An evolutionary cost of separate genders revealed by male-limited evolution

Theory predicts that intralocus sexual conflict can constrain the evolution of sexual dimorphism, preventing each sex from independently maximizing its fitness. To test this idea, we limited genome-wide gene expression to males in four replicate Drosophila melanogaster populations, removing female-specific selection. Over 25 generations, male fitness increased markedly, as sexually dimorphic traits evolved in the male direction. When male-evolved genomes were expressed in females, their fitness displayed a nearly symmetrical decrease. These results suggest that intralocus conflict strongly limits sex-specific adaptation, promoting the maintenance of genetic variation for fitness. Populations may carry a heavy genetic load as a result of selection for separate genders.     

Wolbachia infection can bias estimates of intralocus sexual conflict

Males and females share most of their genome and develop many of the same traits. However, each sex frequently has different optimal values for these shared traits, creating intralocus sexual conflict. This conflict has been observed in wild and laboratory populations of insects and affects important evolutionary processes such as sexual selection, the maintenance of genetic variation, and possibly even speciation. Given the broad impacts of intralocus conflict, accurately detecting and measuring it is important. A common way to detect intralocus sexual conflict is to calculate the intersexual genetic correlation for fitness, with negative values suggesting conflict. Here, we highlight a potential confounder of this measure—cytoplasmic incompatibility caused by the intracellular parasite Wolbachia. Infection with Wolbachia can generate negative intersexual genetic correlations for fitness in insects, suggestive of intralocus sexual conflict. This is because cytoplasmic incompatibility reduces the fitness of uninfected females mated to infected males, while uninfected males will not suffer reductions in fitness if they mate with infected females and may even be fitter than infected males. This can lead to strong negative intersexual genetic correlations for fitness, mimicking intralocus conflict. We illustrate this issue using simulations and then present Drosophila simulans data that show how reproductive incompatibilities caused by Wolbachia infection can generate signals of intralocus sexual conflict. Given that Wolbachia infection in insect populations is pervasive, but populations usually contain both infected and uninfected individuals providing scope for cytoplasmic incompatibility, this is an important consideration for sexual conflict research but one which, to date, has been largely underappreciated.     

Evidence for strong intralocus sexual conflict in the Indian meal moth, Plodia interpunctella

Males and females share a genome and express many shared phenotypic traits, which are often selected in opposite directions. This generates intralocus sexual conflict that may constrain trait evolution by preventing the sexes from reaching their optimal phenotype. Furthermore, if present across multiple loci, intralocus sexual conflict can result in a gender load that may diminish the benefits of sexual selection and help maintain genetic variation for fitness. Despite the importance of intralocus sexual conflict, surprisingly few empirical studies conclusively demonstrate its operation. We show that the pattern of multivariate selection acting on three sexually dimorphic life-history traits (development time, body size, and longevity) in the Indian meal moth, Plodia interpunctella, is opposing for the sexes. Moreover, we combined our estimates of selection with the additive genetic variance-covariance matrix (G) to predict the evolutionary response of the life-history traits in the sexes and showed that the angle between the vector of responses and the vector of sexually antagonistic selection was almost orthogonal at 84.70°. Thus, G biases the predicted response of life-history traits in the sexes away from the direction of sexually antagonistic selection, confirming the presence of strong intralocus sexual conflict in this species. Despite this, sexual dimorphism has evolved in all of the life-history traits examined suggesting that mechanism(s) have evolved to resolve this conflict and allow the sexes to reach their life-history optima. We argue that intralocus sexual conflict is likely to play an important role in the evolution of divergent life-history strategies between the sexes in this species.     

Intralocus sexual conflict and the genetic architecture of sexually dimorphic traits in Prochyliza xanthostoma (Diptera: Piophilidae)

