Evolution Of Sexual Size Dimorphism Research Articles

Pre-Copulatory Sexual Selection Predicts Sexual Size Dimorphism: A Meta-Analysis of Comparative Studies.

Size differences between males and females are common across the tree of life (termed sexual size dimorphism; SSD), and have fundamental implications for ecology, life history and behaviour of both sexes. Conventionally, SSD is thought to evolve in response to sex-specific sexual selection but more recent work suggests that ecological processes can also promote sex-differences in size. Here, we provide a global test for the role of sexual selection in the evolution of sexual size dimorphism using data from 77 comparative studies spanning the major classes of the animal kingdom. We show that intense sexual selection typically correlates with male-biased SSD across species. Importantly, pre-copulatory but not post-copulatory sexual selection predicts SSD, suggesting a pervasive role of premating male-male competition and female choice to drive sex differences in body size. Collectively, our findings suggest that pre-copulatory sexual selection plays a major role in the evolution of male-biased SSD.

Complex ontogeny of sexual size dimorphism in a female-larger gecko: Implications of determinate growth for lizard body size and life-history evolution.

Ectothermic vertebrates such as reptiles were assumed to be indeterminate growers, which means that there is no terminal point in time or size for growth in their lifetime. In recent years, evidence for the determinate nature of growth in lizards has accumulated, necessitating a re-examination of models of their ontogeny and evolution of sexual size dimorphism (SSD). In the female-larger gecko Paroedura vazimba, we monitored post-embryonic growth over a period of 15 months. After hatching, females grew faster than males but also reached their final body size, that is, closed growth of their vertebrae, earlier than males. The closure of bone growth in females correlates with the onset of reproductive maturation. We compared this pattern with the previously minutely studied, male-larger species Paroedura picta, where we documented determinate growth as well. We propose a model to explain the evolutionary switches in the direction of SSD in lizards based on bipotential effects of ovarian hormones on growth. In this model, male growth is assumed to require no male-specific growth modifier, such as sex-limited hormonal regulators, while growth is feminized by ovarian hormones in females. Low levels of ovarian hormones can promote bone growth, but high levels associated with maturation of the reproductive organs promote senescence of bone growth plates and thus cessation of bone growth. We suggest that models on growth, life-history and evolution of body size in many lizards should acknowledge their determinate nature of growth.

Annual temperature, body size, and sexual size dimorphism in the evolution of Pyrgomorphidae.

In many animal species, larger body size is positively correlated with male mating success and female fecundity. However, in the case of insects, in high seasonality environments, natural selection favors a faster maturation that decreases the risk of pre-reproductive death. However, this advantageous adaptation comes at a tradeoff, resulting in a reduction in body size. Maturation time is influenced by environmental factors, such as temperature, season length, and food availability during the rains. The geographic variation in these parameters provides an opportunity to study their impact on the adaptive evolution of body size in Pyrgomorphidae grasshoppers. These grasshoppers exhibit remarkable variation in body size and wing development and can be found in diverse plant communities across Africa, Asia, Australia, and tropical America. In this study, we utilized a phylogenetic approach to examine the evolution of body size, considering climatic factors, and the influence of sexual selection on size differences between males and females. We found a positive correlation between mean annual temperature and sexual size dimorphism (SSD). Remarkably, species exhibiting a strong bias toward larger females were found to be adapted to regions with higher temperatures. In the Pyrgomorphidae family, an intermediate body size was identified as the ancestral trait. Additionally, winged male and female grasshoppers were observed to be larger than their wingless counterparts. Despite the potential conflicting pressures on body size in males and females, these grasshoppers adhere to Rench's Rule, suggesting that sexual selection on males' body size may explain the evolution of SSD.

The effect of miniaturization on the evolution of sexual size dimorphism in geckos.

The evolution of miniaturization can result in dramatic alterations of morphology, physiology, and behavior; however, the effects of miniaturization on sexual dimorphism remain largely unknown. Here we investigate how miniaturization influences patterns of sexual size dimorphism (SSD) in geckos. Measuring 1,875 individuals from 131 species, we characterized patterns of SSD relative to body size across two families. We found that miniaturized species were more female biased than non-miniaturized species. Additionally, one family that contained many miniaturized species (Sphaerodactylidae) displayed allometric patterns in SSD with body size, where larger species were male biased and smaller species were more female biased. Smaller species in this lineage also produced proportionally larger eggs. By contrast, another family containing few miniaturized species (Phyllodactylidae) displayed a more isometric trend. Together, these observations are consistent with the hypothesis that selection for increased reproductive success in small species of Sphaerodactylidae results in female-biased SSD in these taxa, which in turn drives the positive SSD allometry observed in this lineage. Thus, selection for increased miniaturization in the clade may be offset by selection on maintaining a female size in smaller taxa that ensures reproductive success.

