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.     

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.     

Sex‐specific selection and sexual size dimorphism in the waterstrider Aquarius remigis

We estimated selection on adult body size for two generations in two populations of Aquarius remigis, as part of a long‐term study of the adaptive significance of sexual size dimorphism (SSD). Net adult fitness was estimated from the following components: prereproductive survival, daily reproductive success (mating frequency or fecundity), and reproductive lifespan. Standardized selection gradients were estimated for total length and for thorax, abdomen, genital and mesofemur lengths. Although selection was generally weak and showed significant temporal and spatial heterogeneity, patterns were consistent with SSD. Prereproductive survival was strongly influenced by date of eclosion, but size (thorax and genital lengths in females; total and abdomen lengths in males) played a significant secondary role. Sexual selection favoured smaller males with longer external genitalia in one population. Net adult fitness was not significantly related to body size in females, but was negatively related to size (thorax and total length) in males.     

Positive correlations between pre‐ and post‐copulatory sexual traits in warblers

Theoretical models predict that investment in pre‐copulatory and post‐copulatory sexually selected traits should trade‐off. At the macroevolutionary scale, the majority of studies to date have focused on male weaponry as the target of pre‐copulatory sexual selection, but the trade‐off should equally apply to traits used to attract females, such as bird song and plumage. We studied the Old World leaf warblers (Phylloscopidae), a group of socially monogamous songbirds that experience relatively high levels of sperm competition. We examined the relationships between song duration and number of elements in the song with sperm length across 21 species, and between the same song variables and combined testes mass in a subset of these species (n = 10). Across species, these song variables and testes mass/sperm length were generally positively correlated, albeit not statistically significantly so or with borderline significance. In contrast to theory, we found no evidence for negative associations between pre‐ and post‐copulatory traits. We argue that this is a consequence of males of some species investing more into overall fertilization success (i.e. the sum of pre‐ and post‐copulatory sexual selection) than males of other species, and high fertilization success is achieved through investment into both mate attraction and sperm competition.     

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.     

A biogeographic reversal in sexual size dimorphism along a continental temperature gradient

The magnitude and direction of sexual size dimorphism (SSD) varies greatly across the animal kingdom, reflecting differential selection pressures on the reproductive and/or ecological roles of males and females. If the selection pressures and constraints imposed on body size change along environmental gradients, then SSD will vary geographically in a predictable way. Here, we uncover a biogeographical reversal in SSD of lizards from Central and North America: in warm, low latitude environments, males are larger than females, but at colder, high latitudes, females are larger than males. Comparisons to expectations under a Brownian motion model of SSD evolution indicate that this pattern reflects differences in the evolutionary rates and/or trajectories of sex‐specific body sizes. The SSD gradient we found is strongly related to mean annual temperature, but is independent of species richness and body size differences among species within grid cells, suggesting that the biogeography of SSD reflects gradients in sexual and/or fecundity selection, rather than intersexual niche divergence to minimize intraspecific competition. We demonstrate that the SSD gradient is driven by stronger variation in male size than in female size and is independent of clutch mass. This suggests that gradients in sexual selection and male–male competition, rather than fecundity selection to maximize reproductive output by females in seasonal environments, are predominantly responsible for the gradient.     

Evolution of sexual size dimorphism in birds: test of hypotheses using blue tits in contrasted Mediterranean habitats

Many hypotheses, either sex‐related or environment‐related, have been proposed to explain sexual size dimorphism in birds. Two populations of blue tits provide an interesting case study for testing these hypotheses because they live in contrasting environments in continental France and in Corsica and exhibit different degree of sexual size dimorphism. Contrary to several predictions, the insular population is less dimorphic than the continental one but neither the sexual selection hypothesis nor the niche variation hypothesis explain the observed patterns. In the mainland population it is advantageous for both sexes to be large, and males are larger than females. In Corsica, however, reproductive success was greater for pairs in which the male was relatively small, i.e. pairs in which sexual size dimorphism is reduced. The most likely explanation is that interpopulation differences in sexual size dimorphism are determined not by sex‐related factors, but by differences in sex‐specific reproductive roles and responses to environmental factors. Because of environmental stress on the island as a result of food shortage and high parasite infestations, the share of parents in caring for young favours small size in males so that a reduced sexual size dimorphism is not the target of selection but a by‐product of mechanisms that operate at the level of individual sexes.     

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.     

