Phylogeny suggests nondirectional and isometric evolution of sexual size dimorphism in argiopine spiders

Sexual dimorphism describes substantial differences between male and female phenotypes. In spiders, sexual dimorphism research almost exclusively focuses on size, and recent studies have recovered steady evolutionary size increases in females, and independent evolutionary size changes in males. Their discordance is due to negative allometric size patterns caused by different selection pressures on male and female sizes (converse Rensch's rule). Here, we investigated macroevolutionary patterns of sexual size dimorphism (SSD) in Argiopinae, a global lineage of orb‐weaving spiders with varying degrees of SSD. We devised a Bayesian and maximum‐likelihood molecular species‐level phylogeny, and then used it to reconstruct sex‐specific size evolution, to examine general hypotheses and different models of size evolution, to test for sexual size coevolution, and to examine allometric patterns of SSD. Our results, revealing ancestral moderate sizes and SSD, failed to reject the Brownian motion model, which suggests a nondirectional size evolution. Contrary to predictions, male and female sizes were phylogenetically correlated, and SSD evolution was isometric. We interpret these results to question the classical explanations of female‐biased SSD via fecundity, gravity, and differential mortality. In argiopines, SSD evolution may be driven by these or additional selection mechanisms, but perhaps at different phylogenetic scales.     

Juvenile hormone mediates sexual dimorphism in horned beetles

The causes and consequences of sexual dimorphism are major themes in biology. Here we explore the endocrine regulation of sexual dimorphism in horned beetles. Specifically, we explore the role of juvenile hormone (JH) in regulating horn expression in females of two species with regular sexual dimorphism for pronotal horns (females have much shorter horns than males) and a third species with a rare reversed sexual dimorphism for both pronotal and head horns (females have much larger horns in both body regions compared with males). Applications of the JH analog methoprene caused females of the two more typical species to grow significantly shorter pronotal horns than control females, whereas no consistent effect on pronotal horn development was detected in the third, sex-reversed species. Instead, females in this species showed an unexpected and significant increase in head horn expression in response to methoprene treatment. Lastly, horn shape was also affected in females of one of the regularly sexually dimorphic species, but in the opposite direction than horn length. Although methoprene exerted a feminizing effect on female horn length in this species, it significantly masculinized horn shape by inducing a peculiar shape change observed naturally only in males. Our results suggest that JH influences both overall size and shape of female horns, but does so flexibly and as a function of species, sex and horn location. We use our results to review current models on the role of endocrine mechanisms in development and evolution of horned beetle diversity.     

Testosterone,growth and the evolution of sexual size dimorphism

The integration of macroevolutionary pattern with developmental mechanism presents an outstanding challenge for studies of phenotypic evolution. Here, we use a combination of experimental and comparative data to test whether evolutionary shifts in the direction of sexual size dimorphism (SSD) correspond to underlying changes in the endocrine regulation of growth. First, we combine captive breeding studies with mark‐recapture data to show that male‐biased SSD develops in the brown anole lizard (Anolis sagrei) because males grow significantly faster than females as juveniles and adults. We then use castration surgeries and testosterone implants to show that castration inhibits, and testosterone stimulates, male growth. We conclude by reviewing published testosterone manipulations in other squamate reptiles in the context of evolutionary patterns in SSD. Collectively, these studies reveal that the evolution of SSD has been accompanied by underlying changes in the effect of testosterone on male growth, potentially facilitating the rapid evolution of SSD.     

Ecomorphological variation in male and female wall lizards and the macroevolution of sexual dimorphism in relation to habitat use

Understanding how phenotypic diversity evolves is a major interest of evolutionary biology. Habitat use is an important factor in the evolution of phenotypic diversity of many animal species. Interestingly, male and female phenotypes have been frequently shown to respond differently to environmental variation. At the macroevolutionary level, this difference between the sexes is frequently analysed using phylogenetic comparative tools to assess variation in sexual dimorphism (SD) across taxa in relation to habitat. A shortcoming of such analyses is that they evaluate the degree of dimorphism itself and therefore they do not provide access to the evolutionary trajectories of each sex. As such, the relative contribution of male and female phenotypes on macroevolutionary patterns of sexual dimorphism cannot be directly assessed. Here, we investigate how habitat use shapes phenotypic diversity in wall lizards using phylogenetic comparative tools to simultaneously assess the tempo and mode of evolution in males, females and the degree of sexual dimorphism. We find that both sexes have globally diversified under similar, but not identical, processes, where habitat use seems to drive macroevolutionary variation in head shape, but not in body size or relative limb length. However, we also observe small differences in the evolutionary dynamics of male and female phenotypes that have a marked impact on macroevolutionary patterns of SD, with important implications for our interpretation of what drives phenotypic diversification within and between the sexes.     

