Multivariate genetic architecture of the Anolis dewlap reveals both shared and sex‐specific features of a sexually dimorphic ornament

Darwin viewed the ornamentation of females as an indirect consequence of sexual selection on males and the transmission of male phenotypes to females via the ‘laws of inheritance’. Although a number of studies have supported this view by demonstrating substantial between‐sex genetic covariance for ornament expression, the majority of this work has focused on avian plumage. Moreover, few studies have considered the genetic basis of ornaments from a multivariate perspective, which may be crucial for understanding the evolution of sex differences in general, and of complex ornaments in particular. Here, we provide a multivariate, quantitative‐genetic analysis of a sexually dimorphic ornament that has figured prominently in studies of sexual selection: the brightly coloured dewlap of Anolis lizards. Using data from a paternal half‐sibling breeding experiment in brown anoles (Anolis sagrei), we show that multiple aspects of dewlap size and colour exhibit significant heritability and a genetic variance–covariance structure ( G ) that is broadly similar in males ( G _m) and females ( G _f). Whereas sexually monomorphic aspects of the dewlap, such as hue, exhibit significant between‐sex genetic correlations (r_mf), sexually dimorphic features, such as area and brightness, exhibit reduced r_mf values that do not differ from zero. Using a modified random skewers analysis, we show that the between‐sex genetic variance–covariance matrix ( B) should not strongly constrain the independent responses of males and females to sexually antagonistic selection. Our microevolutionary analysis is in broad agreement with macroevolutionary perspectives indicating considerable scope for the independent evolution of coloration and ornamentation in males and females.     

Divergent Sex-Specific Plasticity in Long-Lived Vertebrates with Contrasting Sexual Dimorphism

Sex-specific plasticity can profoundly affect sexual size dimorphism (SSD), but its influence in female-larger-SSD vertebrates remains obscure. Theory predicts that sex-specific plasticity may drive SSD evolution if the larger sex benefits from optimal-growth conditions when available (condition-dependent hypothesis), or if attaining a suboptimal size is penalized by selection (adaptive canalization hypothesis). Sex-specific plasticity enhances the size of the larger sex in male-larger-SSD turtles but whether the same occurs in female-larger species is unknown. Sexual shape dimorphism (SShD) is also widespread in nature but is understudied, and whether SShD derives from sex-specific responses to identical selective pressures or from sex-specific selection remains unclear. Here we tested whether sex-specific growth plasticity underlies the development of sexual size and shape dimorphism in the female-larger-SSD turtle, Podocnemis expansa. Individuals hatched from several incubation temperatures and were raised under common-garden conditions with varying temperature and resources. Body size and shape were plastic and sexually dimorphic, but plasticity did not differ between the sexes, opposite to the male-larger turtle Chelydra serpentina. Maternal effects (egg size) were significant on size and shape, suggesting that females increase their fitness by allocating greater energy to enhance offspring growth. Results ruled out the sex-specific plasticity hypotheses in P. expansa, indicating that SSD and SShD do not derive form differential responses to identical drivers but from sex-specific selective pressures. Our results indicate that differential plasticity does not favor males inherently, nor the larger sex, as would be expected if it was a pervasive driver of macroevolutionary patterns of sexual dimorphism across turtle lineages.     

Implications of Male and Female Contributions to Sexual Size Dimorphism for Inferring Behavior in the Hominin Fossil Record

Sexual dimorphism is commonly used to directly infer or support reconstructions of social behavior in early hominins. This is often done by comparing the magnitude of sexual size dimorphism to that seen in extant primates and extrapolating a likely social behavior. Such comparisons are of limited value, though, allowing only the inference of strong male–male competition when dimorphism is strong. Recent studies have begun to focus on the selective factors that impact female body size, and thereby size dimorphism. Considerations of changes in male and female size in the fossil record potentially allow insight into the meaning of changes in sexual dimorphism through time. To illustrate, I compare estimates of body mass dimorphism for four hominin taxa to assess changes in male and female size. Assuming that early Homo represents a single taxon, sexual size dimorphism increased in early Homo through an increase in male size, but was subsequently reduced through an increase in female size in Homo erectus. This would imply a significant increase in sexual selection acting on males in early Homo. An increase in female size with a loss of dimorphism in Homo erectus would imply a simultaneous shift in female optimal body size through selection for increased female fecundity, and/or an increase in female resource abundance, coupled with a shift in selection acting on male size. Although none of these inferences are certain, the exercise illustrates the potential for considering how dimorphism changes through time, rather than simply focusing on the magnitude of size dimorphism in isolation.     

