressures driving their evolution. In most katydids (Orthoptera: Tettigoniidae), males transfer a spermatophore comprising two parts: the ejaculate‐containing ampulla and the spermatophylax—a gelatinous gift that females eat during ejaculate transfer. Many species, however, have reduced or no spermatophylaces and many have prolonged copulation. Across 44 katydid species, we tested whether spermatophylaces and prolonged copulation following spermatophore transfer are alternative adaptations to protect the ejaculate. We also tested whether prolonged copulation was associated with (i) male cercal adaptations, helping prevent female disengagement, and (ii) female resistance behavior. As predicted, prolonged copulation following (but not before) spermatophore transfer was associated with reduced nuptial gifts, differences in the functional morphology of male cerci, and behavioral resistance by females during copulation. Furthermore, longer copulation following spermatophore transfer was associated with larger ejaculates, across species with reduced nuptial gifts. Our results demonstrate that nuptial gifts and the use of grasping cerci to prolong ejaculate transfer are functionally equivalent.     

Increased opportunity for sexual conflict promotes harmful males with elevated courtship frequencies

Mating systems have a profound influence on the probability of conflict occurring between the sexes. Promiscuity is predicted to generate sexual conflict, thereby driving the evolution of male traits that harm females, whereas monogamy is expected to foster reproductive cooperation, thus rendering such traits redundant. We tested these predictions using experimentally evolved Drosophila pseudoobscura subject to different mating systems. Female survival was not influenced by the mating system treatment of her partner. However, females continuously housed with males evolving under elevated opportunities for female promiscuity produced fewer total progeny, but a relatively greater number of progeny early in their lives, than females housed with males evolving under obligate monogamy. We also found that promiscuous males courted females more frequently than monogamous males. Variation in male courtship frequency and progeny production patterns among treatments reinforces the critical importance of mating system variation for sexual conflict, during both pre‐ and post‐copulatory interactions.     

Standing genetic variance for female resistance to harm from males and its relationship to intralocus sexual conflict

Interlocus sexual conflict theory predicts that some male adaptations are harmful to their mates. Females are therefore expected to evolve resistance to this harm. Using cytogenetic cloning techniques, we tested for heritable genetic variation among females for resistance to harm from males and determined whether propensity to remate, female body size, and intralocus conflict contributes to this variation. We found low but significant heritability for female resistance, but this variation accounted for more than half of the standing genetic variation for net fitness among females. We found no association between female resistance and female body size or level of intralocus sexual conflict. Reluctance to remate was found to be an important factor contributing to the female resistance phenotype, and we found a positive selection gradient on this trait. However, we observed only a nonsignificant positive correlation between a female's resistance and her net fitness. One factor contributing to the observed nominal level of selection on female resistance was that males cause the greatest amount of harm to females with the highest intrinsic fecundity.     

Constraints on the coevolution of contemporary human males and females

Because autosomal genes in sexually reproducing organisms spend on average half their time in each sex, and because the traits that they influence encounter different selection pressures in males and females, the evolutionary responses of one sex are constrained by processes occurring in the other sex. Although intralocus sexual conflict can restrict sexes from reaching their phenotypic optima, no direct evidence currently supports its operation in humans. Here, we show that the pattern of multivariate selection acting on human height, weight, blood pressure and glucose, total cholesterol, and age at first birth differs significantly between males and females, and that the angles between male and female linear (77.8 ± 20.5°) and nonlinear (99.1 ± 25.9°) selection gradients were closer to orthogonal than zero, confirming the presence of sexually antagonistic selection. We also found evidence for intralocus sexual conflict demonstrated by significant changes in the predicted male and female responses to selection of individual traits when cross-sex genetic covariances were included and a significant reduction in the angle between male- and female-predicted responses when cross-sex covariances were included (16.9 ± 15.7°), compared with when they were excluded (87.9 ± 31.6°). We conclude that intralocus sexual conflict constrains the joint evolutionary responses of the two sexes in a contemporary human population.     

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.     

EXPERIMENTALLY ENFORCED MONOGAMY: INADVERTENT SELECTION,INBREEDING, OR EVIDENCE FOR SEXUALLY ANTAGONISTIC COEVOLUTION?

There has been recent criticism of experiments that applied enforced monogamous mating to species with a long history of promiscuity. These experiments indicated that the newly introduced monogamy reversed sexually antagonistic coevolution and caused males to evolve to be less harmful to their mates and females to evolve reduced resistance to harm from males. Several authors have proposed alternative interpretations of these experimental results based on qualitative analysis. If well-founded, these criticisms would invalidate an important part of the empirical foundation for sexually antagonistic coevolution between the sexes. Although these criticisms have a reasonable basis in principle, we find that after quantitative evaluation that they are not supported.     

Sexual conflict does not drive reproductive isolation in experimental populations of Drosophila pseudoobscura

Sexual conflict has been predicted to drive reproductive isolation by generating arbitrary but rapid coevolutionary changes in reproductive traits among allopatric populations. A testable prediction of this proposal is that allopatric populations experiencing different levels of sexual conflict should exhibit different levels of reproductive isolation. We tested this prediction using experimentally evolved populations of the promiscuous Drosophila pseudoobscura. We manipulated sexual conflict by enforcing either monogamy, maintaining natural levels of promiscuity, or elevating promiscuity. Within each treatment, we carried out sympatric and allopatric crosses using replicated populations and examined pre-zygotic (number of mating pairs, mating speed and copulation duration) and post-zygotic (hybrid inviability and sterility) indicators of reproductive isolation. After 50 generations of selection, none of the measures conformed to predictions of sexual conflict driving reproductive isolation. Our results cannot be explained by lack of genetic variation or weak selection and suggest that sexual conflict may not be a widespread engine of speciation.     

