Selection on learning performance results in the correlated evolution of sexual dimorphism in life history

The evolution of learning can be constrained by trade‐offs. As male and female life histories often diverge, the relationship between learning and fitness may differ between the sexes. However, because sexes share much of their genome, intersexual genetic correlations can prevent males and females from reaching their sex‐specific optima resulting in intralocus sexual conflict (IaSC). To investigate if IaSC constraints sex‐specific evolution of learning, we selected Caenorhabditis remanei nematode females for increased or decreased olfactory learning performance and measured learning, life span (in mated and virgin worms), reproduction, and locomotory activity in both sexes. Males from downward‐selected female lines had higher locomotory activity and longer virgin life span but sired fewer progeny than males from upward‐selected female lines. In contrast, we found no effect of selection on female reproduction and downward‐selected females showed higher locomotory activity but lived shorter as virgins than upward‐selected females. Strikingly, selection on learning performance led to the reversal of sexual dimorphism in virgin life span. We thus show sex‐specific trade‐offs between learning, reproduction, and life span. Our results support the hypothesis that selection on learning performance can shape the evolution of sexually dimorphic life histories via sex‐specific genetic correlations.     

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

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

Sexual coevolution in the traumatically inseminating plant bug genus Coridromius

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

Interactions among mechanisms of sexual selection on male body size and head shape in a sexually dimorphic fly

Abstract Darwin envisaged male-male and male-female interactions as mutually supporting mechanisms of sexual selection, in which the best armed males were also the most attractive to females. Although this belief continues to predominate today, it has been challenged by sexual conflict theory, which suggests that divergence in the interests of males and females may result in conflicting sexual selection. This raises the empirical question of how multiple mechanisms of sexual selection interact to shape targeted traits. We investigated sexual selection on male morphology in the sexually dimorphic fly Prochyliza xanthostoma , using indices of male performance in male-male and male-female interactions in laboratory arenas to calculate gradients of direct, linear selection on male body size and an index of head elongation. In male-male combat, the first interaction with a new opponent selected for large body size but reduced head elongation, whereas multiple interactions with the same opponent favored large body size only. In male-female interactions, females preferred males with relatively elongated heads, but male performance of the precopulatory leap favored large body size and, possibly, reduced head elongation. In addition, the amount of sperm transferred (much of which is ingested by females) was an increasing function of both body size and head elongation. Thus, whereas both male-male and male-female interactions favored large male body size, male head shape appeared to be subject to conflicting sexual selection. We argue that conflicting sexual selection may be a common result of divergence in the interests of the sexes.     

RAPID LOSS OF BEHAVIORAL PLASTICITY AND IMMUNOCOMPETENCE UNDER INTENSE SEXUAL SELECTION

Phenotypic plasticity allows animals to maximize fitness by conditionally expressing the phenotype best adapted to their environment. Although evidence for such adjustment in reproductive tactics is common, little is known about how phenotypic plasticity evolves in response to sexual selection. We examined the effect of sexual selection intensity on phenotypic plasticity in mating behavior using the beetle Callosobruchus maculatus. Male genital spines harm females during mating and females exhibit copulatory kicking, an apparent resistance trait aimed to dislodge mating males. After exposing individuals from male‐ and female‐biased experimental evolution lines to male‐ and female‐biased sociosexual environments, we examined behavioral plasticity in matings with standard partners. While females from female‐biased lines kicked sooner after exposure to male‐biased sociosexual contexts, in male‐biased lines this plasticity was lost. Ejaculate size did not diverge in response to selection history, but males from both treatments exhibited plasticity consistent with sperm competition intensity models, reducing size as the number of competitors increased. Analysis of immunocompetence revealed reduced immunity in both sexes in male‐biased lines, pointing to increased reproductive costs under high sexual selection. These results highlight how male and female reproductive strategies are shaped by interactions between phenotypically plastic and genetic mechanisms of sexual trait expression.     