Population density mediates the interaction between pre‐ and postmating sexual selection

When females mate with more than one male, sexual selection acts both before and after mating. The interaction between pre‐ and postmating episodes of selection is expected to be context dependent, but few studies have investigated how total sexual selection changes under different ecological conditions. We examined how population density mediates the interaction between pre‐ and postmating sexual selection by establishing replicate populations of the horned dung beetle Onthophagus taurus at low, medium, and high densities, and then using microsatellite‐based parentage analyses to measure male fitness. We found that mating success and fertilization success were positively correlated at all three densities, but the strength of the correlation decreased with increasing density. We also found a shift from negative to positive linear selection on testes mass as density increased, and opposing selection on weapons and testes at high densities. These patterns suggest that the importance of postmating processes increases with increasing population density, which reduces the selective advantage of weapons for premating contest competition, and increases the selective advantage of large ejaculates for postmating sperm competition. We expect that density‐dependent selection on testes mass has contributed to the phenotypic variation observed between natural populations of O. taurus that differ in density.     

Population variation in sexual selection and its effect on size allometry in two dung fly species with contrasting sexual size dimorphism

Body size is one of the most important quantitative traits under evolutionary scrutiny. Sexual size dimorphism (SSD) in a given species is expected to result if opposing selection forces equilibrate differently in both sexes. We document variation in the intensity of sexual and fecundity selection, male and female body size, and thus SSD among 31 and 27 populations of the two dung fly species, Scathophaga stercoraria and Sepsis cynipsea, across Switzerland. Whereas in S. cynipsea females are larger, the SSD is reversed in S. stercoraria. We comprehensively evaluated Fairbairn and Preziosi's (1994) general, three-tiered scenario, hypothesizing that sexual selection for large male size is the major driving force of SSD allometry within these two species. Sexual selection intensity on male size in the yellow dung fly, S. stercoraria, was overall positive, greater, and more variable among populations than fecundity selection on females. Also, sexual selection intensity in a given population correlated positively with mean male body size of that population for both the field-caught fathers and their laboratory-reared sons, indicating a response to selection. In S. cvnipsea, sexual selection intensity on males was lower overall and significantly positive, about equal in magnitude, but more variable than fecundity selection on females. However, there was no correlation between the intensity of sexual selection and mean male body size among populations. In both species, the laboratory-reared offspring indicate genetic differentiation among populations in body size. Despite fulfillment of all key prerequisites, at least in S. stercoraria, we did not find hypoallometry for SSD (Rensch's rule, i.e., greater evolutionary divergence in male size than female size) for the field-caught parents or the laboratory-reared offspring: Female size was isometric to male size in both species. We conclude that S. cynipsea does not fit some major requirements of Fairbairn and Preziosi's (1994) scenario, whereas for S. stercoraria we found partial support for it. Failure to support Rensch's rule within the latter species may be due to phylogenetic or other constraints, power limitations, erroneous estimates of sexual selection, insufficient genetic isolation of populations, or sex differences in viability selection against large size.     

Sexual selection on male size drives the evolution of male‐biased sexual size dimorphism via the prolongation of male development

Sexual size dimorphism (SSD) arises when the net effects of natural and sexual selection on body size differ between the sexes. Quantitative SSD variation between taxa is common, but directional intraspecific SSD reversals are rare. We combined micro‐ and macroevolutionary approaches to study geographic SSD variation in closely related black scavenger flies. Common garden experiments revealed stark intra‐ and interspecific variation: Sepsis biflexuosa is monomorphic across the Holarctic, while S. cynipsea (only in Europe) consistently exhibits female‐biased SSD. Interestingly, S. neocynipsea displays contrasting SSD in Europe (females larger) and North America (males larger), a pattern opposite to the geographic reversal in SSD of S. punctum documented in a previous study. In accordance with the differential equilibrium model for the evolution of SSD, the intensity of sexual selection on male size varied between continents (weaker in Europe), whereas fecundity selection on female body size did not. Subsequent comparative analyses of 49 taxa documented at least six independent origins of male‐biased SSD in Sepsidae, which is likely caused by sexual selection on male size and mediated by bimaturism. Therefore, reversals in SSD and the associated changes in larval development might be much more common and rapid and less constrained than currently assumed.     

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.     

