X chromosome influences sperm length in the stalk-eyed fly Cyrtodiopsis dalmanni

Whether sexually selected traits are sex linked can have profound effects on their evolution. In the diopsid stalk-eyed fly, Cyrtodiopsis dalmanni, sperm length and female reproductive tract morphology have coevolved across species, postcopulatory sexual selection is known to occur, and X-linked genes affect female ventral sperm receptacle size. Here, we estimate the location of quantitative trait loci (QTL) for spermatocyst tail length by using F2 progeny segregating for an X-linked factor that causes sex-ratio meiotic drive. We found two QTL, including a major X-linked QTL responsible for 25% of the variation in spermatocyst tail length 2.1 cM from the sex-ratio element and 0.8 cM from a major eye span QTL. Sex-ratio males produce shorter spermatocyst tails and shorter eye spans. Thus, X-linked factors affect both pre- and postcopulatory traits, and linkage between the alleles for short eye span and short spermatocyst tail length allow pre- and postcopulatory sexual selection to potentially act in concert against the transmission bias caused by the sex-ratio chromosome.     

Correlated responses to selection on female egg size in male reproductive traits in a butterfly

Genetic correlations between male and female traits can act as evolutionary constraints and, if involving reproductive traits, potentially influence sexual selection. Artificial selection on egg size in the tropical butterfly Bicyclus anynana has yielded highly divergent lines. Here we report evidence for correlated evolution in male traits. Males from the large-egg selected lines produced significantly heavier spermatophores independent of body size and tended to have more fertile sperm stored in their reproductive tracts than those from the small-egg selected lines. This may be due to an underlying genetic correlation in reproductive effort between the sexes. However, non-fertile sperm number and testis size remained unaffected by selection on egg size. Phenotypic correlations within an unselected population revealed that spermatophore mass and fertile sperm number, but not testis size and non-fertile sperm number, were positively related to male body size, and that larger spermatophores contained more fertile, but not non-fertile sperm. In addition, males provided larger females with bigger spermatophores and more fertile sperm, indicating males may be exercising mate choice during copulation.     

Correlated evolution between targets of pre‐ and postcopulatory sexual selection across squamate reptiles

Sexual selection reflects the joint contributions of precopulatory selection, which arises from variance in mating success, and postcopulatory selection, which arises from variance in fertilization success. The relative importance of each episode of selection is variable among species, and comparative evidence suggests that traits targeted by precopulatory selection often covary in expression with those targeted by postcopulatory selection when assessed across species, although the strength and direction of this association varies considerably among taxa. We tested for correlated evolution between targets of pre‐ and postcopulatory selection using data on sexual size dimorphism (SSD) and testis size from 151 species of squamate reptiles (120 lizards, 31 snakes). In squamates, male–male competition for mating opportunities often favors large body size, such that the degree of male‐biased SSD is associated with the intensity of precopulatory selection. Likewise, competition for fertilization often favors increased sperm production, such that testis size (relative to body size) is associated with the intensity of postcopulatory selection. Using both conventional and phylogenetically based analyses, we show that testis size consistently decreases as the degree of male‐biased SSD increases across lizards and snakes. This evolutionary pattern suggests that strong precopulatory selection may often constrain the opportunity for postcopulatory selection and that the relative importance of each selective episode may determine the optimal resolution of energy allocation trade‐offs between traits subject to each form of sexual selection.     

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.     

Evolutionary reduction in testes size and competitive fertilization success in response to the experimental removal of sexual selection in dung beetles

Sexual selection is thought to favor the evolution of secondary sexual traits in males that contribute to mating success. In species where females mate with more than one male, sexual selection also continues after copulation in the form of sperm competition and cryptic female choice. Theory suggests that sperm competition should favor traits such as testes size and sperm production that increase a male's competitive fertilization success. Studies of experimental evolution offer a powerful approach for assessing evolutionary responses to variation in sexual selection pressures. Here we removed sexual selection by enforcing monogamy on replicate lines of a naturally polygamous horned beetle, Onthophagus taurus, and monitoring male investment in their testes for 21 generations. Testes size decreased in monogamous lines relative to lines in which sexual selection was allowed to continue. Differences in testes size were dependent on selection history and not breeding regime. Males from polygamous lines also had a competitive fertilization advantage when in sperm competition with males from monogamous lines. Females from polygamous lines produced sons in better condition, and those from monogamous lines increased their sons condition by mating polygamously. Rather than being costly for females, multiple mating appears to provide females with direct and/or indirect benefits. Neither body size nor horn size diverged between our monogamous and polygamous lines. Our data show that sperm competition does drive the evolution of testes size in onthophagine beetles, and provide general support for sperm competition theory.     