Precopulatory but not postcopulatory male reproductive traits diverge in response to mating system manipulation in Drosophila melanogaster

Competition between males creates potential for pre‐ and postcopulatory sexual selection and conflict. Theory predicts that males facing risk of sperm competition should evolve traits to secure their reproductive success. If those traits are costly to females, the evolution of such traits may also increase conflict between the sexes. Conversely, under the absence of sperm competition, one expectation is for selection on male competitive traits to relax thereby also relaxing sexual conflict. Experimental evolution studies are a powerful tool to test this expectation. Studies in multiple insect species have yielded mixed and partially conflicting results. In this study, we evaluated male competitive traits and male effects on female costs of mating in Drosophila melanogaster after replicate lines evolved for more than 50 generations either under enforced monogamy or sustained polygamy, thus manipulating the extent of intrasexual competition between males. We found that in a setting where males competed directly with a rival male for access to a female and fertilization of her ova polygamous males had superior reproductive success compared to monogamous males. When comparing reproductive success solely in double mating standard sperm competition assays, however, we found no difference in male sperm defense competitiveness between the different selection regimes. Instead, we found monogamous males to be inferior in precopulatory competition, which indicates that in our system, enforced monogamy relaxed selection on traits important in precopulatory rather than postcopulatory competition. We discuss our findings in the context of findings from previous experimental evolution studies in Drosophila ssp. and other invertebrate species.     

Hind Wing Shape Evolves Faster than Front Wing Shape in Calopteryx Damselflies

Wing shape has been shown in a variety of species to be influenced by natural and sexual selection. In damselflies, front- and hind wings can beat independently, and functional differentiation may occur. Males of Calopteryx damselflies show species-specific nuptial flights that differ in colour signalling with the hind wings. Therefore, hind wing shape and colour may evolve in concert to improve colour display, independent of the front wings. We predicted that male hind wing shape evolves faster than front wing shape, due to sexual selection. Females do not engage in sexual displays, so we predicted that females do not show differences in divergence between front- and hind wing shape. We analysed the non-allometric component of wing shape of five European Calopteryx taxa using geometric morphometrics. We found a higher evolutionary divergence of hind wing shape in both sexes. Indeed, we found no significant differences in rate of evolution between the sexes, despite clear sex-specific differences in wing shape. We suggest that evolution of hind wing shape in males is accelerated by sexual selection on pre-copulatory displays and that this acceleration is reflected in females due to genetic correlations that somehow link the rates of wing shape evolution in the two sexes, but not the wing shapes themselves.     

Sex-specific trait architecture in a spider with sexual size dimorphism

Sexual dimorphism, or sex-specific trait expression, may evolve when selection favours different optima for the same trait between sexes, that is, under antagonistic selection. Intra-locus sexual conflict exists when the sexually dimorphic trait under antagonistic selection is based on genes shared between sexes. A common assumption is that the presence of sexual-size dimorphism (SSD) indicates that sexual conflict has been, at least partly, resolved via decoupling of the trait architecture between sexes. However, whether and how decoupling of the trait architecture between sexes has been realized often remains unknown. We tested for differences in architecture of adult body size between sexes in a species with extreme SSD, the African hermit spider (Nephilingis cruentata), where adult female body size greatly exceeds that of males. Specifically, we estimated the sex-specific importance of genetic and maternal effects on adult body size among individuals that we laboratory-reared for up to eight generations. Quantitative genetic model estimates indicated that size variation in females is to a larger extent explained by direct genetic effects than by maternal effects, but in males to a larger extent by maternal than by genetic effects. We conclude that this sex-specific body-size architecture enables body-size evolution to proceed much more independently than under a common architecture to both sexes.     

Field estimates of parentage reveal sexually antagonistic selection on body size in a population of Anolis lizards

Sexual dimorphism evolves when selection favors different phenotypic optima between the sexes. Such sexually antagonistic selection creates intralocus sexual conflict when traits are genetically correlated between the sexes and have sex‐specific optima. Brown anoles are highly sexually dimorphic: Males are on average 30% longer than females and 150% heavier in our study population. Viability selection on body size is known to be sexually antagonistic, and directional selection favors large male size whereas stabilizing selection constrains females to remain small. We build on previous studies of viability selection by measuring sexually antagonistic selection using reproductive components of fitness over three generations in a natural population of brown anoles. We estimated the number of offspring produced by an individual that survived to sexual maturity (termed RS^V), a measure of individual fitness that includes aspects of both individual reproductive success and offspring survival. We found directional selection on male body size, consistent with previous studies of viability selection. However, selection on female body size varied among years, and included periods of positive directional selection, quadratic stabilizing selection, and no selection. Selection acts differently in the sexes based on both survival and reproduction and sexual conflict appears to be a persistent force in this species.     

