Multiple mating in the traumatically inseminating Warehouse pirate bug, Xylocoris flavipes: effects on fecundity and longevity

Optimal mating frequencies differ between sexes as a consequence of the sexual differentiation of reproductive costs per mating, where mating is normally more costly to females than males. In mating systems where sexual reproduction is costly to females, sexual conflict may cause both direct (i.e. by reducing female fecundity or causing mortality) and indirect (i.e. increased risk of mortality, reduced offspring viability) reductions in lifetime reproductive success of females, which have individual and population consequences. We investigated the direct and indirect costs of multiple mating in a traumatically inseminating (TI) predatory Warehouse pirate bug, Xylocoris flavipes (Reuter) (Hemiptera: Anthocoridae), where the male penetrates the female's abdomen during copulation. This study aimed to quantify the effects of TI on female fecundity, egg viability, the lifetime fecundity schedule, longevity and prey consumption in this cosmopolitan biocontrol agent. We found no difference in the total reproductive output between mating treatments in terms of total eggs laid or offspring viability, but there were significant differences found in daily fecundity schedules and adult longevity. In terms of lifetime reproduction, female Warehouse pirate bugs appear to be adapted to compensate for the costs of TI mating to their longevity.     

Sexual conflict and antagonistic coevolution across water strider populations

Microevolutionary studies have demonstrated sexually antagonistic selection on sexual traits, and existing evidence supports a macroevolutionary pattern of sexually antagonistic coevolution. Two current questions are how antagonistic selection within-populations scales to divergence among populations, and to what extent intraspecific divergence matches species-level patterns. To address these questions, we conducted an intraspecific comparative study of sexual armaments and mating behaviors in a water strider (Gerris incognitus) in which male genitals grasp resistant females and female abdominal structures help ward off males. The degree of exaggeration of these armaments coevolves across species. We found a similar strong pattern of antagonistic coevolution among populations, suggesting that sexual conflict drives population differentiation in morphology. Furthermore, relative exaggeration in armaments was closely related to mating outcomes in a common environment. Interestingly, the effect of armaments on mating was mediated by population sexual size dimorphism. When females had a large size advantage, mating activity was low and independent of armaments, but when males had a relative size advantage, mating activity depended on which sex had relatively exaggerated armaments. Thus, a strong signal of sexually antagonistic coevolution is apparent even among populations. These results open opportunities to understand links between sexual arms races, ecological variation, and reproductive isolation.     

Female‐driven intersexual coevolution in beetle genitalia

Genital coevolution is a pervasive phenomenon as changes in one sex tend to impose fitness consequences on the other, generating sexual conflict. Sexual conflict is often thought to cause stronger selection on males due to the Darwin–Bateman's anisogamy paradigm. However, recent studies have demonstrated that female genitalia may be equally elaborated and perform diverse extra‐copulatory functions. These characteristics suggest that female genitals can also be primary targets of selection, especially where natural selection acts on female‐exclusive functions such as oviposition. Here, we test this hypothesis in a statistical phylogenetic framework across the whole beetle (Coleoptera) phylogeny, investigating whether coevolution of specific genital traits may be triggered by changes in females. We focus on traits of the proctiger, which composes part of the male terminalia and the female ovipositor. Our results present a comprehensive case of male–female genital coevolution and provide solid statistical evidence for a female‐initiated coevolutionary process where the vast majority of evolutionary transitions in males have occurred only after changes in females. We corroborate the hypothesis that female traits may change independently and elicit counter‐adaptations in males. Furthermore, by showing a consistent pattern across the phylogeny of the most diverse group of animals, our results suggest that this female‐driven dynamics may persist through long time scales.     

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.     

Inter-genomic sexual conflict drives antagonistic coevolution in harvester ants

The reproductive interests of males and females are not always aligned, leading to sexual conflict over parental investment, rate of reproduction and mate choice. Traits that increase the genetic interests of one sex often occur at the expense of the other, selecting for counter-adaptations leading to antagonistic coevolution. Reproductive conflict is not limited to intraspecific interactions; interspecific hybridization can produce pronounced sexual conflict between males and females of different species, but it is unclear whether such conflict can drive sexually antagonistic coevolution between reproductively isolated genomes. We tested for hybridization-driven sexually antagonistic adaptations in queens and males of the socially hybridogenetic ‘J’ lineages of Pogonomyrmex harvester ants, whose mating system promotes hybridization in queens but selects against it in males. We conducted no-choice mating assays to compare patterns of mating behaviour and sperm transfer between inter- and intra-lineage pairings. There was no evidence for mate discrimination on the basis of pair type, and the total quantity of sperm transferred did not differ between intra- and inter-lineage pairs; however, further dissection of the sperm transfer process into distinct mechanistic components revealed significant, and opposing, cryptic manipulation of copulatory investment by both sexes. Males of both lineages increased their rate of sperm transfer to high-fitness intra-lineage mates, with a stronger response in the rarer lineage for whom mating mistakes are the most likely. By contrast, the total duration of copulation for intra-lineage mating pairs was significantly shorter than for inter-lineage crosses, suggesting that queens respond to prevent excessive sperm loading by prematurely terminating copulation. These findings demonstrate that sexual conflict can lead to antagonistic coevolution in both intra-genomic and inter-genomic contexts. Indeed, the resolution of sexual conflict may be a key determinant of the long-term evolutionary potential of host-dependent reproductive strategies, counteracting the inherent instabilities arising from such systems.     