Mimetic butterflies support Wallace's model of sexual dimorphism

Theoretical and empirical observations generally support Darwin's view that sexual dimorphism evolves due to sexual selection on, and deviation in, exaggerated male traits. Wallace presented a radical alternative, which is largely untested, that sexual dimorphism results from naturally selected deviation in protective female coloration. This leads to the prediction that deviation in female rather than male phenotype causes sexual dimorphism. Here I test Wallace's model of sexual dimorphism by tracing the evolutionary history of Batesian mimicry-an example of naturally selected protective coloration-on a molecular phylogeny of Papilio butterflies. I show that sexual dimorphism in Papilio is significantly correlated with both female-limited Batesian mimicry, where females are mimetic and males are non-mimetic, and with the deviation of female wing colour patterns from the ancestral patterns conserved in males. Thus, Wallace's model largely explains sexual dimorphism in Papilio. This finding, along with indirect support from recent studies on birds and lizards, suggests that Wallace's model may be more widely useful in explaining sexual dimorphism. These results also highlight the contribution of naturally selected female traits in driving phenotypic divergence between species, instead of merely facilitating the divergence in male sexual traits as described by Darwin's model.     

Sexual selection,sexual dimorphism and plant phylogeny

Summary Darwin examined sexual dimorphism in animals, arguing that sexual selection was important in the evolution of such dimorphism. Sexual dimorphism in plants may have parallel causes and costs.The processes that contribute to sexual dimorphism may also lead to speciation and morphological differences among related species, as argued originally by Darwin. Where sexes are separate and dimorphism is well-developed, males of related animal species (both vertebrate and invertebrate) are often strikingly different from each other, while females may be virtually indistinguishable. A similar pattern may exist in plants: it is frequently the males (of dioecious taxa) or the male portions of the flower (in co-sexual flowers) that apparently have diversified. I suggest that the similarity of pattern may be accounted for by a similarity of process.In addition, sexual selection may have contributed to certain evolutionary trends within the angiosperms and, indeed, to angiosperm radiation.     

Proximate determination of male horn dimorphism in the beetle Onthophagus taurus (Coleoptera: Scarabaeidae)

The existence of discrete phenotypic variation within one sex poses interesting questions regarding how such intrasexual polymorphisms are produced and modified during the course of evolution. Approaching these kinds of questions requires insights into the genetic architecture underlying a polymorphism and an understanding of the proximate mechanisms determining phenotype expression. Here we explore the genetic underpinnings and proximate factors influencing the expression of beetle horns – a dramatic sexually selected trait exhibiting intramale dimorphism in many species. Two relatively discrete male morphs are present in natural populations of the dung beetle Onthophagus taurus (Scarabaeidae, Onthophagini). Males exceeding a critical body size develop a pair of long, curved horns on their heads, while those smaller than this critical body size remain essentially hornless. We present results from laboratory breeding experiments designed to assess the relative importance of inherited and environmental factors as determinants of male morphology. Using father–son regressions, our findings demonstrate that horn length and body size of male progeny are not predicted from paternal morphology. Instead, natural variation in an environmental factor, the amount of food available to larvae, determined both the body sizes exhibited by males as adults and the presence or absence of horns. The nonlinear scaling relationship between the body size and horn length of males bred in the laboratory did not differ from the pattern of variation present in natural populations, suggesting that nutritional conditions account for variation in male morphology in natural populations as well. We discuss our results by extending ideas proposed to explain the evolution of conditional expression of alternative phenotypes in physically heterogeneous environments toward incorporating facultative expression of secondary sexual traits. We use this synthesis to begin characterizing the potential origin and subsequent evolution of facultative horn expression in onthophagine beetles.     

Ecology and mating competition influence sexual dimorphism in Tanganyikan cichlids