Because homologous traits of males and females are likely to have a common genetic basis, sex-specific selection (often resulting from sexual selection on one sex) may generate an evolutionary tug-of-war known as intralocus sexual conflict, which will constrain the adaptive divergence of the sexes. Theory suggests that intralocus sexual conflict can be mitigated through reduction of the intersexual genetic correlation (rMF), predicting negative covariation between rMF and sexual dimorphism. In addition, recent work showed that selection should favor reduced expression of alleles inherited from the opposite-sex parent (intersexual inheritance) in traits subject to intralocus sexual conflict. For traits under sexual selection in males, this should be manifested either in reduced maternal heritability or, when conflict is severe, in reduced heritability through the opposite-sex parent in offspring of both sexes. However, because we do not know how far these hypothesized evolutionary responses can actually proceed, the importance of intralocus sexual conflict as a long-term constraint on adaptive evolution remains unclear. In this study, we investigated the genetic architecture of sexual and nonsexual morphological traits in Prochyliza xanthostoma. The lowest rMF and greatest dimorphism were exhibited by two sexual traits (head length and antenna length) and, among all traits, the degree of sexual dimorphism was correlated negatively with rMF. Moreover, sexual traits exhibited reduced maternal heritabilities, and the most strongly dimorphic sexual trait (antenna length) was heritable only through the same-sex parent in offspring of both sexes. Our results support theory and suggest that intralocus sexual conflict can be resolved substantially by genomic adaptation. Further work is required to identify the proximate mechanisms underlying these patterns.     

Partitioning of resources: the evolutionary genetics of sexual conflict over resource acquisition and allocation

Fitness depends on both the resources that individuals acquire and the allocation of those resources to traits that influence survival and reproduction. Optimal resource allocation differs between females and males as a consequence of their fundamentally different reproductive strategies. However, because most traits have a common genetic basis between the sexes, conflicting selection between the sexes over resource allocation can constrain the evolution of optimal allocation within each sex, and generate trade‐offs for fitness between them (i.e. ‘sexual antagonism’ or ‘intralocus sexual conflict’). The theory of resource acquisition and allocation provides an influential framework for linking genetic variation in acquisition and allocation to empirical evidence of trade‐offs between distinct life‐history traits. However, these models have not considered the emergence of trade‐offs within the context of sexual dimorphism, where they are expected to be particularly common. Here, we extend acquisition–allocation theory and develop a quantitative genetic framework for predicting genetically based trade‐offs between life‐history traits within sexes and between female and male fitness. Our models demonstrate that empirically measurable evidence of sexually antagonistic fitness variation should depend upon three interacting factors that may vary between populations: (1) the genetic variances and between‐sex covariances for resource acquisition and allocation traits, (2) condition‐dependent expression of resource allocation traits and (3) sex differences in selection on the allocation of resource to different fitness components.     

CORRELATED EVOLUTION OF SEXUAL DIMORPHISM AND MALE DIMORPHISM IN A CLADE OF NEOTROPICAL HARVESTMEN

Secondary sexual traits increase male fitness, but may be maladaptive in females, generating intralocus sexual conflict that is ameliorated through sexual dimorphism. Sexual selection on males may also lead some males to avoid expenditure on secondary sexual traits and achieve copulations using alternative reproductive tactics (ARTs). Secondary sexual traits can increase or decrease fitness in males, depending on which ART they employ, generating intralocus tactical conflict that can be ameliorated through male dimorphism. Due to the evolutionary forces acting against intralocus sexual and tactical conflicts, male dimorphism could coevolve with sexual dimorphism, a hypothesis that we tested by investigating these dimorphisms across 48 harvestman species. Using three independently derived phylogenies, we consistently found that the evolution of sexual dimorphism was correlated with that of male dimorphism, and suggest that the major force behind this relationship is the similarity between selection against intralocus sexual conflict and selection against intralocus tactical conflict. We also found that transitions in male dimorphism were more likely in the presence of sexual dimorphism, indicating that if a sexually selected trait arises on an autosome and is expressed in both sexes, its suppression in females probably evolves earlier than its suppression in small males that adopt ARTs.     

Adult locomotory activity mediates intralocus sexual conflict in a laboratory-adapted population of Drosophila melanogaster

The strongest form of intralocus sexual conflict occurs when two conditions are met: (i) there is a positive intersexual genetic correlation for a trait and (ii) the selection gradients on the trait in the two sexes are in opposite directions. Intralocus sexual conflict can constrain the adaptive evolution of both sexes and thereby contribute to a species' 'gender load'. Previous studies of adult lifetime fitness of the same sets of genes expressed in both males and females have established that there is substantial intralocus conflict in the LHM laboratory-adapted population of Drosophila melanogaster. Here, we investigated whether a highly dimorphic trait-adult locomotory activity-contributed substantially to the established intralocus sexual conflict. To measure the selection gradient on activity level, both this trait and adult lifetime fitness were measured under the same environmental conditions to which the flies were adapted. We found significant phenotypic variation in both sexes for adult locomotory activity, and that the selection gradients on this variation were large and in opposite directions in the two sexes. Using hemiclonal analysis to screen 99% of the entire genome, we found abundant genetic variation for adult locomotory activity and showed that this variation occurs on both the X and autosomes. We also established that there is a strong positive intersexual genetic correlation for locomotory activity. These assays revealed that, despite the strong, extant sexual dimorphism for the trait, locomotory activity continues to contribute strongly to intralocus sexual conflict in this population.     