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.     

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.     

Potential sexual transmission of environmental microbes in a traumatically inseminating insect

Abstract.  1. Very little attention has been paid to the importance of environmental microbes and how they gain access to potential hosts during host wounding or sexual interactions. Male members of the family Cimicidae (including the haematophagous human pest, the bed bug, Cimex lectularius ) show traumatic insemination: in order to transfer sperm the male punctures the female's cuticle using a needle-like intromittent organ. The microbes from the local environment that gain entry into females during mating have previously been shown to be an important source of mortality. This study aimed to identify these microbes and their natural environmental substrates.
2. Nine different microbe taxa from the surface of the cuticle were identified, five of them (two Penicillium spp., Stenotrophomonas , Enterobacter , Bacillus ) were found in the local environment as well as on the intromittent organ of male bed bugs: these are strong candidates for the causal agents of mating-induced female mortality. Local differences in the microbial communities and their hosts' response to them are discussed as a source of reproductive isolation.
3. Four microbe genera ( Scopulariopsis , Staphylococcus , Arthrobacter , Micrococcus ) were found exclusively on blood agar. One of them, and four grown on regular agar, are classified as human pathogens. However, because no microbes were isolated from the piercing and sucking mouthparts the epidemiological significance of bed bugs carrying externally attached microbes is probably low.     

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.     

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.     

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 in primates

Sexual conflict is increasingly recognized as a major force for evolutionary change and holds great potential for delineating variation in primate behavior and morphology. The goals of this review are to highlight the rapidly rising field of sexual conflict and the ongoing shift in our understanding of interactions between the sexes. We discuss the evidence for sexual conflict within the Order Primates, and assess how studies of primates have illuminated and can continue to increase our understanding of sexual conflict and sexual selection. Finally, we introduce a framework for understanding the behavioral, anatomical, and genetic expression of sexual conflict across primate mating systems and suggest directions for future research.     

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.     

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.     

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.     

Sexual conflict and indirect benefits

Recent work on sexual selection and sexual conflict has explored the influence of indirect effects on the evolution of female mating behaviour. It has been suggested that the importance of these effects has been underestimated and that the influence of indirect effects may actually be of relatively greater significance than direct effects. Additionally, it has also been suggested that all indirect effects, both good genes and sexy son, are qualitatively equivalent. Here a counterpoint to these suggestions is offered. We argue two main points: (1) it is unlikely that indirect effects will commonly outweigh direct effects, and (2) that there are important differences between good genes and sexy son indirect effects that must be recognized. We suggest that acknowledgement of these distinctions will lead to increased understanding of processes operating in both sexual conflict and sexual selection.     

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.     

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.     

Sexual selection affects lifespan and aging in the seed beetle

Sexual selection in general, and sexual conflict in particular, should affect the evolution of lifespan and aging. Using experimental evolution, we tested whether removal of sexual selection leads to the evolution of accelerated or decelerated senescence. We subjected replicated populations of the seed beetle Callosobruchus maculatus to either of two selection regimes for 35 generations. These regimes either allowed (polygamy) or removed the potential (monogamy) for sexual selection to operate. To test for the evolution of intrinsic differences between the two selection regimes, we assayed longevity in replicate cohorts of virgin females and males. Virgin females from populations evolving under sexual selection had reduced lifespan as predicted by the sexual conflict theory of aging. However, this reduction was due to increased baseline mortality rather than an increase in age-specific mortality rates with age. We discuss these findings in light of other data from this model system and suggest that system-specific idiosyncrasies may often modulate the general effects of male–female coevolution on the evolution of aging.     

Comparative evidence for a cost to males of manipulating females in bushcrickets

Recent theoretical and empirical research on sexual conflicthas tended to focus on the costs to females of being manipulatedby males. The costs to males associated with the productionof manipulative traits have received relatively little attention.In numerous insects, including bushcrickets (Orthoptera: Tettigoniidae),males are known to transfer substances in the ejaculate thatinhibit the receptivity of females to further matings in a dose-dependentmanner. The aim of this study was to test the prediction that,across bushcricket taxa, larger ejaculates and nuptial giftswill be associated with, on the one hand, longer sexual refractoryperiods in females and, on the other hand, longer sexual refractoryperiods in males. Data on the duration of the sexual refractoryperiod in both males and females, together with ejaculate mass,spermatophylax mass, and male body mass, were obtained for 23species of bushcricket. Both comparative analysis by independentcontrasts and species regression revealed a positive relationship,across taxa, between the duration of the female's sexual refractoryperiod and both relative ejaculate mass and relative nuptialgift mass. Positive relationships were also found between theduration of the male's sexual refractory period and both relativeejaculate mass and relative nuptial gift mass, indicating thatthere is a trade-off between resources spent on spermatophoresize and the male's potential mating rate. This appears to bethe first comparative evidence that there is a cost to malesassociated with manipulating the remating behavior of theirmates.