The macroevolution of sexual size dimorphism in birds

Abstract There is considerable variation of sexual size dimorphism (SSD) in body mass among animal groups, yet the drivers of interspecific variation in SSD are still poorly understood. Possible mechanisms have been suggested, including sexual selection, selection for fecundity in females, niche divergence between sexes, and allometry, yet their relative importance is still poorly understood. Here, we tested predictions of these four hypotheses in different avian groups using a large-scale dataset on SSD of body mass for 4761 species. Specifically, we estimated the probability of transition between male- and female-biased SSD, tested for differences in evolutionary rates of body mass evolution for males and females, and assessed the potential ecological and spatial correlates of SSD. Our results were consistent with the sexual selection, fecundity, and niche divergence hypotheses, but their support varied considerably among avian orders. In addition, we found little evidence that the direction of SSD affected the evolution of male or female body mass, and no relationship was detected between SSD and environmental predictors (i.e. temperature and precipitation seasonality, productivity, species richness, and absolute latitude). These results suggest that avian evolution of SSD is likely to be multifactorial, with sexual selection, fecundity, and niche divergence playing important roles in different avian orders.

Revisiting niche divergence hypothesis in sexually dimorphic birds: Is diet overlap correlated with sexual size dimorphism?

The evolution of sexual size dimorphism (SSD) is a long-standing topic in evolutionary biology, but there is little agreement on the extent to which SSD is driven by the different selective forces. While sexual selection and fecundity selection have traditionally been proposed as the two leading hypotheses, SSD may also result from natural selection through mechanisms such as sexual niche divergence, which might have reduced resource competition between sexes. Here, we revisited the niche divergence hypothesis by testing the relationship between the sexual overlap in diet and SSD of 56 bird species using phylogenetic comparative analyses. We then assessed how SSD variation relates to the three main hypotheses: sexual selection, fecundity selection, and sexual niche divergence using phylogenetic generalized least squares (PGLS). Then, we compared sexual selection, fecundity selection and niche divergence selection as SSD drivers through phylogenetic confirmatory path analyses to disentangle the possible causal evolutionary relationships between SSD and the three hypotheses. Phylogenetic generalized least squares showed that SSD was negatively correlated with diet overlap, that is, the greater the difference in body size between males and females, the less diet overlap. As predicted by sexual selection theory, the difference in body size between sexes was higher in polygynous species. Confirmatory phylogenetic path analyses suggested that the most likely evolutionary path might include the mating system as a main driver in SSD and niche divergence as a result of SSD. We found no evidence of a role of fecundity selection in the evolution of female-biased SSD. Our study provides evidence that sexual selection has likely been the main cause of SSD and that dietary divergence is likely an indirect effect of SSD.

A diving beetle’s dilemma: the impact of sexual conflict on Rensch’s rule

Abstract Sexual conflict is believed to be an important evolutionary force driving phenotypic diversification, especially sexual dimorphism. Males of diving beetles sometimes resort to coercive tactics to increase their chances of successful reproduction, which can impose costs on females. Sexual conflict can also drive sexual size dimorphism (SSD), particularly in species where males are larger than females. In this context, Rensch’s rule states that SSD tends to increase with body size in species with male-biased SSD and decrease with body size in species with female-biased SSD. The role of sexual conflict in driving the evolution of the allometric relationships between males and females remains unclear. We addressed whether sexual conflict in diving beetles might drive SSD. We found that dytiscids do not follow Rensch’s rule, whereby the SSD is isometric in relationship to species body size. Species with adhesive pads (Dytiscinae) showed a more pronounced SSD than other diving beetle species. These results suggest that the presence of adhesive pads might reduce the force necessary to control female movement during copulation and drive the evolution of smaller males. The findings of this study provide new insights into the role of sexual conflict in driving the evolution of SSD in animals.

Chigger mite (Eutrombicula alfreddugesi) ectoparasitism does not contribute to sex differences in growth rate in eastern fence lizards (Sceloporus undulatus).