Artificial selection on male longevity influences age-dependent reproductive effort in the black field cricket Teleogryllus commodus

Although the trade-off between reproductive effort and longevity is central to both sexual selection and evolutionary theories of aging, there has been little synthesis between these fields. Here, we selected directly on adult longevity of male field crickets Teleogryllus commodus and measured the correlated responses of age-dependent male reproductive effort, female lifetime fecundity, and several other life-history traits. Male longevity responded significantly to five generations of divergent selection. Males from downward-selected lines commenced calling sooner and reached their peak calling effort at a younger age. They called more per night and, despite living less than half as long, called more overall than males selected for increased longevity. Females from the downward-selected lines lived significantly shorter lives than females from the upward-selected lines but still produced the same number of offspring. Nymph survival, development time, and body size and weight at eclosion did not show significant correlated response to selection on male longevity, despite evidence for substantial genetic variation in each of these traits. Collectively, our findings directly support the antagonistic pleiotropy model of aging and suggest an important role for sexual selection in the aging process.     

Different sexual traits show covariation among genotypes: implications for sexual selection

An unresolved question in sexual selection research is whetherdifferent secondary sexual traits are developmentally independentor instead whether their degree of expression is a manifestationof a general resource pool (i.e., condition) within the organism.If degree of expression of different sexual traits reflectsability to accumulate condition, then covariation should existacross genotypes in the expression of these traits, even ifthey are very different in kind. Here we present evidence forpredicted covariation between morphological (sex comb size)and behavioral (courtship song) sexual traits among geneticlines of Drosophila bipectinata Duda extracted from a naturalpopulation. There is evidence that both these traits in Drosophilaare condition dependent and subject to sexual selection. Wedetected significant body size–independent differencesin comb size among 32 lines. Replicate lines exhibiting relativelyhigh and low values of comb size were then subjected to analysesof courtship song. High sex comb lines exhibited shorter meanburst period and shorter mean burst duration than low sex comblines. These song differences occurred only during the distantpursuit phase of male courtship and existed despite factoringout individual variations in sex comb size, the trait on thebasis of which test lines were originally chosen. The resultsverify the prediction of an association between condition-dependentsecondary sexual traits across genotypes and, therefore, supportthe existence of an overall genetic quality related to conditionacquisition.     

Evolutionary dynamics of a sexual ornament in the house sparrow (Passer domesticus): the role of indirect selection within and between sexes

The relative contribution of sexual and natural selection to evolution of sexual ornaments has rarely been quantified under natural conditions. In this study we used a long-term dataset of house sparrows in which parents and offspring were matched genetically to estimate the within- and across-sex genetic basis for variation and covariation among morphological traits. By applying two-sex multivariate "animal models" to estimate genetic parameters, we estimated evolutionary changes in a male sexual ornament, badge size, from the contribution of direct and indirect selection on correlated traits within males and females, after accounting for overlapping generations and age-structure. Indirect natural selection on genetically correlated traits in males and females was the major force causing evolutionary change in the male ornament. Thus, natural selection on female morphology may cause indirect evolutionary changes in male ornaments. We observed however no directional phenotypic change in the ornament size of one-year-old males during the study period. On the other hand, changes were recorded in other morphological characters of both sexes. Our analyses of evolutionary dynamics in sexual characters require application of appropriate two-sex models to account for how selection on correlated traits in both sexes affects the evolutionary outcome of sexual selection.     

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.     