INTRALOCUS SEXUAL CONFLICT OVER IMMUNE DEFENSE,GENDER LOAD,AND SEX‐SPECIFIC SIGNALING IN A NATURAL LIZARD POPULATION

In species with separate sexes, antagonistic selection on males and females (intralocus sexual conflict) can result in a gender load that can be resolved through the evolution of sexual dimorphism. We present data on intralocus sexual conflict over immune defense in a natural population of free‐ranging lizards (Uta stansburiana) and discuss the resolution of this conflict. Intralocus sexual conflict arises from correlational selection between immune defense and orange throat coloration in these lizards. Males with orange throats and high antibody responses had enhanced survival, but the same trait combination reduced female fitness. This sexual antagonism persisted across the life cycle and was concordant between the juvenile and adult life stages. The opposing selective pressure on males and females is ameliorated by a negative intersexual genetic correlation (r_m,f=?0.86) for immune defense. Throat coloration was also genetically correlated with immune defense, but the sign of this genetic correlation differed between the sexes. This resulted in sex‐specific signaling of immunological condition. We also found evidence for a sex‐specific maternal effect on sons with potential to additionally reduce the gender load. These results have implications for signaling evolution, genetic integration between adaptive traits, sex allocation, and mutual mate choice for indirect fitness benefits.     

Inbreeding alters intersexual fitness correlations in Drosophila simulans.

Intralocus sexual conflict results from sexually antagonistic selection on traits shared by the sexes. This can displace males and females from their respective fitness optima, and negative intersexual correlations (r_mf) for fitness are the unequivocal indicator of this evolutionary conflict. It has recently been suggested that intersexual fitness correlations can vary depending on the segregating genetic variation present in a population, and one way to alter genetic variation and test this idea is via inbreeding. Here, we test whether intersexual correlations for fitness vary with inbreeding in Drosophila simulans isolines reared under homogenous conditions. We measured male and female fitness at different times following the establishment of isofemale lines and found that the sign of the association between the two measures varied with time after initial inbreeding. Our results are consistent with suggestions that the type of genetic variation segregating within a population can determine the extent of intralocus sexual conflict and also support the idea that sexually antagonistic alleles segregate for longer in populations than alleles with sexually concordant effects.     

Low Cross-Sex Genetic Correlation in Carotenoid-Based Plumage Traits in the Blue Tit Nestlings (Cyanistes caeruleus)

In some bird species, both adult and juvenile individuals are often brightly coloured. It has been commonly assumed that identical plumage colouration present in both sexes results from strong intersexual genetic correlations in colour-related traits. Here, we aimed at testing this hypothesis in juvenile individuals and looked at genetic parameters describing carotenoid-based colouration of blue tit nestlings in a wild population. To separate genetic and environmental sources of phenotypic variation we performed a cross-fostering experiment. Our analyses confirmed the existence of sexual dichromatism in blue tit nestlings and revealed a significant, although low, genetic component of carotenoid-based colouration. However, genetic effects are expressed differently across sexes as indicated by low cross-sex genetic correlations (r_mf). Thus our results do not support the prediction of generally high r_mf and suggest that intersexual constraints on the evolution of colouration traits may be weaker than expected. We hypothesise that observed patterns of genetic correlations result from sex-specific selective pressures acting on nestling plumage colouration.     