Ontogenetic stage‐specific quantitative trait loci contribute to divergence in developmental trajectories of sexually dimorphic fins between medaka populations

Sexual dimorphism can evolve when males and females differ in phenotypic optima. Genetic constraints can, however, limit the evolution of sexual dimorphism. One possible constraint is derived from alleles expressed in both sexes. Because males and females share most of their genome, shared alleles with different fitness effects between sexes are faced with intralocus sexual conflict. Another potential constraint is derived from genetic correlations between developmental stages. Sexually dimorphic traits are often favoured at adult stages, but selected against as juvenile, so developmental decoupling of traits between ontogenetic stages may be necessary for the evolution of sexual dimorphism in adults. Resolving intralocus conflicts between sexes and ages is therefore a key to the evolution of age‐specific expression of sexual dimorphism. We investigated the genetic architecture of divergence in the ontogeny of sexual dimorphism between two populations of the Japanese medaka (Oryzias latipes) that differ in the magnitude of dimorphism in anal and dorsal fin length. Quantitative trait loci (QTL) mapping revealed that few QTL had consistent effects throughout ontogenetic stages and the majority of QTL change the sizes and directions of effects on fin growth rates during ontogeny. We also found that most QTL were sex‐specific, suggesting that intralocus sexual conflict is almost resolved. Our results indicate that sex‐ and age‐specific QTL enable the populations to achieve optimal developmental trajectories of sexually dimorphic traits in response to complex natural and sexual selection.     

Between‐sex genetic covariance constrains the evolution of sexual dimorphism in Drosophila melanogaster

Males and females share much of their genome, and as a result, intralocus sexual conflict is generated when selection on a shared trait differs between the sexes. This conflict can be partially or entirely resolved via the evolution of sex‐specific genetic variation that allows each sex to approach, or possibly achieve, its optimum phenotype, thereby generating sexual dimorphism. However, shared genetic variation between the sexes can impose constraints on the independent expression of a shared trait in males and females, hindering the evolution of sexual dimorphism. Here, we examine genetic constraints on the evolution of sexual dimorphism in Drosophila melanogaster cuticular hydrocarbon (CHC) expression. We use the extended G matrix, which includes the between‐sex genetic covariances that constitute the B matrix, to compare genetic constraints on two sets of CHC traits that differ in the extent of their sexual dimorphism. We find significant genetic constraints on the evolution of further dimorphism in the least dimorphic traits, but no such constraints for the most dimorphic traits. We also show that the genetic constraints on the least dimorphic CHCs are asymmetrical between the sexes. Our results suggest that there is evidence both for resolved and ongoing sexual conflict in D. melanogaster CHC profiles.     

Intralocus sexual conflict unresolved by sex-limited trait expression

Sexually antagonistic selection generates intralocus sexual conflict, an evolutionary tug-of-war between males and females over optimal trait values [1-4]. Although the potential for this conflict is universal, the evolutionary importance of intralocus conflict is controversial because conflicts are typically thought to be resolvable through the evolution of sex-specific trait development [1-8]. However, whether sex-specific trait expression always resolves intralocus conflict has not been established. We assessed this with beetle populations subjected to bidirectional selection on an exaggerated sexually selected trait, the mandible. Mandibles are only ever developed in males for use in male-male combat, and larger mandibles increase male fitness (fighting [9, 10] and mating success, as we show here). We find that females from populations selected for larger male mandibles have lower fitness, whereas females in small-mandible populations have highest fitness, even though females never develop exaggerated mandibles. This is because mandible development changes genetically correlated characters, resulting in a negative intersexual fitness correlation across these populations, which is the unmistakable signature of intralocus sexual conflict [1]. Our results show that sex-limited trait development need not resolve intralocus sexual conflict, because traits are rarely, if ever, genetically independent of other characters [11]. Hence, intralocus conflict resolution is not as easy as currently thought.     