Experimental evaluation of the relationship between lethal or non-lethal virulence and transmission success in malaria parasite infections

Background

Theoretical studies suggest that direct and indirect selection have the potential to cause substantial evolutionary change in female mate choice. Similarly, sexual selection is considered a strong force in the evolution of male attractiveness and the exaggeration of secondary sexual traits. Few studies have, however, directly tested how female mate choice and male attractiveness respond to selection. Here we report the results of a selection experiment in which we selected directly on female mating preference for attractive males and, independently, on male attractiveness in the guppy, Poecilia reticulata. We measured the direct and correlated responses of female mate choice and male attractiveness to selection and the correlated responses of male ornamental traits, female fecundity and adult male and female survival.

Results

Surprisingly, neither female mate choice nor male attractiveness responded significantly to direct or to indirect selection. Fecundity did differ significantly among lines in a way that suggests a possible sexually-antagonistic cost to male attractiveness.

Conclusions

The opportunity for evolutionary change in female mate choice and male attractiveness may be much smaller than predicted by current theory, and may thus have important consequences for how we understand the evolution of female mate choice and male attractiveness. We discuss a number of factors that may have constrained the response of female choice and male attractiveness to selection, including low heritabilities, low levels of genetic (co)variation in the multivariate direction of selection, sexually-antagonistic constraint on sexual selection and the "environmental covariance hypothesis".

     

Can sexual selection drive female life histories? A comparative study on Galliform birds

Sexual selection has been identified as a major evolutionary force shaping male life history traits but its impact on female life history evolution is less clear. Here we examine the impact of sexual selection on three key female traits (body size, egg size and clutch size) in Galliform birds. Using comparative independent contrast analyses and directional discrete analyses, based on published data and a new genera-level supertree phylogeny of Galliform birds, we investigated how sexual selection [quantified as sexual size dimorphism (SSD) and social mating system (MS)] affects these three important female traits. We found that female body mass was strongly and positively correlated with egg size but not with clutch size, and that clutch size decreased as egg size increased. We established that SSD was related to MS, and then used SSD as a proxy of the strength of sexual selection. We found both a positive relationship between SSD and female body mass and egg size and that increases in female body mass and egg size tend to occur following increases in SSD in this bird order. This pattern of female body mass increases lagging behind changes in SSD, established using our directional discrete analysis, suggests that female body mass increases as a response to increases in the level of sexual selection and not simply through a strong genetic relationship with male body mass. This suggests that sexual selection is linked to changes in female life history traits in Galliformes and we discuss how this link may shape patterns of life history variation among species.     

Signal trait sexual dimorphism and mutual sexual selection in Drosophila serrata

Abstract The evolution of sexual dimorphism may occur when natural and sexual selection result in different optimum trait values for males and females. Perhaps the most prominent examples of sexual dimorphism occur in sexually selected traits, for which males usually display exaggerated trait levels, while females may show reduced expression of the trait. In some species, females also exhibit secondary sexual traits that may either be a consequence of a correlated response to sexual selection on males or direct sexual selection for female secondary sexual traits. In this experiment, we simultaneously measure the intersex genetic correlations and the relative strength of sexual selection on males and females for a set of cuticular hydrocarbons in Drosophila serrata . There was significant directional sexual selection on both male and female cuticular hydrocarbons: the strength of sexual selection did not differ among the sexes but males and females preferred different cuticular hydrocarbons. In contrast with many previous studies of sexual dimorphism, intersex genetic correlations were low. The evolution of sexual dimorphism in D. serrata appears to have been achieved by sex-limited expression of traits controlled by genes on the X chromosome and is likely to be in its final stages.     

Sequential mate encounters: female but not male body size influences female remating behavior

Whether and how individuals choose sequentially among matesis an important but largely neglected aspect in sexual selectionstudies. Here, we explore female remating behavior in the cellarspider Pholcus phalangioides. We focus on body size as one ofthe most important traits involved in mate choice. Large andsmall females (n = 216) were double mated with large or smallmales in all eight possible combinations. All females copulatedwhen virgin, but only 82% accepted a second male. The chanceof a female remating was not significantly predicted by thebody size of the second or first male or by the size differencebetween the two. In contrast, a previous study demonstrateda male size effect in that larger males monopolized femalesuntil egg laying when two males of different sizes were present.We suggest that sequential encounters are more common undernatural conditions than male monopolization of females becauseestimates of concurrent multiple paternity together with observationsin a natural population do not favor mate guarding as the predominantmating strategy in this species. It follows from our study thatthe intensity of sexual selection on male size may be greatlyoverestimated when using a competitive laboratory setting fora species in which females generally encounter mates in a sequentialfashion. Female remating probability was significantly predictedby female size, with large females remating with higher probabilitythan small females. Thus, when mating with large females, malesmay gain higher fertilization success through increased femalefecundity but also face a higher sperm competition risk.     

