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.     

Spatial variation in the temporal change of male and female melanic ornamentation in the barn owl

Because the magnitude of selection can vary between sexes and in space and time, sexually antagonistic selection is difficult to demonstrate. In a Swiss population of barn owls (Tyto alba), a heritable eumelanic colour trait (size of black spots on ventral feathers) was positively selected with respect to yearling survival only in females. It remains unclear whether the absence of negative selection in males is typical in this species. To tackle this issue indirectly, we measured the size of black spots in 1733 skin specimens collected by museums from 1816 to 2001 in seven European countries and in the Middle-East. The temporal change in spot size was sex- and country-specific. In males, spots became smaller particularly in three countries (Middle-East, Italy and Switzerland). In females, the size of spots increased significantly in two countries (UK and Spain) and decreased in two others (Germany and Switzerland). Because migration and phenotypic plasticity cannot explain these results, selection is the most likely cause. The weaker temporal change in spot size in females than males may be because of the combined effect of strong genetic correlation between the sexes and stronger negative selection in males than positive selection in females. We thus suggest that in the barn owl, spot size (or genetically correlated traits) is sexually antagonistically selected and that its pattern of selection may account for the maintenance of its variation and sexual dimorphism.     

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.     

Sexually antagonistic coevolution in insects is associated with only limited morphological diversity

Morphological traits involved in male-female sexual interactions, such as male genitalia, often show rapid divergent evolution. This widespread evolutionary pattern could result from sustained sexually antagonistic coevolution, or from other types of selection such as female choice or selection for species isolation. I reviewed the extensive but under-utilized taxonomic literature on a selected subset of insects, in which male-female conflict has apparently resulted in antagonistic coevolution in males and females. I checked the sexual morphology of groups comprising 500-1000 species in six orders for three evolutionary trends predicted by the sexually antagonistic coevolution hypothesis: males with species-specific differences and elaborate morphology in structures that grasp or perforate females in sexual contexts; corresponding female structures with apparently coevolved species-specific morphology; and potentially defensive designs of female morphology. The expectation was that the predictions were especially likely to be fulfilled in these groups. A largely qualitative overview revealed several surprising patterns: sexually antagonistic coevolution is associated with frequent, relatively weak species-specific differences in males, but male designs are usually relatively simple and conservative (in contrast to the diverse and elaborate designs common in male structures specialized to contact and hold females in other species, and also in weapons such as horns and pincers used in intra-specific battles); coevolutionary divergence of females is not common; and defensive female divergence is very uncommon. No cases were found of female defensive devices that can be facultatively deployed. Coevolutionary morphological races may have occurred between males and females of some bugs with traumatic insemination, but apparently as a result of female attempts to control fertilization, rather than to reduce the physical damage and infections resulting from insertion of the male's hypodermic genitalia. In sum, the sexually antagonistic coevolution that probably occurs in these groups has generally not resulted in rapid, sustained evolutionary divergence in male and female external sexual morphology. Several limitations of this study, and directions for further analyses are discussed.     

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.     

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.     

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.     

Comparing the intersex genetic correlation for fitness across novel environments in the fruit fly,Drosophila serrata

Sexually antagonistic genetic variation can pose limits to the independent evolution and adaptation of the sexes. The extent of sexually antagonistic variation is reflected in the intersex genetic correlation for fitness (r_w^FM). Previous estimates of this correlation have been mostly limited to populations in environments to which they are already well adapted, making it difficult to gauge the importance of sexually antagonistic genetic variance during the early stages of adaptation, such as that occurring following abrupt environmental change or upon the colonization of new habitat. Here we assayed male and female lifetime fitness in a population of Drosophila serrata in four novel laboratory environments. We found that r_w^FM varied significantly across environments, with point estimates ranging from positive to negative values of considerable magnitude. We also found that the variability among estimates was because, at least in part, of significant differences among environments in the genetic variances of both male and female fitness, with no evidence of any significant changes in the intersex covariance itself, although standard errors of these estimates were large. Our results illustrate the unpredictable nature of r_w^FM in novel environments and suggest that, although sexually antagonistic genetic variance can be pronounced in some novel environments, it may have little effect in constraining the early stages of adaptation in others.     

Sexy sons from re-mating do not recoup the direct costs of harmful male interactions in the Drosophila melanogaster laboratory model system

The empirical foundation for sexual conflict theory is the data from many different taxa demonstrating that females are harmed while interacting with males. However, the interpretation of this keystone evidence has been challenged because females may more than counterbalance the direct costs of interacting with males by the indirect benefits of obtaining higher quality genes for their offspring. A quantification of this trade-off is critical to resolve the controversy and is presented here. A multi-generation fitness assay in the Drosophila melanogaster laboratory model system was used to quantify both the direct costs to females due to interactions with males and indirect benefits via sexy sons. We specifically focus on the interactions that occur between males and nonvirgin females. In the laboratory environment of our base population, females mate soon after eclosion and store sufficient sperm for their entire lifetime, yet males persistently court these nonvirgin females and frequently succeed in re-mating them. Females may benefit from these interactions despite direct costs to their lifetime fecundity if re-mating allows them to trade-up to mates of higher genetic quality and thereby secure indirect benefits for their offspring. We found that direct costs of interactions between males and nonvirgin females substantially exceeded indirect benefits through sexy sons. These data, in combination with past studies of the good genes route of indirect benefits, demonstrate that inter-sexual interactions drive sexually antagonistic co-evolution in this model system.     

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.