Operational sex ratio influences the opportunity for sexual selection in guppies

The opportunity for sexual selection was greater when the operational sex ratio (OSR) in guppies Poecilia reticulata was biased towards males. This could be due to an increase in both male-male competition and female mate choice under male-biased OSR.     

Seasonal change in the opportunity for sexual selection

Environmental and population parameters that influence the strength of sexual selection may vary considerably over the course of the reproductive season. However, the potential for sexual selection frequently fails to translate into variation in reproductive success among individuals. We investigated seasonal changes in variation in reproductive success, measured as the opportunity for sexual selection, using parentage analysis in 20 experimental populations of the European bitterling (Rhodeus amarus, Cyprinidae), a small freshwater fish with a promiscuous, resource-based mating system. We showed that although the largest males sired most offspring over the entire reproductive season, variation in reproductive success and hence the opportunity for sexual selection was low at the start of the season but increased significantly at its end. This seasonal difference probably arose from the superior competitive endurance of large males and from a higher temporal clustering of reproductively active females at the start of the breeding season than later in the season. The spatial distribution of oviposition sites had a negligible effect on the variation in reproductive success. We discuss the potential implications of our results for the importance and strength of sexual selection in natural populations.     

The total opportunity for sexual selection and the integration of pre‐ and post‐mating episodes of sexual selection in a complex world

It is well known that sexual selection can target reproductive traits during successive pre‐ and post‐mating episodes of selection. A key focus of recent studies has been to understand and quantify how these episodes of sexual selection interact to determine overall variance in reproductive success. In this article, we review empirical developments in this field but also highlight the considerable variability in patterns of pre‐ and post‐mating sexual selection, attributable to variation in patterns of resource acquisition and allocation, ecological and social factors, genotype‐by‐environment interaction and possible methodological factors that might obscure such patterns. Our aim is to highlight how (co)variances in pre‐ and post‐mating sexually selected traits can be sensitive to changes in a range of ecological and environmental variables. We argue that failure to capture this variation when quantifying the opportunity for sexual selection may lead to erroneous conclusions about the strength, direction or form of sexual selection operating on pre‐ and post‐mating traits. Overall, we advocate for approaches that combine measures of pre‐ and post‐mating selection across contrasting environmental or ecological gradients to better understand the dynamics of sexual selection in polyandrous species. We also discuss some directions for future research in this area.     

Long-term paternity skew and the opportunity for selection in a mammal with reversed sexual size dimorphism

Most mammalian groups are characterized by male-biased sexual size dimorphism, in which size-dependent male-male competition and reproductive skew are tightly linked. By comparison, little is known about the opportunity for sexual selection in mammalian systems without male-biased dimorphism, where the traits under sexual selection might be less obvious. We examined 10 years of parentage data in a colony of greater horseshoe bats (Rhinolophus ferrumequinum) to determine the magnitude of male reproductive skew and the opportunity for sexual selection in a mammal in which females are the larger sex. Annual paternity success was weakly skewed but consistent patterns led to strong longitudinal paternity skew among breeders. Just three males accounted for a third of all paternity assignments, representing at least a fifth of all colony offspring born in a decade. Paternity success was in part determined by age but was not influenced by dispersal status. Our results show that paternity skew and the opportunity for sexual selection in a species with reversed sexual size dimorphism can approach levels reported for classical examples of species with polygyny and male-biased dimorphism, even where the traits under sexual selection are not known.     