No fecundity cost of female secondary sexual trait expression in the horned beetle Onthophagus sagittarius

Typically males bear the products of sexual selection in the form of ornaments and/or weapons used to compete for and attract females. Secondary sexual traits in females have been thought of as the product of correlated responses to sexual selection on males. However, there is increasing phylogenetic evidence that female secondary sexual traits can arise independently of selection on males, and may be subject to sexual selection. Theoretical models of the evolution of female ornamentation via male mate choice have assumed that females suffer a cost of ornament expression via reduced fecundity, and hence female ornaments are less likely to evolve than male ornaments. In the dung beetle Onthophagus sagittarius, there has been an independent evolutionary origin of horns in females that are qualitatively different from the horns produced by males. We use this system as a model to examine the costs of horn expression for females within a life-history context. We identified a longevity cost of reproduction for females that was independent of horn expression. Large females lived longer, and after controlling for lifespan, had a higher lifetime fecundity, and invested more heavily in maternal provisioning than did small females. We found no evidence of a cost to females of investment in horns. Rather, the rate of increase in fecundity and horn expression with body size were equal, so that absolute horn size provides an accurate indicator of body size and maternal quality. The effects we observe were independent of female contest competition and/or male mate choice, which were excluded in our experimental protocol. However, we speculate on the potential functional contributions female horns might make to female fitness.     

Coevolution of male and female reproductive structures in Drosophila

The morphology of male genitalia whilst stable within species, exhibits huge interspecific variation. This variation is likely to be as a result of sexual selection due to the direct involvement of these reproductive structures in mating and sperm transfer. In contrast, internal soft tissue components of the genitalia are generally poorly investigated as they are not directly involved in physical and mechanical adequacy during sperm transfer. However, these soft tissue structures may also drive differential male–female interactions, particularly in internally fertilising organisms where females have the ability to store sperm and bias male reproductive success. In this paper we use the drosophila model to investigate the role of male and female reproductive elements in sexual selection. Our meta-analysis supplemented with additional new data clearly shows that within species, sperm length versus testis length, and sperm length versus seminal receptacle length, are highly correlated. Thus, independent of the phylogenetic relationship among species, gamete evolution is likely to result in sexual selection interactions that drive the evolution of internal reproductive components in both sexes. Our results and discussion of the literature highlight the importance of considering internal soft structures that may influence fertilisation, when investigating selective forces acting on the evolution of reproductive traits.     

A quantitative genetic analysis of male sexual traits distinguishing the sibling species Drosophila simulans and D. sechellia

A quantitative trait locus (QTL) genetic analysis of morphological and reproductive traits distinguishing the sibling species Drosophila simulans and D. sechellia was carried out in a backcross design, using 38 markers with an average spacing of 8.4 cM. The direction of QTL effects for the size of the posterior lobe was consistent across the identified QTL, indicating directional selection for this trait. Directional selection also appears to have acted on testis length, indicating that sexual selection may have influenced many reproductive traits, although other forms of directional selection cannot be ruled out. Sex comb tooth number exhibited high levels of variation both within and among isofemale lines and showed no evidence for directional selection and, therefore, may not have been involved in the early speciation process. A database search for genes associated with significant QTL revealed a set of candidate loci for posterior lobe shape and size, sex comb tooth number, testis length, tibia length, and hybrid male fertility. In particular, decapentaplegic (dpp), a gene known to influence the genital arch, was found to be associated with the largest LOD peak for posterior lobe shape and size.     