Sexual selection contributes strongly to the evolution of sexual dimorphism among animal taxa. However, recent comparative analyses have shown that evolution of sexual dimorphism can be influenced by extrinsic factors like mating system and environment, and also that different types of sexual dimorphism may present distinct evolutionary pathways. Investigating the co-variation among different types of sexual dimorphism and their association with environmental factors can therefore provide important information about the mechanisms generating variation in sexual dimorphism among contemporary species. Using phylogenetic comparative analyses comparing 49 species of Tanganyikan cichlid fishes, we first investigated the pairwise relationship between three types of sexual dimorphism [size dimorphism (SSD), colour dimorphism (COD) and shape dimorphism (SHD)] and how they were related to the strength of pre- and post-copulatory sexual selection. We then investigated the influence of ecological features on sexual dimorphism. Our results showed that although SSD was associated with the overall strength of sexual selection it was not related to other types of sexual dimorphism. Also, SSD co-varied with female size and spawning habitat, suggesting a role for female adaptations to spawn in small crevices and shells influencing SSD in this group. Further, COD and SHD were positively associated and both show positive relationships with the strength of sexual selection. Finally, the level of COD and SHD was related to habitat complexity. Our results thus highlight distinct evolutionary pathways for different types of sexual dimorphism and further that ecological factors have influenced the evolution of sexual dimorphism in Tanganyikan cichlid fishes.     

Sexual and male horn dimorphism in Copris ochus (Coleoptera: Scarabaeidae)

Copris ochus (Coleoptera: Scarabaeidae), an endangered species, is the largest dung beetle in Japan. In C. ochus, males have a long head horn, while females lack this long horn (sexual dimorphism). Very large males of C. ochus have disproportionately longer head horns than small males, suggesting male horn dimorphism, although the dimorphism has not been investigated quantitatively. To clarify sexual and male horn dimorphism in C. ochus quantitatively, we examined the scaling relationship between body size (prothorax width) and head horn length in 94 females and 76 males. These beetles were captured during July 1978 from a natural population on Mt. Aso in southwestern Japan using a light trap. Although the horn length of the females and males scaled with prothorax width, the scaling relationship differed between the sexes, i.e., the relationship was linear in females and nonlinear in males. Statistical tests for dimorphism in male horn length showed a significant discontinuous relationship, thus indicating distinct sexual and male dimorphism in head horns. Long- and short-horned C. ochus males may have different reproductive behaviors, as described in other horned dung beetles.     

Testing some hypotheses on human evolution and sexual dimorphism

Research on human evolution and sexual dimorphism motivates an interesting test problem. In studying hominid phylogeny it is of interest to test whether parallel evolution plays a role. With regard to sexual dimorphism it is of interest to known whether the directions of sexual dimorphism in the populations being compared are the same. We show that testing these two problems gives rise to the same type of hypothesis testing, viz. the problem of testing the hypothesis that the means of independent, normally distributed random vectors with unit covariance matrices are situated on a straight line through the origin. A test is proposed and applied to study the sexual dimorphism of 20 recent skull populations. In this example the hypothesis of equal directions of sexual dimorphism is rejected. The classical theory of constructing multiple discriminant functions (canonical variates) is adapted to the problem of comparing sexual dimorphisms.     

Testing some hypotheses on Human Evolution and sexual dimorphism

Research on human evolution and sexual dimorphism motivates an interesting test problem. In studying hominid phylogeny it is of interest to test whether parallel evolution plays a role. With regard to sexual dimorphism it is of interest to know whether the directions of sexual dimorphism in the populations being compared are the same. We show that testing these two problems gives rise to the same type of hypothesis testing, viz. the problem of testing the hypothesis that the means of independent, normally distributed random vectors with unit covariance matrices are situated on a straight line through the origin. A test is proposed and applied to study the sexual dimorphism of 20 recent skull populations. In this example the hypothesis of equal directions of sexual dimorphism is rejected. The classical theory of constructing multiple discriminant functions (canonical variates) is adapted to the problem of comparing sexual dimorphisms.     

Selection in a fluctuating environment and the evolution of sexual dimorphism in the seed beetle Callosobruchus maculatus

Temperature changes in the environment, which realistically include environmental fluctuations, can create both plastic and evolutionary responses of traits. Sexes might differ in either or both of these responses for homologous traits, which in turn has consequences for sexual dimorphism and its evolution. Here, we investigate both immediate changes in and the evolution of sexual dimorphism in response to a changing environment (with and without fluctuations) using the seed beetle Callosobruchus maculatus. We investigate sex differences in plasticity and also the genetic architecture of body mass and developmental time dimorphism to test two existing hypotheses on sex differences in plasticity (adaptive canalization hypothesis and condition dependence hypothesis). We found a decreased sexual size dimorphism in higher temperature and that females responded more plastically than males, supporting the condition dependence hypothesis. However, selection in a fluctuating environment altered sex-specific patterns of genetic and environmental variation, indicating support for the adaptive canalization hypothesis. Genetic correlations between sexes (r(MF) ) were affected by fluctuating selection, suggesting facilitated independent evolution of the sexes. Thus, the selective past of a population is highly important for the understanding of the evolutionary dynamics of sexual dimorphism.     