Quantifying sexual selection: a comparison of competing indices with mating system data from a terrestrially breeding salamander

Calculations for quantifying the potential for sexual selection remain controversial. Many indices have been promoted in the literature, but each has unique sets of advantages and disadvantages. Using marbled salamanders, I evaluated the performance of several measures by manipulating intensity of sexual selection in experimental breeding replicates of varying operational sex ratio. Theory predicts that sexual selection among males will be higher when sex ratio is male‐biased and lower when female‐biased. I used microsatellite data to assign hatchling parentage, estimate adult fitness, and calculate several indices of inequality for quantifying sexual selection. Opportunity for selection and Morisita index always conformed to theoretical expectations, which was not the case for index of resource monopolization, standardized Morisita index, or binomial skew index. Although I conclude that opportunity for selection is advantageous in sexual selection studies because of its link to formal theory, this should be tested against the null hypothesis of random variation in ambiguous cases. In the present study, although variation in both reproductive and mating success was high when quantified using opportunities for selection, it was only significantly greater than random expectations for reproductive success. This study provides further empirical support for the continued use of opportunity for selection in sexual selection studies. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 73–83.     

Extrapair paternity and the opportunity for sexual selection in a socially monogamous passerine

Effects of alternate mating strategies on the opportunity forsexual selection are widely debated, and recent studies haveconcluded that the effects of extrapair (EP) paternity on theopportunity for sexual selection may have been overstated dueto 1) methodological limitations of empirical studies and 2)the potential for males to gain from additional within-pair(WP) reproductive opportunities. We therefore examined the impactof EP paternity on the opportunity for sexual selection in thesocially monogamous and single-brooded eastern kingbird (Tyrannustyrannus). EP paternity was common in all 3 years of our study(61% of 89 broods, 47% of nestlings) and realized reproductivesuccess (EP + WP young) ranged from 0 to 9 young/male/year.A total of 31% of males lost all WP paternity (24% sired neitherWP nor EP young, whereas 7% sired EP but not WP young), andvariance in male realized reproductive success was more than9 times greater than that of apparent reproductive success.Nearly half of EP mates were not nearest neighbors, and manywere separated by 3 or more territories (>1000 m). EP successwas independent of nest defense behavior, but early singingmales and males with high song rates were most successful atboth a population level and when cuckolders and cuckoldees werecompared. EP paternity contributed significantly to the opportunityfor sexual selection in kingbirds, and we suggest that thisis probably due to the low potential for WP variation in reproductivesuccess, apparent long-distance movements of one or both sexes,and consequent absence of reciprocal cuckoldry.     

The mismeasurement of sexual selection

Sexual selection can explain major micro‐ and macro‐evolutionary patterns. Much of current theory predicts that the strength of sexual selection (i) is driven by the relative abundance of males and females prepared to mate (i.e. the operational sex ratio, OSR) and (ii) can be generally estimated by calculating intra‐sexual variation in mating success (e.g. the opportunity for sexual selection, I_s). Here, we demonstrate the problematic nature of these predictions. The OSR and I_s only accurately predict sexual selection under a limited set of circumstances, and more specifically, only when mate monopolization is extremely strong. If mate monopolization is not strong, using OSR or I_s as proxies or measures of sexual selection is expected to produce spurious results that lead to the false conclusion that sexual selection is strong when it is actually weak. These findings call into question the validity of empirical conclusions based on these measures of sexual selection.     

High opportunity for postcopulatory sexual selection under field conditions

In polygamous systems, male fitness is determined not only by mating success but also by fertilization success. Despite the growing interest over the past several decades in postcopulatory sexual selection, its relative importance compared to precopulatory sexual selection remains a subject of debate. Here, we use extensive behavioral observations of a seminatural population of Hawaiian swordtail crickets, Laupala cerasina, and molecular paternity assignment to measure the opportunities for pre‐ and postcopulatory selection. Because postcopulatory selection has the potential to operate at multiple stages, we also separately attribute its effects to factors specific to mating events versus factors specific to males. We find that variance in postcopulatory success is over four times as great as variance in precopulatory success, with most of it unexplained by male mating order or the number of nuptial gifts given. Surprisingly, we also find that male singing effort is under postcopulatory selection, suggesting that males who sing more frequently also have more competitive ejaculates. Our results are consistent with the hypothesis that high polyandry levels promote greater relative postcopulatory selection. They also highlight the need for detailed behavioral observations under conditions as natural as possible when measuring mating and reproductive success.     