Female behaviour and the interaction of male and female genital traits mediate sperm transfer during mating

Natural selection and post‐copulatory sexual selection, including sexual conflict, contribute to genital diversification. Fundamental first steps in understanding how these processes shape the evolution of specific genital traits are to determine their function experimentally and to understand the interactions between female and male genitalia during copulation. Our experimental manipulations of male and female genitalia in red‐sided garter snakes (Thamnophis sirtalis parietalis) reveal that copulation duration and copulatory plug deposition, as well as total and oviductal/vaginal sperm counts, are influenced by the interaction between male and female genital traits and female behaviour during copulation. By mating females with anesthetized cloacae to males with spine‐ablated hemipenes using a fully factorial design, we identified significant female–male copulatory trait interactions and found that females prevent sperm from entering their oviducts by contracting their vaginal pouch. Furthermore, these muscular contractions limit copulatory plug size, whereas the basal spine of the male hemipene aids in sperm and plug transfer. Our results are consistent with a role of sexual conflict in mating interactions and highlight the evolutionary importance of female resistance to reproductive outcomes.     

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.     

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.     

Sexual dimorphism in wing beat frequency in relation to eye span in stalk‐eyed flies (Diopsidae)

Although male ornaments may provide benefits to individuals bearing them, such structures may also entail fitness costs. Selection should favour aspects of the phenotype that act to reduce such costs, yet such compensatory traits are often ignored in studies of sexual selection. If a male ornament increases predation risk via reduced locomotor performance, then there may be selection for changes in morphological traits to compensate for behavioural or biomechanical changes in how individuals use their morphology (or both). We took a comparative approach aiming to test whether changes in wing beat frequency are evolutionarily correlated with increases in male ornamentation across stalk‐eyed fly species. Previous studies have shown that increased male eye span is evolutionarily correlated with increased wing size; thus, we tested whether there is additional compensation via increases in size‐adjusted wing beat frequency. The results obtained revealed that relative wing beat frequency is negatively related to relative eye span in males, and sexual dimorphism in wing beat frequency is negatively related to dimorphism in eye span. These findings, in addition to our finding that eye span dimorphism is positively related to aspect ratio dimorphism, suggest that male stalk‐eyed flies compensate primarily by increasing wing size and shape, which may then have resulted in the subsequent evolutionary reduction in wing beat frequency. Thus, exaggerated ornaments can result in evolutionary modifications in wing morphology, which in turn lead to adjustments in flapping kinematics, illustrating the tight envelope of trade‐offs when compensating for exaggerated ornaments. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 670–679.     

Intraspecific mating system evolution and its effect on complex male secondary sexual traits: Does male–male competition increase selection on size or shape?

Sexual selection is generally held responsible for the exceptional diversity in secondary sexual traits in animals. Mating system evolution is therefore expected to profoundly affect the covariation between secondary sexual traits and mating success. Whereas there is such evidence at the interspecific level, data within species remain scarce. We here investigate sexual selection acting on the exaggerated male fore femur and the male wing in the common and widespread dung flies Sepsis punctum and S. neocynipsea (Diptera: Sepsidae). Both species exhibit intraspecific differences in mating systems and variation in sexual size dimorphism (SSD) across continents that correlates with the extent of male–male competition. We predicted that populations subject to increased male–male competition will experience stronger directional selection on the sexually dimorphic male foreleg. Our results suggest that fore femur size, width and shape were indeed positively associated with mating success in populations with male‐biased SSD in both species, which was not evident in conspecific populations with female‐biased SSD. However, this was also the case for wing size and shape, a trait often assumed to be primarily under natural selection. After correcting for selection on overall body size by accounting for allometric scaling, we found little evidence for independent selection on any of these size or shape traits in legs or wings, irrespective of the mating system. Sexual dimorphism and (foreleg) trait exaggeration is therefore unlikely to be driven by direct precopulatory sexual selection, but more so by selection on overall size or possibly selection on allometric scaling.     

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.     

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.     