Sexual dimorphism and courtship behavior in Drosophila prolongata

Sexual dimorphism is often derived from sexual selection. In sexually dimorphic Drosophila species, exaggerated male structures are used for specific behaviors in male-to-male competition or courtship toward females. In Drosophila prolongata, a member of the melanogaster species group, males have enlarged forelegs whereas females do not. However, the adaptive role of the enlarged forelegs is unclear because little is known about the behavior of D. prolongata. In this study, the courtship behavior of D. prolongata was investigated in comparison with closely related species. Males of D. prolongata use their forelegs in a specific behavior, “leg vibration”, in which the male vigorously vibrates the female’s abdomen by extending his forelegs from in front of her. Leg vibration was observed immediately before “attempting copulation”, indicating that it has an adaptive role in the mating process. In contrast, leg vibration was not observed in closely related species. Because the large forelegs are necessary to accomplish leg vibration, it was suggested that the sexual dimorphism of D. prolongata forelegs is currently under the influence of sexual selection in courtship behavior.     

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.     

The importance of pre-and postcopulatory sexual selection promoting adaptation to increasing temperatures

Global temperatures are increasing rapidly affecting species globally. Understanding if and how different species can adapt fast enough to keep up with increasing temperatures is of vital importance. One mechanism that can accelerate adaptation and promote evolutionary rescue is sexual selection. Two different mechanisms by which sexual selection can facilitate adaptation are pre- and postcopulatory sexual selection. However, the relative effects of these different forms of sexual selection in promoting adaptation are unknown. Here, we present the results from an experimental study in which we exposed fruit flies Drosophila melanogaster to either no mate choice or 1 of 2 different sexual selection regimes (pre- and postcopulatory sexual selection) for 6 generations, under different thermal regimes. Populations showed evidence of thermal adaptation under precopulatory sexual selection, but this effect was not detected in the postcopulatory sexual selection and the no choice mating regime. We further demonstrate that sexual dimorphism decreased when flies evolved under increasing temperatures, consistent with recent theory predicting more sexually concordant selection under environmental stress. Our results suggest an important role for precopulatory sexual selection in promoting thermal adaptation and evolutionary rescue.     

Relationship of sexual dimorphism in canine size and body size to social,behavioral, and ecological correlates in anthropoid primates

Among anthropoid primates there are interspecific differences in the degree of sexual dimorphism in both body size and canine size. Within the suborder body size dimorphism and canine size dimorphism are positively correlated,r=0.76. This correlation suggests that the two dimorphisms are equally developed in some species, while in other species there is a differential degree of sexual dimorphism. An analysis of these results and their relation to social organization and other ecological variables reveals: (1) the degree of canine size dimorphism is closely related to the amount of male intrasexual selection in a given mating system; and (2) the degree of body size dimorphism is also related to male intrasexual selection, but may be modified (either enhanced or diminished) by selection pressure from factors such as habitat, diet, foraging behavior, antipredator behavior, locomotory behavior, and female preference.     

The evolution of sexual size dimorphism in the house finch. II. Population divergence in relation to local selection

Recent colonization of ecologically distinct areas in North America by the house finch (Carpodacus mexicanus) was accompanied by strong population divergence in sexual size dimorphism. Here we examined whether this divergence was produced by population differences in local selection pressures acting on each sex. In a long-term study of recently established populations in Alabama, Michigan, and Montana, we examined three selection episodes for each sex: selection for pairing success, overwinter survival, and within-season fecundity. Populations varied in intensity of these selection episodes, the contribution of each episode to the net selection, and in the targets of selection. Direction and intensity of selection strongly differed between sexes, and different selection episodes often favored opposite changes in morphological traits. In each population, current net selection for sexual dimorphism was highly concordant with observed sexual dimorphism--in each population, selection for dimorphism was the strongest on the most dimorphic traits. Strong directional selection on sexually dimorphic traits, and similar intensities of selection in both sexes, suggest that in each of the recently established populations, both males and females are far from their local fitness optimum, and that sexual dimorphism has arisen from adaptive responses in both sexes. Population differences in patterns of selection on dimorphism, combined with both low levels of ontogenetic integration in heritable sexually dimorphic traits and sexual dimorphism in growth patterns, may account for the close correspondence between dimorphism in selection and observed dimorphism in morphology across house finch populations.     