Selection on an antagonistic behavioral trait can drive rapid genital coevolution in the burying beetle,Nicrophorus vespilloides

Male and female genital morphology varies widely across many taxa, and even among populations. Disentangling potential sources of selection on genital morphology is problematic because each sex is predicted to respond to adaptations in the other due to reproductive conflicts of interest. To test how variation in this sexual conflict trait relates to variation in genital morphology we used our previously developed artificial selection lines for high and low repeated mating rates. We selected for high and low repeated mating rates using monogamous pairings to eliminate contemporaneous female choice and male–male competition. Male and female genital shape responded rapidly to selection on repeated mating rate. High and low mating rate lines diverged from control lines after only 10 generations of selection. We also detected significant patterns of male and female genital shape coevolution among selection regimes. We argue that because our selection lines differ in sexual conflict, these results support the hypothesis that sexually antagonistic coevolution can drive the rapid divergence of genital morphology. The greatest divergence in morphology corresponded with lines in which the resolution of sexual conflict over mating rate was biased in favor of male interests.     

An assessment of Putative Sexually Antagonistic Traits in a Freshwater Amphipod Species

Sexual conflict can result in an ‘evolutionary arms race’ between males and females, with the evolution of sexual antagonistic traits used to resolve the conflict in favor of one sex over the other. We assessed the resolution of sexual conflict in a Hyalella amphipod species by manipulating putative sexually antagonistic traits in males and females and used mate‐guarding duration as our metric of conflict resolution. We discovered that large male posterior gnathopod size increased mate‐guarding duration, which suggests that it is a sexually antagonistic trait in this species. In contrast, female and male body size did not significantly affect mate‐guarding duration. Given that male posterior gnathopods show heightened condition dependence, future investigations should explore the interactive effects of sexual conflict and ecological context on trait evolution, phenotypic divergence, and speciation to elucidate the complex mechanisms involved in the evolution of biological diversity.     

Sexual coevolution in the traumatically inseminating plant bug genus Coridromius

Sexual conflict has recently been proposed as a driving force behind the rapid diversification of genitalia among sexually reproducing organisms. In traumatically inseminating insects, males stab females in the side of the body with needle‐like genitalia, ejaculating into their body cavity. Such mating is costly to females and has led to the evolution of cost‐reducing ‘paragenitalia’ in some species. Whereas some consider this evidence of sexually antagonistic coevolution, others remain unconvinced. Variation in the reproductive morphology of both sexes – particularly males – is alleged to be negligible, contradicting the expectations of a coevolutionary arms race. Here, we use a phylogeny of the traumatically inseminating plant bug genus Coridromius to show that external female paragenitalia have evolved multiply across the genus and are correlated with changes in male genital shape. This pattern is characteristic of an evolutionary arms race driven by sexual conflict.     

Benefits of size dimorphism and copulatory silk wrapping in the sexually cannibalistic nursery web spider,Pisaurina mira

In sexually cannibalistic animals, male fitness is influenced not only by successful mate acquisition and egg fertilization, but also by avoiding being eaten. In the cannibalistic nursery web spider, Pisaurina mira, the legs of mature males are longer in relation to their body size than those of females, and males use these legs to aid in wrapping a female''s legs with silk prior to and during copulation. We hypothesized that elongated male legs and silk wrapping provide benefits to males, in part through a reduced likelihood of sexual cannibalism. To test this, we paired females of random size with males from one of two treatment groups—those capable of silk wrapping versus those incapable of silk wrapping. We found that males with relatively longer legs and larger body size were more likely to mate and were less likely to be cannibalized prior to copulation. Regardless of relative size, males capable of silk wrapping were less likely to be cannibalized during or following copulation and had more opportunities for sperm transfer (i.e. pedipalpal insertions). Our results suggest that male size and copulatory silk wrapping are sexually selected traits benefiting male reproductive success.     

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.     

Interaction Between Sexually Antagonistic Selection and Mate Choice in the Evolution of Female Responses to Male Traits

Theoretical analyses of selection on mutations affecting female responsiveness to male traits suggested that sexually antagonistic selection and traditional female choice are not exclusive alternatives. They can act simultaneously on the same female traits, and can either reinforce or act against each other. These analyses do not yield theoretical predictions regarding the relative frequency and importance of the two types of selection on female responsiveness, as the balance between them is affected by complex factors, including the frequency distribution of male traits, and the mechanisms of male action. Male–female interactions differ from many other evolutionary interactions involving potential evolutionary conflict, in that male and female genomes are irretrievably mixed in their offspring, thus increasing the possibility of indirect payoffs to one participant from the traits of its partner.     

Intentional multiple mating by females in a species where sneak fertilization circumvents female choice for parental males

This paper describes how individual female ocellated wrasse Symphodus ocellatus distribute their spawning among males and nests in space and time. It is based on previously collected genetic data of larvae from ten different nests (used to reconstruct half and full‐sibling groupings both within and among nests on multiple days) and behavioural data of marked females across the reproductive season. Both the genetic analyses and behavioural observations confirm that female S. ocellatus intentionally engage in multiple mating, by repeatedly spawning at the same nest on different days and at several different nests (up to 12 spawning events over 3 weeks), leading to mixed paternity among her young. The main benefit of such high and intentional multiple mating is probably insurance against brood failure due to nest predation, desertion or poor paternal care by the male. These findings reveal that even in systems where females attempt to avoid male‐controlled mixed paternity, they may still engage in intentional multiple mating due to these potential benefits.