Parasitism is nearly ubiquitous in animals and is frequently associated with fitness costs in host organisms, including reduced growth, foraging, and reproduction. In many species, males tend to be more heavily parasitized than females and thus may bear greater costs of parasitism. Sceloporus undulatus is a female-larger, sexually size dimorphic lizard species that is heavily parasitized by chigger mites (Eutrombicula alfreddugesi). In particular, the intensity of mite parasitism is higher in male than in female juveniles during the period of time when sex differences in growth rate lead to the development of sexual size dimorphism (SSD). Sex-biased differences in fitness costs of parasitism have been documented in other species. We investigated whether there are growth costs of mite ectoparasitism, at a time coinciding with sex differences in growth rate and the onset of SSD. If there are sex-biased growth costs of parasitism, then this could suggest a contribution to the development of SSD in S. undulatus. We measured growth and mite loads in two cohorts of unmanipulated, field-active yearlings by conducting descriptive mark-recapture studies during the activity seasons of 2016 and 2019. Yearling males had consistently higher mid-summer mite loads and consistently lower growth rates than females. However, we found that growth rate and body condition were independent of mite load in both sexes. Furthermore, growth rates and mite loads were higher in 2019 than in 2016. Our findings suggest that juveniles of S. undulatus are highly tolerant of chigger mites and that any costs imposed by mites may be at the expense of functions other than growth. We conclude that sex-biased mite ectoparasitism does not contribute to sex differences in growth rate and, therefore, does not contribute to the development of SSD.

Genetic Variation in Sexual Size Dimorphism Is Associated with Variation in Sex-Specific Plasticity in Drosophila.

AbstractThe difference in body size between females and males, or sexual size dimorphism (SSD), is ubiquitous, yet we have a poor understanding of the developmental genetic mechanisms that generate it and how these mechanisms may vary within and among species. Such an understanding of the genetic architecture of SSD is important if we are to evaluate alternative models of SSD evolution, but the genetic architecture is difficult to describe because SSD is a characteristic of populations, not individuals. Here, we overcome this challenge by using isogenic lineages of Drosophila to measure SSD for 196 genotypes. We demonstrate extensive genetic variation for SSD, primarily driven by higher levels of genetic variation for body size among females than among males. While we observe a general increase in SSD with sex-averaged body size (pooling for sex) among lineages, most of the variation in SSD is independent of sex-averaged body size and shows a strong genetic correlation with sex-specific plasticity, such that increased female-biased SSD is associated with increased body size plasticity in females. Our data are consistent with the condition dependence hypothesis of sexual dimorphism and suggest that SSD in Drosophila is a consequence of selection on the developmental genetic mechanisms that regulate the plasticity of body size.

Role of sexual and natural selection in the evolution of sexual size dimorphism in primates

AbstractIn mammals, the dominant theory proposes that sexual size dimorphism evolved by sexual selection in a polygynous reproductive scenario. Natural selection is an alternative hypothesis where dimorphism represents an adaptation to ecological pressures. I tested evolutionary models based on sexual and natural selection processes using phylogenetic confirmatory path analyses. I employed data for 225 primate species in terms of their diel activity, body mass, sexual size dimorphism, level of sociality, and level of polygyny. The model that received the most support from path analyses was a mixed model in which dimorphism evolved after an increase in body size that resulted from a response to an ecological pressure, i.e., a change from nocturnal to diurnal habits, with a lesser role of polygyny. Phylogenetic path analysis suggests that natural selection has played an important role in the evolution of sexual size dimorphism in primates.

Climate shapes patterns of sexual size and shape dimorphism across the native range of the green anole lizard,Anolis carolinensis(Squamata: Dactyloidae)

AbstractGeographical variation in sexual size dimorphism (SSD) can result from the combined effects of environmental and sexual selection. To understand the determinants of SSD across geographical landscapes, we tested for relationships between SSD and climatic variables in the widespread lizard Anolis carolinensis. To distinguish alternative hypotheses for observed patterns of variation in SSD, we also examined sex-specific patterns of body size evolution and asked whether SSD was associated with certain patterns of sexual shape dimorphism. We found strong evidence for Rensch’s rule (an increase in male-biased SSD with average body size) in A. carolinensis and evidence for the reversed version of Bergmann’s rule (an increase in body size towards warmer environments) in males. Across populations, SSD was positively related to temperature; however, female body size was not related to any climatic variable, suggesting that the latitudinal gradient of SSD might be driven by a gradient in the intensity of sexual selection acting on males. Sexual size dimorphism was positively correlated with sexual dimorphism in head shape and negatively correlated with limb length dimorphism, suggesting that sexual selection in males might drive the evolution of SSD and that differences in size and limb shape between sexes might represent alternative strategies to avoid competition for the same resources.