Cross‐sex genetic covariances limit the evolvability of wing‐shape within and among species of Drosophila

The independent evolution of males and females is potentially constrained by both sexes inheriting the same alleles from their parents. This genetic constraint can limit the evolvability of complex traits; however, there are few studies of multivariate evolution that incorporate cross‐sex genetic covariances in their predictions. Drosophila wing‐shape has emerged as a model high‐dimensional phenotype; wing‐shape is highly evolvable in contemporary populations, and yet perplexingly stable across phylogenetic timescales. Here, we show that cross‐sex covariances in Drosophila melanogaster, given by the B ‐matrix, may considerably bias wing‐shape evolution. Using random skewers, we show that B would constrain the response to antagonistic selection by 90%, on average, but would double the response to concordant selection. Both cross‐sex within‐trait and cross‐sex cross‐trait covariances determined the predicted response to antagonistic selection, but only cross‐sex within‐trait covariances facilitated the predicted response to concordant selection. Similar patterns were observed in the direction of extant sexual dimorphism in D. melanogaster, and in directions of most and least dimorphic variation across the Drosophila phylogeny. Our results highlight the importance of considering between‐sex genetic covariances when making predictions about evolution on both macro‐ and microevolutionary timescales, and may provide one more explanatory piece in the puzzle of stasis.     

Subtle,pervasive genetic correlation between the sexes in the evolution of dimorphic hummingbird tail ornaments*

Male hummingbirds have repeatedly evolved sexually dimorphic tails that they use as ornaments during courtship. We examine how male ornament evolution is reflected in female morphology. Lande's two-step model of the evolution of dimorphism predicts that γ (the genetic correlation between the sexes) causes trait elaboration to first evolve quickly in both sexes, then dimorphism evolves more slowly. On the hummingbird phylogeny, tail length does not fit this two-step model; although hummingbirds repeatedly evolved ornamental, elongated tails, dimorphism evolves on the same phylogenetic branch as elongation, implying that γ quickly evolves to be low over phylogenetic timescales. Male “bee” hummingbirds have evolved diverse rectrix shapes that they use to produce sound. Female morphologies exhibit subtle, pervasive correlations with male morphology. No female-adaptive hypotheses explain these correlations, since females do not also make sounds with their tail. Subtle shape similarity has arisen through the genetic correlation with males, and is subject to intralocus sexual conflict. Intralocus sexual conflict may produce increased phenotypic variation of female ornaments. Other evolutionary constraints on tail morphology include a developmental correlation between neighboring tail-feathers, biasing tail elaboration to occur most often at the ends of the feather tract (rectrix 5 or 1) and not the middle.     

Sexual conflict and environmental change: trade-offs within and between the sexes during the evolution of desiccation resistance

Intralocus sexual conflict occurs when males and females experience sex-specific selection on a shared genome. With several notable exceptions, intralocus sexual conflict has been investigated in constant environments to which the study organisms have had an opportunity to adapt. However, a change in the environment can result in differential or even opposing selection pressures on males and females, creating sexual conflict. We used experimental evolution to explore the interaction between intralocus sexual conflict, sexual dimorphism and environmental variation in Drosophila melanogaster. Six populations were selected for adult desiccation resistance (D), with six matched control populations maintained in parallel (C). After 46 generations, the D populations had increased in survival time under arid conditions by 68% and in body weight by 20% compared to the C populations. The increase in size was the result of both extended development and faster growth rate of D juveniles. Adaptation to the stress came at a cost in terms of preadult viability and female fecundity. Because males are innately less tolerant of desiccation stress, very few D males survived desiccation-selection; while potentially a windfall for survivors, these conditions mean that most males’ fitness was determined posthumously. We conjectured that selection for early maturation and mating in males was in conflict with selection for survival and later reproduction in females. Consistent with this prediction, the sexes showed different patterns of age-specific desiccation resistance and resource acquisition, and there was a trend towards increasingly female-biased sexual size dimorphism. However, levels of desiccation resistance were unaffected, with D males and females increasing in parallel. Either there is a strong positive genetic correlation between the sexes that limits independent evolution of desiccation resistance, or fitness pay-offs from the strategy of riding out the stress bout are great enough to sustain concordant selection on the two sexes. We discuss the forces that mould fitness in males under a regimen where trade-offs between survival and reproduction may be considerable.