Multivariate selection and intersexual genetic constraints in a wild bird population

When selection differs between the sexes for traits that are genetically correlated between the sexes, there is potential for the effect of selection in one sex to be altered by indirect selection in the other sex, a situation commonly referred to as intralocus sexual conflict (ISC). While potentially common, ISC has rarely been studied in wild populations. Here, we studied ISC over a set of morphological traits (wing length, tarsus length, bill depth and bill length) in a wild population of great tits (Parus major) from Wytham Woods, UK. Specifically, we quantified the microevolutionary impacts of ISC by combining intra‐ and intersex additive genetic (co)variances and sex‐specific selection estimates in a multivariate framework. Large genetic correlations between homologous male and female traits combined with evidence for sex‐specific multivariate survival selection suggested that ISC could play an appreciable role in the evolution of this population. Together, multivariate sex‐specific selection and additive genetic (co)variance for the traits considered accounted for additive genetic variance in fitness that was uncorrelated between the sexes (cross‐sex genetic correlation = ?0.003, 95% CI = ?0.83, 0.83). Gender load, defined as the reduction in a population's rate of adaptation due to sex‐specific effects, was estimated at 50% (95% CI = 13%, 86%). This study provides novel insights into the evolution of sexual dimorphism in wild populations and illustrates how quantitative genetics and selection analyses can be combined in a multivariate framework to quantify the microevolutionary impacts of ISC.     

Sexual selection, genetic architecture, and the condition dependence of body shape in the sexually dimorphic fly Prochyliza xanthostoma (Piophilidae)

The hypothesis that sexual selection drives the evolution of condition dependence is not firmly supported by empirical evidence, and the process remains poorly understood. First, even though sexual competition typically involves multiple traits, studies usually compare a single sexual trait with a single "control" trait, ignoring variation among sexual traits and raising the possibility of sampling bias. Second, few studies have addressed the genetic basis of condition dependence. Third, even though condition dependence is thought to result from a form of sex-specific epistasis, the evolution of condition dependence has never been considered in relation to intralocus sexual conflict. We argue that condition dependence may weaken intersexual genetic correlations and facilitate the evolution of sexual dimorphism. To address these questions, we manipulated an environmental factor affecting condition (larval diet) and examined its effects on four sexual and four nonsexual traits in Prochyliza xanthostoma adults. As predicted by theory, the strength of condition dependence increased with degree of exaggeration among male traits. Body shape was more condition dependent in males than in females and, perhaps as a result, genetic and environmental effects on body shape were congruent in males, but not in females. However, of the four male sexual traits, only head length was significantly larger in high-condition males after controlling for body size. Strong condition dependence was associated with reduced intersexual genetic correlation. However, homologous male and female traits exhibited correlated responses to condition, suggesting an intersexual genetic correlation for condition dependence itself. Our findings support the role of sexual selection in the evolution of condition dependence, but reveal considerable variation in condition dependence among sexual traits. It is not clear whether the evolution of condition dependence has mitigated or exacerbated intralocus sexual conflict in this species.     

Sexes suffer from suboptimal lifespan because of genetic conflict in a seed beetle

Males and females have different routes to successful reproduction, resulting in sex differences in lifespan and age-specific allocation of reproductive effort. The trade-off between current and future reproduction is often resolved differently by males and females, and both sexes can be constrained in their ability to reach their sex-specific optima owing to intralocus sexual conflict. Such genetic antagonism may have profound implications for evolution, but its role in ageing and lifespan remains unresolved. We provide direct experimental evidence that males live longer and females live shorter than necessary to maximize their relative fitness in Callosobruchus maculatus seed beetles. Using artificial selection in a genetically heterogeneous population, we created replicate long-life lines where males lived on average 27 per cent longer than in short-life lines. As predicted by theory, subsequent assays revealed that upward selection on male lifespan decreased relative male fitness but increased relative female fitness compared with downward selection. Thus, we demonstrate that lifespan-extending genes can help one sex while harming the other. Our results show that sexual antagonism constrains adaptive life-history evolution, support a novel way of maintaining genetic variation for lifespan and argue for better integration of sex effects into applied research programmes aimed at lifespan extension.     