Causes of secondary sexual differences in plants — Evidence from extreme leaf dimorphism in Leucadendron (Proteaceae)

In extreme cases leaves in male plants of the dioecious genus Leucadendron (Proteaceae) are up to an order of magnitude smaller than female leaves. This secondary sexual dimorphism (SSD) in leaf size has previously been suggested to be due to intra-male sexual selection, leading to an increase in male allocation to reproduction in dimorphic species. After critically evaluating previous data provided to support this hypothesis, I suggest on both theoretical grounds and on re-analysis that this argument is unlikely and unsupported. Leaf size dimorphism could theoretically evolve directly due to disruptive ecological selection between genders, leading to niche dimorphism either within or between habitats. I test this ecological causation hypothesis by providing data on specific leaf area (sla) and water use efficiency (δ ¹³C) of leaves from males and females of several Leucadendron species. Results confirm the expectation of minimal gender differences. I argue that leaf dimorphism is a consequence of selection on flower size and architecture.     

Context‐dependent expression of sexual dimorphism in island populations of the common wall lizard (Podarcis muralis)

The condition‐dependent sexual dimorphism model explains the evolution and maintenance of sexual dimorphism in traits targeted by sexual selection, and predicts that the magnitude of sexual dimorphism depends on the variability of individual condition, male traits being more variable than female corresponding traits. Most convincing examples concern insects, while studies among vertebrates are scanty because manipulating condition often is not possible, and the time to reach sexual maturity may be too long. Islands offer a unique opportunity to compare how the environment affects the expression of sexual dimorphism, since they represent ‘natural experimental sets’ in which different populations of the same species may experience alternative environmental constraints. We investigated the occurrence of context‐dependent expression in sexual dimorphism of head shape in insular populations of the common wall lizards (Podarcis muralis) inhabiting the Tuscan Archipelago (Tyrrhenian Sea). Alternative models were formulated: H₀ assumes that the sexual dimorphism is uninfluenced by islands, H₁ assumes the only effect of phylogeny, H_2A and H_2B account for the biogeography of the archipelago (island size and distance from the mainland), while H₃ assumes island‐specific effects on sexual dimorphism. Models were compared using Akaike's information criterion adjusted for multivariate analyses. All hypotheses performed better than H₀, but H₃ largely outperformed all other alternative hypotheses, indicating that environmental features of islands play an additive effect to ontogenetic, biogeographic and genetic factors in defining variation in head shape sexual dimorphism. Our results support the hypothesis of a context‐dependent sexual dimorphism in common wall lizards. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 552–565.     

Reproductive skew drives patterns of sexual dimorphism in sponge-dwelling snapping shrimps

Sexual dimorphism is typically a result of strong sexual selection on male traits used in male–male competition and subsequent female choice. However, in social species where reproduction is monopolized by one or a few individuals in a group, selection on secondary sexual characteristics may be strong in both sexes. Indeed, sexual dimorphism is reduced in many cooperatively breeding vertebrates and eusocial insects with totipotent workers, presumably because of increased selection on female traits. Here, we examined the relationship between sexual dimorphism and sociality in eight species of Synalpheus snapping shrimps that vary in social structure and degree of reproductive skew. In species where reproduction was shared more equitably, most members of both sexes were physiologically capable of breeding. However, in species where reproduction was monopolized by a single individual, a large proportion of females—but not males—were reproductively inactive, suggesting stronger reproductive suppression and conflict among females. Moreover, as skew increased across species, proportional size of the major chela—the primary antagonistic weapon in snapping shrimps—increased among females and sexual dimorphism in major chela size declined. Thus, as reproductive skew increases among Synalpheus, female–female competition over reproduction appears to increase, resulting in decreased sexual dimorphism in weapon size.     