Sexual selection, antennae length and the mating advantage of large males in Asellus aquaticus

In crustacean species with precopulatory mate-guarding, sexual size dimorphism has most often been regarded as the consequence of a large male advantage in contest competition for access to females. However, large body size in males may also be favoured indirectly through scramble competition. This might partly be the case if the actual target of selection is a morphological character, closely correlated with body size, involved in the detection of receptive females. We studied sexual selection on body size and antennae length in natural populations of Asellus aquaticus, an isopod species with precopulatory mate guarding. In this species, males are larger than females and male pairing success is positively related to body size. However, males also have longer antennae, relative to body size, than females, suggesting that this character may also be favoured by sexual selection. We used multivariate analysis of selection to assess the relative influences of body size and antennae length in five different populations in the field. Selection gradients indicated that overall body size was a better predictor of male pairing success than antennae length, although some variation was observed between sites. We then manipulated male antennae length in a series of experiments conducted in the laboratory, and compared the pairing ability of males with short or long antennae. Males with short antennae were less likely to detect, orient to and to pair with a receptive female compared to males with long antennae. We discuss the implications of our results for studies of male body size and sexual dimorphism in relation to sexual selection in crustaceans.     

Sexual selection, antennae length and the mating advantage of large males in Asellus aquaticus

In crustacean species with precopulatory mate-guarding, sexual size dimorphism has most often been regarded as the consequence of a large male advantage in contest competition for access to females. However, large body size in males may also be favoured indirectly through scramble competition. This might partly be the case if the actual target of selection is a morphological character, closely correlated with body size, involved in the detection of receptive females. We studied sexual selection on body size and antennae length in natural populations of Asellus aquaticus, an isopod species with precopulatory mate guarding. In this species, males are larger than females and male pairing success is positively related to body size. However, males also have longer antennae, relative to body size, than females, suggesting that this character may also be favoured by sexual selection. We used multivariate analysis of selection to assess the relative influences of body size and antennae length in five different populations in the field. Selection gradients indicated that, overall, body size was a better predictor of male pairing success than antennae length, although some variation was observed between sites. We then manipulated male antennae length in a series of experiments conducted in the lab, and compared the pairing ability of males with short or long antennae. Males with short antennae were less likely to detect, orient to, and to pair with a receptive female compared with males with long antennae. We discuss the implications of our results for studies of male body size and sexual dimorphism in relation to sexual selection in crustaceans.     

昆虫性选择行为研究进展

本文综述了昆虫的各种性选择行为,包括与个体大小有关的性选择行为、与鸣声有关的性选择行为、与“婚礼食物”有关的性选择行为以及精子竞争等。     

Adult sex ratio,sexual dimorphism and sexual selection in a Mesozoic reptile

The evolutionary history of sexual selection in the geologic past is poorly documented based on quantification, largely because of difficulty in sexing fossil specimens. Even such essential ecological parameters as adult sex ratio (ASR) and sexual size dimorphism (SSD) are rarely quantified, despite their implications for sexual selection. To enable their estimation, we propose a method for unbiased sex identification based on sexual shape dimorphism, using size-independent principal components of phenotypic data. We applied the method to test sexual selection in Keichousaurus hui, a Middle Triassic (about 237 Ma) sauropterygian with an unusually large sample size for a fossil reptile. Keichousaurus hui exhibited SSD biased towards males, as in the majority of extant reptiles, to a minor degree (sexual dimorphism index −0.087). The ASR is about 60% females, suggesting higher mortality of males over females. Both values support sexual selection of males in this species. The method may be applied to other fossil species. We also used the Gompertz allometric equation to study the sexual shape dimorphism of K. hui and found that two sexes had largely homogeneous phenotypes at birth except in the humeral width, contrary to previous suggestions derived from the standard allometric equation.     

Limits to sexual size dimorphism in red‐winged blackbirds: the cost of getting big?

A fundamental assumption of sexual selection theory is that the reproductive advantage of large size is balanced by a survival disadvantage. Previous studies of the sexually size-dimorphic red-winged blackbird ( Agelaius phoeniceus ) have indicated that the largest adult males have a survival advantage, suggesting that the limit to male size may be the cost of getting big rather than the cost of being big. If the cost of getting big limits male size, then starvation rates for male nestlings should exceed those of female nestlings. In addition, given high heritability of body size, larger parents should lose more nestlings, particularly males, to starvation. We tested these predictions for red-winged blackbirds using data on the sex of 1356 fledglings from 465 nests collected over 10 years. We found no disadvantage for male nestlings relative to females – 49% of fledglings were male and previous research had shown that 48% of hatchlings are male. We also found no disadvantage for male nestlings that would become large adults (i.e. those with larger parents) – partial brood loss and fledging sex ratios did not vary with mid-parent size. Given no apparent disadvantage to large size for males either as adults or as nestlings, this leaves only the period between fledging and adulthood during which natural selection might limit sexual size dimorphism, although other mechanisms might explain the failure to find a limit to male size.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 85 , 353–361.