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.     

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.     

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.     

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.     

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.     

Female,but not male,nematodes evolve under experimental sexual coevolution

Coevolution between the sexes is often considered to be male-driven: the male genome is constantly scanned by selection for traits that increase relative male fertilization success. Whenever these traits are harmful to females, the female genome is scanned for resistance traits. The resulting antagonistic coevolution between the sexes is analogous to Red Queen dynamics, where adaptation and counteradaptation keep each other in check. However, the underlying assumption that male trait evolution precedes female trait counteradaptation has received few empirical tests. Using the gonochoristic nematode Caenorhabditis remanei, we now show that 20 generations of relaxed versus increased sexual selection pressure lead to female, but not to male, trait evolution, questioning the generality of a male-driven process.     

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.     

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.     

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 INTERACTING PHENOTYPES: A QUANTITATIVE GENETIC ANALYSIS OF FECUNDITY AND COPULA DURATION IN DROSOPHILA MELANOGASTER

Many reproductive traits that have evolved under sexual conflict may be influenced by both sexes. Investigation of the genetic architecture of such traits can yield important insight into their evolution, but this entails that the heritable component of variation is estimated for males and females—as an interacting phenotype. We address the lack of research in this area through an investigation of egg production and copula duration in the fruit fly, Drosophila melanogaster. Despite egg production rate being determined by both sexes, which may cause sexual conflict, an assessment of this trait as an interacting phenotype is lacking. It is currently unclear whether copula duration is determined by males and/or females. We found significant female, but not male, genetic variance for egg production rate that may indicate reduced potential for ongoing sexually antagonistic coevolution. In contrast, copula duration was determined by significant genetic variance in both sexes. We also identified genetic variation in egg retention among virgin females. Although previously identified in wild populations, it is unclear why this should be present in a laboratory stock. This study provides a novel insight into the shared genetic architecture of reproductive traits that are the subject of sexual conflict.     

Sexual selection on bushcricket genitalia operates in a mosaic pattern

In most species with internal fertilization, male genitalia evolve faster than other morphological structures. This holds true for genital titillators, which are used exclusively during mating in several bushcricket subfamilies. Several theories have been proposed for the sexual selection forces driving the evolution of internal genitalia, especially sperm competition, sexually antagonistic coevolution (SAC), and cryptic female choice (CFC). However, it is unclear whether the evolution of genitalia can be described with a single hypothesis or a combination of them. The study of species‐specific genitalia action could contribute to the controversial debate about the underlying selective evolutionary forces. We studied female mating behaviors in response to experimentally modified titillators in a phylogenetically nested set of four bushcricket species: Roeseliana roeselii, Pholidoptera littoralis littoralis, Tettigonia viridissima (of the subfamily Tettigoniinae), and Letana inflata (Phaneropterinae). Bushcricket titillators have several potential functions; they stimulate females and suppress female resistance, ensure proper ampulla or spermatophore attachment, and facilitate male fixation. In R. roeselii, titillators stimulate females to accept copulations, supporting sexual selection by CFC. Conversely, titillator modification had no observable effect on the female's behavior in T. viridissima. The titillators of Ph. l. littoralis mechanically support the mating position and the spermatophore transfer, pointing to sexual selection by SAC. Mixed support was found in L. inflata, where manipulation resulted in increased female resistance (evidence for CFC) and mating failures by reduced spermatophore transfer success (evidence for SAC). Sexual selection is highly species‐specific with a mosaic support for either cryptic female choice or sexually antagonistic coevolution or a combination of both in the four species.     

Latitudinal variation and coevolutionary diversification of sexually dimorphic traits in the false blister beetle Oedemera sexualis

Sexual traits are subject to evolutionary forces that maximize reproductive benefits and minimize survival costs, both of which can depend on environmental conditions. Latitude explains substantial variation in environmental conditions. However, little is known about the relationship between sexual trait variation and latitude, although body size often correlates with latitude. We examined latitudinal variation in male and female sexual traits in 22 populations of the false blister beetle Oedemera sexualis in the Japanese Archipelago. Males possess massive hind legs that function as a female‐grasping apparatus, while females possess slender hind legs that are used to dislodge mounting males. Morphometric analyses revealed that male and female body size (elytron length), length and width of the hind femur and tibia, and allometric slopes of these four hind leg dimensions differed significantly among populations. Of these, three traits showed latitudinal variation, namely, male hind femur was stouter; female hind tibia was slenderer, and female body was smaller at lower latitudes than at higher latitudes. Hind leg sizes and shapes, as measured by principal component analysis of these four hind leg dimensions in each sex, covaried significantly between sexes, suggesting coevolutionary diversification in sexual traits. Covariation between sexes was weaker when variation in these traits with latitude was removed. These results suggest that coevolutionary diversification between male and female sexual traits is mediated by environmental conditions that vary with latitude.     

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.     

Effects of antagonistic coevolution on parasite‐mediated host coexistence

Parasites can promote diversity by mediating coexistence between a poorer and superior competitor, if the superior competitor is more susceptible to parasitism. However, hosts and parasites frequently undergo antagonistic coevolution. This process may result in the accumulation of pleiotropic fitness costs associated with host resistance, and could breakdown coexistence. We experimentally investigated parasite‐mediated coexistence of two genotypes of the bacterium Pseudomonas fluorescens, where one genotype underwent coevolution with a parasite (a virulent bacteriophage), whereas the other genotype was resistant to the evolving phages at all time points, but a poorer competitor. In the absence of phages, the resistant genotype was rapidly driven extinct in all populations. In the presence of the phages, the resistant genotype persisted in four of six populations and eventually reached higher frequencies than the sensitive genotype. The coevolving genotype showed a reduction in the growth rate, consistent with a cost of resistance, which may be responsible for a decline in its relative fitness. These results demonstrate that the stability of parasite‐mediated coexistence of resistant and susceptible species or genotypes is likely to be affected if parasites and susceptible hosts coevolve.     

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.     

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.     

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.     

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.     

The evolution of female genitalia

Female genitalia have been largely neglected in studies of genital evolution, perhaps due to the long‐standing belief that they are relatively invariable and therefore taxonomically and evolutionarily uninformative in comparison with male genitalia. Contemporary studies of genital evolution have begun to dispute this view, and to demonstrate that female genitalia can be highly diverse and covary with the genitalia of males. Here, we examine evidence for three mechanisms of genital evolution in females: species isolating ‘lock‐and‐key’ evolution, cryptic female choice and sexual conflict. Lock‐and‐key genital evolution has been thought to be relatively unimportant; however, we present cases that show how species isolation may well play a role in the evolution of female genitalia. Much support for female genital evolution via sexual conflict comes from studies of both invertebrate and vertebrate species; however, the effects of sexual conflict can be difficult to distinguish from models of cryptic female choice that focus on putative benefits of choice for females. We offer potential solutions to alleviate this issue. Finally, we offer directions for future studies in order to expand and refine our knowledge surrounding female genital evolution.