Female-limited X-chromosome evolution effects on male pre- and post-copulatory success

Intralocus sexual conflict arises when the expression of shared alleles at a single locus generates opposite fitness effects in each sex (i.e. sexually antagonistic alleles), preventing each sex from reaching its sex-specific optimum. Despite its importance to reproductive success, the relative contribution of intralocus sexual conflict to male pre- and post-copulatory success is not well-understood. Here, we used a female-limited X-chromosome (FLX) evolution experiment in Drosophila melanogaster to limit the inheritance of the X-chromosome to the matriline, eliminating possible counter-selection in males and allowing the X-chromosome to accumulate female-benefit alleles. After more than 100 generations of FLX evolution, we studied the effect of the evolved X-chromosome on male attractiveness and sperm competitiveness. We found a non-significant increase in attractiveness and decrease in sperm offence ability in males expressing the evolved X-chromosomes, but a significant increase in their ability to avoid displacement by other males'' sperm. This is consistent with a trade-off between these traits, perhaps mediated by differences in body size, causing a small net reduction in overall male fitness in the FLX lines. These results indicate that the X-chromosome in D. melanogaster is subject to selection via intralocus sexual conflict in males.     

Assessing the extent of genome-wide intralocus sexual conflict via experimentally enforced gender-limited selection

Intralocus sexual conflict, which occurs when a trait is selected in opposite directions in the two sexes, is a taxonomically widespread phenomenon. The strongest genetic evidence for a gender load due to intralocus sexual conflict comes from the Drosophila melanogaster laboratory model system, in which a negative genetic correlation between male and female lifetime fitness has been observed. Here, using a D. melanogaster model system, we utilize a novel modification of the 'middle class neighbourhood' design to relax selection in one sex, while maintaining selection in the other. After 26 generations of asymmetrical selection, we observed the expected drop in fitness of the non-selected sex compared to that of the selected sex, consistent with previous studies of intralocus sexual conflict in this species. However, the fitness of the selected sex also dropped compared to the base population. The overall decline in fitness of both the selected and the unselected sex indicates that most new mutations are harmful to both sexes, causing recurrent mutation to build a positive genetic correlation for fitness between the sexes. However, the steeper decay in the fitness of the unselected sex indicates that a substantial number of mutations are gender-limited in expression or sexually antagonistic. Our experiment cannot definitively resolve these two possibilities, but we use recent genomic data and results from previous studies to argue that sexually antagonistic alleles are the more likely explanation.     

Two sexes,one genome: the evolutionary dynamics of intralocus sexual conflict

As the evolutionary interests of males and females are frequently divergent, a trait value that is optimal for the fitness of one sex is often not optimal for the other. A shared genome also means that the same genes may underlie the same trait in both sexes. This can give rise to a form of sexual antagonism, known as intralocus sexual conflict (IASC). Here, a tug‐of‐war over allelic expression can occur, preventing the sexes from reaching optimal trait values, thereby causing sex‐specific reductions in fitness. For some traits, it appears that IASC can be resolved via sex‐specific regulation of genes that subsequently permits sexual dimorphism; however, it seems that whole‐genome resolution may be impossible, due to the genetic architecture of certain traits, and possibly due to the changing dynamics of selection. In this review, we explore the evolutionary mechanisms of, and barriers to, IASC resolution. We also address the broader consequences of this evolutionary feud, the possible interactions between intra‐ and interlocus sexual conflict (IRSC: a form of sexual antagonism involving different loci in each sex), and draw attention to issues that arise from using proxies as measurements of conflict. In particular, it is clear that the sex‐specific fitness consequences of sexual dimorphism require characterization before making assumptions concerning how this relates to IASC. Although empirical data have shown consistent evidence of the fitness effects of IASC, it is essential that we identify the alleles mediating these effects in order to show IASC in its true sense, which is a “conflict over shared genes.”     

Intralocus sexual conflict for fitness: sexually antagonistic alleles for testosterone

Intralocus sexual conflict occurs when a trait encoded by the same genetic locus in the two sexes has different optima in males and females. Such conflict is widespread across taxa, however, the shared phenotypic traits that mediate the conflict are largely unknown. We examined whether the sex hormone, testosterone (T), that controls sexual differentiation, contributes to sexually antagonistic fitness variation in the bank vole, Myodes glareolus. We compared (opposite-sex) sibling reproductive fitness in the bank vole after creating divergent selection lines for T. This study shows that selection for T was differentially associated with son versus daughter reproductive success, causing a negative correlation in fitness between full siblings. Our results demonstrate the presence of intralocus sexual conflict for fitness in this small mammal and that sexually antagonistic selection is acting on T. We also found a negative correlation in fitness between parents and their opposite-sex progeny (e.g. father-daughter), highlighting a dilemma for females, as the indirect genetic benefits of selecting reproductively successful males (high T) are lost with daughters. We discuss mechanisms that may mitigate this disparity between progeny quality.     