Sexual size dimorphism in shorebirds, gulls, and alcids: the influence of sexual and natural selection

Abstract. Charadrii (shorebirds, gulls, and alcids) have an unusual diversity in their sexual size dimorphism, ranging from monomorphism to either male-biased or female-biased dimorphism. We use comparative analyses to investigate whether this variation relates to sexual selection through competition for mates or natural selection through different use of resources by males and females. As predicted by sexual selection theory, we found that in taxa with socially polygynous mating systems, males were relatively larger than females compared with less polygynous species. Furthermore, evolution toward socially polyandrous mating systems was correlated with decreases in relative male size. These patterns depend on the kinds of courtship displays performed by males. In taxa with acrobatic flight displays, males are relatively smaller than in taxa in which courtship involves simple flights or displays from the ground. This result remains significant when the relationship with mating system is controlled statistically, thereby explaining the enigma of why males are often smaller than females in socially monogamous species. We did not find evidence that evolutionary changes in sexual dimorphism relate to niche division on the breeding grounds. In particular, biparental species did not have greater dimorphism in bill lengths than uniparental species, contrary to the hypothesis that selection for ecological divergence on the breeding grounds has been important as a general explanation for patterns of bill dimorphism. Taken together, these results strongly suggest that sexual selection has had a major influence on sexual size dimorphism in Charadrii, whereas divergence in the use of feeding resources while breeding was not supported by our analyses.     

Directional changes in sexual size dimorphism in shorebirds, gulls and alcids

The Charadrii (shorebirds, gulls and alcids) are one of the most diverse avian groups from the point of view of sexual size dimorphism, exhibiting extremes in both male-biased and female-biased dimorphism, as well as monomorphism. In this study we use phylogenetic comparative analyses to investigate how size dimorphism has changed over evolutionary time, distinguishing between changes that have occurred in females and in males. Independent contrasts analyses show that both body mass and wing length have been more variable in males than in females. Directional analyses show that male-biased dimorphism has increased after inferred transitions towards more polygynous mating systems. There have been analogous increases in female-biased dimorphism after transitions towards more socially polyandrous mating systems. Changes in dimorphism in both directions are attributable to male body size changing more than female body size. We suggest that this might be because females are under stronger natural selection constraints related to fecundity. Taken together, our results suggest that the observed variation in dimorphism of Charadrii can be best explained by male body size responding more sensitively to variable sexual selection than female body size.     

Evolution of mating preference and sexual dimorphism

A quantitative genetic model of the joint evolution of female mating preferences and sexual dimorphism in homologous characters of the sexes is described for polygamous species with no male parental effort, such that mating preferences are selectively neutral and evolve only by indirect selection on genetically correlated characters. The male character and the homologous female character are each under stabilizing natural selection toward an optimum phenotype. At an evolutionary equilibrium the female character under natural selection is at its optimum, whereas there is a line of possible equilibria between female mating preferences and the male character. The line of equilibria may be stable or unstable, depending on the intensity of natural selection, the type of mating preferences, and the inheritance of the characters. Various mechanisms for maladaptive evolution of mating preferences and sexual dimorphism are discussed.     

Ontogeny of sexual dimorphism via tissue duplication in an ostracod (Crustacea)

SUMMARY The adaptive significance of specific sexual dimorphism is well studied. However, the evolutionary history and ontogenic origins of the dimorphism are often unknown. As dimorphism represents two phenotypes generated from relatively similar genotypes, it is of interest to understand both its evolutionary and developmental/genetic underpinnings. Here, we present the first ontogenetic examination of the eyes of philomedid ostracods (Crustacea), which exhibit extremely sexually dimorphic lateral eyes. Adult male philomedids have large compound lateral eyes, whereas females have rudimentary lateral eyes. First, we show that eye dimorphism is unlikely to be due to additional genes present on a male-specific chromosome because karyotype analysis suggests philomedids are XX/XO. We then examine the ontogeny of eye development and find that in at least two species of Euphilomedes , this dimorphism is not generated solely by differences in tissue growth rates, as has been commonly shown for sexually dimorphic characters of other species. Instead, the dimorphism appears to arise during development via tissue duplication, where a single tissue becomes two, perhaps with different developmental potentials. The second eye field is only observed in male Euphilomedes , producing most of the adult eye tissue. We point out that tissue duplication is a developmental process with evolutionary implications because novel characters could evolve via alternative modification of the duplicated fields, analogous to the origin of new genes by gene duplication and alternative modification. Depending on the evolutionary history of the duplicated field, it may have either facilitated or directly caused the observed sexual dimorphism of philomedid ostracods.     

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.     

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.