Contemporary sexual selection does not explain variation in male display traits among populations

Sexual selection is widely hypothesized to facilitate the evolution of reproductive isolation through divergence in sexual traits and sexual trait preferences among populations. However, direct evidence of divergent sexual selection causing intraspecific trait divergence remains limited. Using the wolf spider Schizocosa crassipes, we characterized patterns of female mate choice within and among geographic locations and related those patterns to geographic variation in male display traits to test whether divergent sexual selection caused by mate choice explains intraspecific trait variation. We found evidence of phenotypic selection on male behavior arising from female mate choice, but no evidence that selection varied among locations. Only those suites of morphological and behavioral traits that did not influence mate choice varied geographically. These results are inconsistent with ongoing divergent sexual selection underlying the observed intraspecific divergence in male display traits. These findings align with theory on the potentially restrictive conditions under which divergent sexual selection may persist, and suggest that long‐term studies capable of detecting periodic or transient divergent sexual selection will be critical to rigorously assess the relative importance of divergent sexual selection in intraspecific trait divergence.     

Male choice generates stabilizing sexual selection on a female fecundity correlate

We know very little about male mating preferences and how they influence the evolution of female traits. Theory predicts that males may benefit from choosing females on the basis of traits that indicate their fecundity. Here, we explore sexual selection generated by male choice on two components of female body size (wing length and body mass) in Drosophila serrata. Using a dietary manipulation to alter female size and 828 male mate choice trials, we analysed linear and nonlinear sexual selection gradients on female mass and wing length. In contrast to theoretical expectations and prevailing empirical data, males exerted stabilizing rather than directional sexual selection on female body mass, a correlate of fecundity. Sexual selection was detected only among females with access to standard resource levels as an adult, with no evidence for sexual selection among resource-depleted females. Thus the mating success of females with the same body mass differed depending upon their access to resources as an adult. This suggests that males in this species may rely on signal traits to assess body mass rather than assessing it directly. Stabilizing rather than directional sexual selection on body mass together with recent evidence for stabilizing sexual selection on candidate signal traits in this species suggests that females may trade-off resources allocated to reproduction and sexual signalling.     

Intraspecific evidence from guppies for correlated patterns of male and female genital trait diversification

The role of sexual selection in fuelling genital evolution is becoming increasingly apparent from comparative studies revealing interspecific divergence in male genitalia and evolutionary associations between male and female genital traits. Despite this, we know little about intraspecific variance in male genital morphology, or how male and female reproductive traits covary among divergent populations. Here we address both topics using natural populations of the guppy, Poecilia reticulata, a livebearing fish that exhibits divergent patterns of male sexual behaviour among populations. Initially, we performed a series of mating trials on a single population to examine the relationship between the morphology of the male's copulatory organ (the gonopodium) and the success of forced matings. Using a combination of linear measurements and geometric morphometrics, we found that variation in the length and shape of the gonopodium predicted the success of forced matings in terms of the rate of genital contacts and insemination success, respectively. We then looked for geographical divergence in these traits, since the relative frequency of forced matings tends to be greater in high-predation populations. We found consistent patterns of variation in male genital size and shape in relation to the level of predation, and corresponding patterns of (co)variation in female genital morphology. Together, these data enable us to draw tentative conclusions about the underlying selective pressures causing correlated patterns of divergence in male and female genital traits, which point to a role for sexually antagonistic selection.     

Sexual size dimorphism and reproductive ecology in relation to mating system in waders

The relationship between sexual size dimorphism, body-weight and different reproductive traits (e.g. clutch size, egg weight and incubation period) in relation to mating system and forms of parental care was studied in waders. Two hypotheses were examined. (1) Sexual size dimorphism is correlated with the intensity of sexual selection. (2) The degree of sexual size dimorphism is the result of an interrelationship between the reproductive strategy of the female and her body size. In the polygynous species the male was significantly larger than the female. This is consistent with the sexual selection hypothesis. However, among waders, a positive correlation exists between egg weight, clutch mass and body-weight. Selection for small eggs or a short incubation period may therefore have an influence on female body-weight. If the lack of paternal care reduces the female's possibility for producing large eggs or incubating a large clutch mass, we would expect a selection pressure for small female size among polygynous species. Thus, large sexual size dimorphism among polygynous waders may be a result of selection for small female size to lack of paternal care, or selection for large male size due to intramale competition or a female preference for large-sized males. In multiple-clutch species (viz. species in which the female regularly lays more than one clutch during the season) egg weight was low both for a given female and male body-weight. The low egg weight of multiple-clutch species is assumed to be a result of the constraints placed on the female from producing several clutches during a single breeding season.