INTRALOCUS SEXUAL CONFLICT OVER IMMUNE DEFENSE,GENDER LOAD,AND SEX‐SPECIFIC SIGNALING IN A NATURAL LIZARD POPULATION

In species with separate sexes, antagonistic selection on males and females (intralocus sexual conflict) can result in a gender load that can be resolved through the evolution of sexual dimorphism. We present data on intralocus sexual conflict over immune defense in a natural population of free‐ranging lizards (Uta stansburiana) and discuss the resolution of this conflict. Intralocus sexual conflict arises from correlational selection between immune defense and orange throat coloration in these lizards. Males with orange throats and high antibody responses had enhanced survival, but the same trait combination reduced female fitness. This sexual antagonism persisted across the life cycle and was concordant between the juvenile and adult life stages. The opposing selective pressure on males and females is ameliorated by a negative intersexual genetic correlation (r_m,f=?0.86) for immune defense. Throat coloration was also genetically correlated with immune defense, but the sign of this genetic correlation differed between the sexes. This resulted in sex‐specific signaling of immunological condition. We also found evidence for a sex‐specific maternal effect on sons with potential to additionally reduce the gender load. These results have implications for signaling evolution, genetic integration between adaptive traits, sex allocation, and mutual mate choice for indirect fitness benefits.     

Male-limited evolution suggests no extant intralocus sexual conflict over the sexually dimorphic cuticular hydrocarbons of <Emphasis Type="Italic">Drosophila melanogaster</Emphasis>

Sexually dimorphic traits are likely to have evolved through sexually antagonistic selection. However, recent empirical data suggest that intralocus sexual conflict often persists, even when traits have diverged between males and females. This implies that evolved dimorphism is often incomplete in resolving intralocus conflict, providing a mechanism for the maintenance of genetic variance in fitness-related traits. We used experimental evolution in Drosophila melanogaster to directly test for ongoing conflict over a suite of sexually dimorphic cuticular hydrocarbons (CHCs) that are likely targets of sex-specific selection. Using a set of experimental populations in which the transmission of genetic material had been restricted to males for 82 generations, we show that CHCs did not evolve, providing experimental evidence for the absence of current intralocus sexual conflict over these traits. The absence of ongoing conflict could indicate that CHCs have never been the target of sexually antagonistic selection, although this would require the existing dimorphism to have evolved via completely sexlinked mutations or as a result of former, but now absent, pleiotropic effects of the underlying loci on another trait under sexually antagonistic selection. An alternative interpretation, and which we believe to be more likely, is that the extensive CHC sexual dimorphism is the result of past intralocus sexual conflict that has been fully resolved, implying that these traits have evolved genetic independence between the sexes and that genetic variation in them is therefore maintained by alternative mechanisms. This latter interpretation is consistent with the known roles of CHCs in sexual communication in this species and with previous studies suggesting the genetic independence of CHCs between males and females. Nevertheless, direct estimates of sexually antagonistic selection will be important to fully resolve these alternatives.     

Multivariate intralocus sexual conflict in seed beetles

Intralocus sexual conflict (IaSC) is pervasive because males and females experience differences in selection but share much of the same genome. Traits with integrated genetic architecture should be reservoirs of sexually antagonistic genetic variation for fitness, but explorations of multivariate IaSC are scarce. Previously, we showed that upward artificial selection on male life span decreased male fitness but increased female fitness compared with downward selection in the seed beetle Callosobruchus maculatus. Here, we use these selection lines to investigate sex‐specific evolution of four functionally integrated traits (metabolic rate, locomotor activity, body mass, and life span) that collectively define a sexually dimorphic life‐history syndrome in many species. Male‐limited selection for short life span led to correlated evolution in females toward a more male‐like multivariate phenotype. Conversely, males selected for long life span became more female‐like, implying that IaSC results from genetic integration of this suite of traits. However, while life span, metabolism, and body mass showed correlated evolution in the sexes, activity did not evolve in males but, surprisingly, did so in females. This led to sexual monomorphism in locomotor activity in short‐life lines associated with detrimental effects in females. Our results thus support the general tenet that widespread pleiotropy generates IaSC despite sex‐specific genetic architecture.