Influence of microhabitat, fecundity, and parental care on the evolution of sexual size dimorphism in Caribbean Eleutherodactylus frogs.

Rensch's rule suggests that sexual size dimorphism (SSD) increases with species size when males are the larger sex, whereas it decreases when females are the larger sex. However, the process responsible for this pattern remains obscure. SSD can result from sexual selection, such as intrasexual competition for access to mates, or from natural selection, due to resource partitioning or fecundity selection. We studied SSD in Caribbean Eleutherodactylus frogs using phylogenetic comparative methods to investigate the influence of microhabitat, fecundity, and parental care. Our results show that in Caribbean Eleutherodactylus females tend to be larger and, contrary to Rensch's rule, dimorphism increases with species size. SSD was not related to microhabitat use. However, SSD was positively correlated with fecundity, mediated by a greater increase in female size. SSD was also influenced by parental care, suggesting that male care promotes larger male size and reduces the female bias in SSD. As suggested for other anurans, female-biased SSD in Caribbean Eleutherodactylus results from fecundity selection, although the magnitude is countered by increased male size in species with paternal care. Our results highlight the importance of considering various selective forces that may act in concert to influence the evolution of SSD.

Species-Specific Expression of Growth-Regulatory Genes in 2 Anoles with Divergent Patterns of Sexual Size Dimorphism.

SynopsisSexual size dimorphism is widespread in nature and often develops through sexual divergence in growth trajectories. In vertebrates, the growth hormone/insulin-like growth factor (GH/IGF) network is an important regulator of growth, and components of this network are often regulated in sex-specific fashion during the development of sexual size dimorphism. However, expression of the GH/IGF network is not well characterized outside of mammalian model systems, and the extent to which species differences in sexual size dimorphism are related to differences in GH/IGF network expression is unclear. To begin bridging this gap, we compared GH/IGF network expression in liver and muscle from 2 lizard congeners, one with extreme male-biased sexual size dimorphism (brown anole, Anolis sagrei), and one that is sexually monomorphic in size (slender anole, A. apletophallus). Specifically, we tested whether GH/IGF network expression in adult slender anoles resembles the highly sex-biased expression observed in adult brown anoles or the relatively unbiased expression observed in juvenile brown anoles. We found that adults of the 2 species differed significantly in the strength of sex-biased expression for several key upstream genes in the GH/IGF network, including insulin-like growth factors 1 and 2. However, species differences in sex-biased expression were minor when comparing adult slender anoles to juvenile brown anoles. Moreover, the multivariate expression of the entire GH/IGF network (as represented by the first two principal components describing network expression) was sex-biased for the liver and muscle of adult brown anoles, but not for either tissue in juvenile brown anoles or adult slender anoles. Our work suggests that species differences in sex-biased expression of genes in the GH/IGF network (particularly in the liver) may contribute to the evolution of species differences in sexual size dimorphism.

Body growth, mass at sexual maturity, and sexual dimorphism in Florida panthers (Puma concolor coryi)

Abstract Recognizing individual variation in body growth characteristics and size at sexual maturity is of particular interest because they indicate a potential source of variance in survival and reproductive fitness. I used the Richards group of unified models method to examine body growth characteristics, mass at sexual maturity, and development of sexual size dimorphism in Florida panthers (Puma concolor coryi). A larger asymptotic body size and mass at sexual maturity in males resulted from a greater instantaneous growth rate across the life span and longer duration of growth than in females. Juvenile males attained larger body mass than female counterparts before achieving independence and sexual maturity, suggesting that a greater instantaneous growth rate developed from precopulatory intrasexual selection. Body mass growth rapidly decreased proximate to the minimum age at first conception in both sexes, suggesting that energetic costs of reproduction inhibited additional growth. Intrasexual selection among males to enhance fighting ability and promote access to a territory and mates is implicated as the cause for sexual size dimorphism, together with more direct underlying energetic costs of reproduction in females. The results provide uniform sex-specific body mass-at-age growth and mass at sexual maturity statistics for comparison with other puma populations and reference values to implement measurable criteria to evaluate trends in Florida panther population health.

Dancing drives evolution of sexual size dimorphism in manakins.