Sexual size dimorphism and selection in the wild in the waterstrider Aquarius remigis: Body size,components of body size and male mating success

Sexual size dimorphism is assumed to be adaptive and is expected to evolve in response to a difference in the net selection pressures on the sexes. Although a demonstration of sexual selection is neither necessary nor sufficient to explain the evolution of sexual size dimorphism, sexual selection is generally assumed to be a major evolutionary force. If contemporary sexual selection is important in the evolution and maintenance of sexual size dimorphism then we expect to see concordance between patterns of sexual selection and patterns of sexual dimorphism. We examined sexual selection in the wild, acting on male body size, and components of body size, in the waterstrider Aquarius remigis, as part of a long term study examining net selection pressures on the two sexes in this species. Selection was estimated on both a daily and annual basis. Since our measure of fitness (mating success) was behavioral, we estimated reliabilities to determine if males perform consistently. Reliabilities were measured as ? statistics and range from fair to perfect agreement with substantial agreement overall. We found significant univariate sexual selection favoring larger total length in the first year of our study but not in the second. Multivariate analysis of components of body size revealed that sexual selection for larger males was not acting directly on total length but on genital length. Sexual selection for larger male body size was opposed by direct selection favoring smaller midfemoral lengths. While males of this species are smaller than females, they have longer genital segments and wider forefemora. Patterns of contemporary sexual selection and sexual size dimorphism agree only for genital length. For total length, and all other components of body size examined, contemporary sexual selection was either nonsignificant or opposed the pattern of size dimporhism. Thus, while the net pressures of contemporary selection for the species may still act to maintain sexual size dimorphism, sexual selection alone does not.     

Sexual dimorphism in the tusked frog, Adelotus brevis (Anura:Myobatrachidae): the roles of natural and sexual selection

At least two adaptive processes can lead to the evolution of sexual dimorphism: sexual selection (e.g. male-male combat) or natural selection (e.g. dietary divergence). We investigated the adaptive significance of a distinctive pattern of sexual dimorphism in a south-eastern Australian frog, Adelotus brevis. Male Adelotus grow larger than female conspecifics, have larger heads relative to body size, and have large paired projections (‘tusks’) in the lower jaw. All of these traits are rare among anurans. We quantified the degree of dimorphism in Adelotus, and gathered data on diets and mating systems of this species to evaluate the possible roles of sexual selection and dietary divergence in favoring die evolution of these sexually dimorphic traits. Analysis of prey items in alimentary tracts revealed significant sex differences in prey types. For example, females ate proportionally more arthropods and fewer molluscs than did males. However, this difference is likely to be a secondary consequence of habitat differences between the sexes (due in turn to their different reproductive roles) rather than a selective force for the evolution of sexual dimorphism. Calling males spend their time in moist habitats where pondsnails are abundant, whereas females are more often encountered in the drier arthropod-rich woodlands. A three-year behavioural ecology study on a field population revealed that reproductive males engage in agonistic interactions, with the sexually dimorphic tusks used to attack rivals. Larger body size contributed to male reproductive success. Small males were excluded from calling sites and, among the calling males, larger animals had higher reproductive success (numbers of matings) than did smaller individuals. Hence, the atypical pattern of sexual dimorphism in Adelotus brevis seems to have resulted from sexual selection for larger body size and tusk size in males, in the context of male-male agonistic behaviour, rather than natural selection for ecological divergence between the sexes.     

Sexual Size Dimorphism in the Color Pattern Elements of Two Mimetic Heliconius Butterflies

Sexual dichromatism and sexual dimorphism of body size are reasonably well studied in butterflies. Sexual size dimorphism of color pattern elements, however, is much less explored. The object of this study is Heliconius, a genus of butterflies well known for the coevolution between mate color preferences and mimicry. Given the sexual role of wing coloration, we investigated the existence of sexual size dimorphism in the wing color elements of a mimetic pair—Heliconius erato phyllis Fabricius and Heliconius besckei Ménétriés—and analyzed the allometric patterns of these traits. Correlation between size of elements in the dorsal and ventral wing surfaces were also estimated. In both species, three out of four elements were larger in males, but the non-dimorphic element was not the same. With regard to the allometric patterns, our most important finding was that smaller males of one species have proportionally larger yellow bars. This is the first study specifically concerning quantitative sexual dimorphism in the coloration of this well-known genus of butterflies and it opens new prospects to investigate sex-related natural selection and sexual selection of color pattern elements.     