The opportunity to be misled in studies of sexual selection

It is a challenge to measure sexual selection because both stochastic events (chance) and deterministic factors (selection) generate variation in individuals' reproductive success. Most researchers realize that random events ('noise') make it difficult to detect a relationship between a trait and mating success (i.e. the presence of sexual selection). There is, however, less appreciation of the dangers that arise if stochastic events vary systematically. Systematic variation makes variance-based approaches to measuring the role of selection problematic. This is why measuring the opportunity for sexual selection (I(s) and I(mates)) is so vulnerable to misinterpretation. Although I(s) does not measure actual sexual selection (because it includes stochastic variation in mating/fertilization success) it is often implicitly assumed that it will be correlated with the actual strength of sexual selection. The hidden assumption is that random noise is randomly distributed across populations, species or the sexes. Here we present a simple numerical example showing why this practice is worrisome. Specifically, we show that chance variation in mating success is higher when there are fewer potential mates per individual of the focal sex [i.e. when the operational sex ratio (OSR), is more biased]. This will lead to the OSR covarying with I(s) even when the strength of sexual selection is unaffected by the OSR. This can generate false confidence in identifying factors that determine variation in the strength of sexual selection. We emphasize that in nature, even when sexual selection is strong, chance variation in mating success is still inevitable because the number of mates per individual is a discrete number. We hope that our worked example will clarify a recent debate about how best to measure sexual selection.     

Female-specific resource limitation does not make the opportunity for selection more female biased

Competition for limiting resources and stress can magnify variance in fitness and therefore selection. But even in a common environment, the strength of selection can differ across the sexes, as their fitness is often limited by different factors. Indeed, most taxa show stronger selection in males, a bias often ascribed to intense competition for access to mating partners. This sex bias could reverberate on many aspects of evolution, from speed of adaptation to genome evolution. It is unclear, however, whether stronger opportunity for selection in males is a pattern robust to sex-specific stress or resource limitation. We test this in the model species Callosobruchus maculatus by comparing female and male opportunity for selection (i) with and without limitation of quality oviposition sites, and (ii) under delayed age at oviposition. Decreasing the abundance of the resource key to females or increasing their reproductive age was challenging, as shown by a reduction in mean fitness, but opportunity for selection remained stronger in males across all treatments, and even more so when oviposition sites were limiting. This suggests that males remain the more variable sex independent of context, and that the opportunity for selection through males is indirectly affected by female-specific resource limitation.     

Sexual selection and sexual size dimorphism in animals

Sexual selection is often considered as a critical evolutionary force promoting sexual size dimorphism (SSD) in animals. However, empirical evidence for a positive relationship between sexual selection on males and male-biased SSD received mixed support depending on the studied taxonomic group and on the method used to quantify sexual selection. Here, we present a meta-analytic approach accounting for phylogenetic non-independence to test how standardized metrics of the opportunity and strength of pre-copulatory sexual selection relate to SSD across a broad range of animal taxa comprising up to 95 effect sizes from 59 species. We found that SSD based on length measurements was correlated with the sex difference in the opportunity for sexual selection but showed a weak and statistically non-significant relationship with the sex difference in the Bateman gradient. These findings suggest that pre-copulatory sexual selection plays a limited role for the evolution of SSD in a broad phylogenetic context.     

Dietary stress increases the total opportunity for sexual selection and modifies selection on condition‐dependent traits

Although it is often expected that adverse environmental conditions depress the expression of condition‐dependent sexually selected traits, the full consequences of environmental change for the action of sexual selection, in terms of the opportunity for total sexual selection and patterns of phenotypic selection, are unknown. Here we show that dietary stress in guppies, Poecilia reticulata, reduces the expression of several sexually selected traits and increases the opportunity for total sexual selection (standardized variance in reproductive success) in males. Furthermore, our results show that dietary stress modulates the relative importance of precopulatory (mating success) and postcopulatory (relative fertilization success) sexual selection, and that the form of multivariate sexual selection (linear vs. nonlinear) depends on dietary regime. Overall, our results are consistent with a pattern of heightened directional selection on condition‐dependent sexually selected traits under environmental stress, and underscore the importance of sexual selection in shaping adaptation in a changing world.     