Body size mediates life history, physiology and inter- and intra-specific interactions. Within species, sexes frequently differ in size, reflecting divergent selective pressures and/or constraints. Both sexual selection and differences in environmentally mediated reproductive constraints can drive sexual size dimorphism, but empirically testing causes of dimorphism is challenging. Manakins (Pipridae), a family of Neotropical birds comprising approximately 50 species, exhibit a broad range of size dimorphism from male- to female-biased and are distributed across gradients of precipitation and elevation. Males perform courtship displays ranging from simple hops to complex aerobatic manoeuvres. We tested associations between sexual size dimorphism and (a) agility and (b) environment, analysing morphological, behavioural and environmental data for 22 manakin species in a phylogenetic framework. Sexual dimorphism in mass was most strongly related to agility, with males being lighter than females in species performing more aerial display behaviours. However, wing and tarsus length dimorphism were more strongly associated with environmental variables, suggesting that different sources of selection act on different aspects of body size. These results highlight the strength of sexual selection in shaping morphology-even atypical patterns of dimorphism-while demonstrating the importance of constraints and ecological consequences of body size evolution.

Evolution of sexual size dimorphism and sexual segregation in artiodactyls: the chicken or the egg?

Evolution of sexual size dimorphism and sexual segregation in artiodactyls: the chicken or the egg?

Evolution of sexual dimorphism in an endemic toad of the Qinghai–Tibet plateau fails to obey Rensch’s rule

According to Rensch's rule, sexual size dimorphism (SSD) decreases with increasing body size in species where females are larger than males, whereas SSD increases with body size when males are larger than females. In this study, we examined body size from 15 populations of Bufo minshanicus in the Qinghai–Tibet plateau in China. We estimated the age of the individuals from eight populations to evaluate Rensch's rule and possible causes of variation in SSD. After or before correcting male and female body size for age differences, the patterns of SSD failed to obey Rensch's rule or its inverse, even though fecundity selection in toads tends to favor larger female body size. We also found that the degree of SSD was positively correlated with the operational sex ratio in the field across B. minshanicus populations. Thus, sexual and fecundity selection play an equal role driving the evolution of SSD within toads. In addition, sex-specific growth rate and age structure explain part of the variation observed in SSD across populations.

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.

Rapid evolution of sexual size dimorphism facilitated by Y-linked genetic variance.

Sexual dimorphism is ubiquitous in nature but its evolution is puzzling given that the mostly shared genome constrains independent evolution in the sexes. Sex differences should result from asymmetries between the sexes in selection or genetic variation but studies investigating both simultaneously are lacking. Here, we combine a quantitative genetic analysis of body size variation, partitioned into autosomal and sex chromosome contributions and ten generations of experimental evolution to dissect the evolution of sexual body size dimorphism in seed beetles (Callosobruchus maculatus) subjected to sexually antagonistic or sex-limited selection. Female additive genetic variance (VA) was primarily linked to autosomes, exhibiting a strong intersexual genetic correlation with males ([Formula: see text] = 0.926), while X- and Y-linked genes further contributed to the male VA and X-linked genes contributed to female dominance variance. Consistent with these estimates, sexual body size dimorphism did not evolve in response to female-limited selection but evolved by 30-50% under male-limited and sexually antagonistic selection. Remarkably, Y-linked variance alone could change dimorphism by 30%, despite the C. maculatus Y chromosome being small and heterochromatic. Our results demonstrate how the potential for sexual dimorphism to evolve depends on both its underlying genetic basis and the nature of sex-specific selection.

Allometry constrains the evolution of sexual dimorphism in Drosophila across 33 million years of divergence.

Sexual dimorphism is widely viewed as adaptive, reflecting the evolution of males and females toward divergent fitness optima. Its evolution, however, may often be constrained by the shared genetic architecture of the sexes, and by allometry. Here, we investigated the evolution of sexual size dimorphism, shape dimorphism, and their allometric relationship, in the wings of 82 taxa in the family Drosophilidae that have been diverging for at least 33 million years. Shape dimorphism among species was remarkably similar, with males characterized by longer, thinner wings than females. There was, however, quantitative variation among species in both size and shape dimorphism, with evidence that they have adapted to different evolutionary optima in different clades on timescales of about 10 million years. Within species, shape dimorphism was predicted by size, and among species, there was a strong relationship between size dimorphism and shape dimorphism. Allometry constrained the evolution of shape dimorphism for the two most variable traits we studied, but dimorphism was evolutionary labile in other traits. The keys for disentangling alternative explanations for dimorphism evolution are studies of natural and sexual selection, together with a deeper understanding of how microevolutionary parameters of evolvability relate to macroevolutionary patterns of divergence.