Sexual size dimorphism and sexual selection in primates

1. In most animals, females are larger than males. Paradoxically, sexual size dimorphism is biased towards males in most mammalian species. An accepted explanation is that sexual dimorphism in mammals evolved by intramale sexual selection. I tested this hypothesis in primates, by relating sexual size dimorphism to seven proxies of sexual selection intensity: operational sex ratio, mating system, intermale competition, group sex ratio, group size, maximum mating percentage (percentage of observed copulations involving the most successful male), and total paternity (a genetic estimate of the percentage of young sired by the most successful male).
2. I fitted phylogenetic generalised least squares models using sexual size dimorphism as the dependent variable and each of the seven measures of intensity of sexual selection as independent variables. I conducted this comparative analysis with data from 50 extant species of primates, including Homo sapiens, Pan troglodytes, and Gorilla spp.
3. Sexual dimorphism was positively related to the four measures of female monopolisation (operational sex ratio, mating system, intermale competition, and group sex ratio) and in some cases to group size, but was not associated with maximum mating percentage or total paternity. Additional regression analyses indicated that maximum mating percentage and total paternity were negatively associated with group size.
4. These results are predicted by reproductive skew theory: in large groups, males can lose control of the sexual behaviour of the other members of the group or can concede reproductive opportunities to others. The results are also consistent with the evolution of sexual size dimorphism before polygyny, due to the effects of natural, rather than sexual, selection. In birds, the study of molecular paternity showed that variance in male reproductive success is much higher than expected by behaviour. In mammals, recent studies have begun to show the opposite trend, i.e. that intensity of sexual selection is lower than expected by polygyny.
5. Results of this comparative analysis of sexual size dimorphism and sexual selection intensity in primates suggest that the use of intramale sexual selection theory to explain the evolution of polygyny and sexual dimorphism in mammals should be reviewed, and that natural selection should be considered alongside sexual selection as an evolutionary driver of sexual size dimorphism and polygyny in mammals.

     

Becoming Different But Staying Alike: Patterns of Sexual Size and Shape Dimorphism in Bills of Hummingbirds

Hummingbirds are known for their distinctive patterns of sexual dimorphism, with many species exhibiting sex-related differences in various ecologically-relevant traits, including sex-specific differences in bill shape. It is generally assumed that such patterns are consistent across all hummingbird lineages, yet many taxa remain understudied. In this study we examined patterns of sexual size and sexual shape dimorphism in bills of 32 of 35 species in the monophyletic Mellisugini lineage. We also compared patterns of bill size dimorphism in this group to other hummingbird lineages, using data from 219 hummingbird species. Overall, the presence and degree of sexual size dimorphism was similar across all hummingbird lineages, with the majority of Mellisugini species displaying female-biased sexual size dimorphism, patterns that remain unchanged when analyzed in a phylogenetic context. Surprisingly however, we found that sexual dimorphism in bill shape was nearly absent in the Mellisugini clade, with only 3 of the 32 species examined displaying bill shape dimorphism. Based on observations in other hummingbird lineages, the lack of sexual shape dimorphism in Mellisugini is particularly unusual. We hypothesize that the patterns of sexual size dimorphism observed here may be the consequence of differential selective forces that result from competition for ecological resources. We further propose that an influential mechanism underlying shape dimorphism is competition and niche segregation. Taken together, the evolutionary changes in patterns of sexual shape dimorphism observed in Mellisugini suggest that the evolutionary trends of sexual dimorphism in the Trochilidae are far more dynamic than was previously believed.