Promiscuity drives sexual selection in a socially monogamous bird

Many socially monogamous species paradoxically show signs of strong sexual selection, suggesting cryptic sources of sexual competition among males. Darwin argued that sexual selection could operate in monogamous systems if breeding sex ratios are biased or if some males attract highly fecund females. Alternatively, sexual selection might result from promiscuous copulations outside the pair bond, although several recent studies have cast doubt on this possibility, in particular by showing that variance in apparent male reproductive success (number of social young) differs little from variance in actual male reproductive success (number of young sired). Our results from a long-term study of the socially monogamous splendid fairy-wren (Malurus splendens) demonstrate that such comparisons are misleading and do not adequately assess the effects of extra-pair paternity (EPP). By partitioning the opportunity for selection and calculating Bateman gradients, we show that EPP has a strong effect on male annual and lifetime fitness, whereas other proposed mechanisms of sexual selection do not. Thus, EPP drives sexual selection in this, and possibly other, socially monogamous species.     

Operational sex ratio predicts the opportunity and direction of sexual selection across animals

The operational sex ratio (OSR) has long been assumed to be a key ecological factor determining the opportunity and direction of sexual selection. However, recent theoretical work has challenged this view, arguing that a biased OSR does not necessarily result in greater monopolisation of mates and therefore stronger sexual selection in the mate‐limited sex. Hence, the role of the OSR for shaping animal mating systems remains a conundrum in sexual selection research. Here we took a meta‐analytic approach to test whether OSR explains interspecific variation in sexual selection metrics across a broad range of animal taxa. Our results demonstrate that the OSR predicts the opportunity for sexual selection in males and the direction of sexual selection in terms of sex differences in both the opportunity for sexual selection and the Bateman gradient (i.e. the selection differential of mating success), as predicted by classic theory.     

Quantitative measures of sexual selection reveal no evidence for sex-role reversal in a sea spider with prolonged paternal care

Taxa in which males alone invest in postzygotic care of offspring are often considered good models for investigating the proffered relationships between sexual selection and mating systems. In the pycnogonid sea spider Pycnogonum stearnsi, males carry large egg masses on their bodies for several weeks, so this species is a plausible candidate for sex-role reversal (greater intensity of sexual selection on females than on males). Here, we couple a microsatellite-based assessment of the mating system in a natural population with formal quantitative measures of genetic fitness to investigate the direction of sexual selection in P. stearnsi. Both sexes proved to be highly polygamous and showed similar standardized variances in reproductive and mating successes. Moreover, the fertility (number of progeny) of males and females appeared to be equally and highly dependent on mate access, as shown by similar Bateman gradients for the two sexes. The absence of sex-role reversal in this population of P. stearnsi is probably attributable to the fact that males are not limited by brooding space but have evolved an ability to carry large numbers of progeny. Body length was not a good predictor of male mating or reproductive success, so the aim of future studies should be to determine what traits are the targets of sexual selection in this species.     

How to quantify (the response to) sexual selection on traits

Natural selection operates via fitness components like mating success, fecundity, and longevity, which can be understood as intermediaries in the causal process linking traits to fitness. In particular, sexual selection occurs when traits influence mating or fertilization success, which, in turn, influences fitness. We show how to quantify both these steps in a single path analysis, leading to better estimates of the strength of sexual selection. Our model controls for confounding variables, such as body size or condition, when estimating the relationship between mating and reproductive success. Correspondingly, we define the Bateman gradient and the Jones index using partial rather than simple regressions, which better captures how they are commonly interpreted. The model can be applied both to purely phenotypic data and to quantitative genetic parameters estimated using information on relatedness. The phenotypic approach breaks down selection differentials into a sexually selected and a “remainder” component. The quantitative genetic approach decomposes the estimated evolutionary response to selection analogously. We apply our method to analyze sexual selection in male dusky pipefish, Syngnathus floridae, and in two simulated datasets. We highlight conceptual and statistical limitations of previous path‐based approaches, which can lead to substantial misestimation of sexual selection.     

Models of sexual selection on a quantitative genetic trait when preference is acquired by sexual imprinting

The evolution of a quantitative genetic trait under stabilizing viability selection and sexual selection is modeled for a polygynous species in which female mating preferences are acquired by sexual imprinting on the parents and by exposure to the surviving population at large. Stabilizing viability selection acts equally on both sexes in the case of a sexually monomorphic trait and on males only in the case of a dimorphic trait. A genetically fixed sensory or perceptual bias defines the origin of the scale on which the trait is measured, and the possibility is incorporated that female preferences may deviate asymmetrically from the familiar-either toward or away from this origin. When viability selection is strong relative to sexual selection, the models predict that the mean trait value will evolve to the viability optimum. With intermediate ratios of the strength of viability to sexual selection, a stable equilibrium can occur on either side of this viability optimum, depending on the direction of asymmetry in female preferences. When viability selection is relatively weak and certain other conditions are also satisfied, runaway selection is predicted.     

Within‐season variation in sexual selection in a fish with dynamic sex roles

The strength of sexual selection may vary between species, among populations and within populations over time. While there is growing evidence that sexual selection may vary between years, less is known about variation in sexual selection within a season. Here, we investigate within‐season variation in sexual selection in male two‐spotted gobies (Gobiusculus flavescens). This marine fish experiences a seasonal change in the operational sex ratio from male‐ to female‐biased, resulting in a dramatic decrease in male mating competition over the breeding season. We therefore expected stronger sexual selection on males early in the season. We sampled nests and nest‐holding males early and late in the breeding season and used microsatellite markers to determine male mating and reproductive success. We first analysed sexual selection associated with the acquisition of nests by comparing nest‐holding males to population samples. Among nest‐holders, we calculated the potential strength of sexual selection and selection on phenotypic traits. We found remarkable within‐season variation in sexual selection. Selection on male body size related to nest acquisition changed from positive to negative over the season. The opportunity for sexual selection among nest‐holders was significantly greater early in the season rather than late in the season, partly due to more unmated males. Overall, our study documents a within‐season change in sexual selection that corresponds with a predictable change in the operational sex ratio. We suggest that many species may experience within‐season changes in sexual selection and that such dynamics are important for understanding how sexual selection operates in the wild.     

Efficiency of direct selection on quantitative trait loci for a two-trait breeding objective

Selection on known loci affecting quantitative traits (DSQ) was compared to phenotypic selection index for a single and a two-trait selection objective. Two situations were simulated; a single known quantitative locus, and ten identified loci accounting for all the additive genetic variance. Selection efficiency of DSQ relative to traitbased selection was higher for two-trait selection, than was selection on a single trait with the same heritability. The advantage of DSQ was greater when the traits were negatively correlated. Relative selection efficiency (RSE) for a single locus responsible for 0.1 of the genetic variance was 1.11 with heritabilities of 0.45 and 0.2 and zero genetic and phenotypic correlations between the traits. RSE of DSQ for ten known loci was 1.5 to 1.8 in the first 3 generations of selection, but declined in each subsequent generation. With DSQ most loci reached fixation after 7 generations. Response to trait-based selection continued through generation 15 and approached the response obtained with DSQ after 10 generations. The cumulative genetic response after 10 generations of DSQ was only 93% to 97% of the economically optimum genotype because the less favorable allele reached fixation for some loci, generally those with effects in opposite directions on the two traits.