Robert M. Cox

Sexually Antagonistic Selection, Sexual Dimorphism, and the Resolution of Intralocus Sexual Conflict

Males and females share most of their genomes and express many of the same traits, yet the sexes often have markedly different selective optima for these shared traits. This sexually antagonistic (SA) selection generates intralocus sexual conflict that is thought to be resolved through the evolution of sexual dimorphism. However, we currently know little about the prevalence of SA selection, the components of fitness that generate sexual antagonism, or the relationship between sexual dimorphism and current SA selection. We reviewed published studies to address these questions, using 424 selection estimates representing 89 traits from 34 species. Males and females often differed substantially in the direction and magnitude of selection on shared traits, although statistically significant SA selection was relatively uncommon. Sexual selection generated stronger sexual antagonism than fecundity or viability selection, and these individual components of fitness tended to reinforce one another to generate even stronger sexual antagonism for net fitness. Traits exhibiting strong sexual dimorphism exhibited greater SA selection than did weakly dimorphic traits, although this pattern was not significant after we controlled for the inclusion of multiple traits nested within species. Our results suggest that intralocus sexual conflict often may persist despite the evolution of sexual dimorphism.

A COMPARATIVE TEST OF ADAPTIVE HYPOTHESES FOR SEXUAL SIZE DIMORPHISM IN LIZARDS

Abstract.— It is commonly argued that sexual size dimorphism (SSD) in lizards has evolved in response to two primary, nonexclusive processes: (1) sexual selection for large male size, which confers an advantage in intrasexual mate competition (intrasexual selection hypothesis), and (2) natural selection for large female size, which confers a fecundity advantage (fecundity advantage hypothesis). However, outside of several well‐studied lizard genera, the empirical support for these hypotheses has not been examined with appropriate phylogenetic control. We conducted a comparative phylogenetic analysis to test these hypotheses using literature data from 497 lizard populations representing 302 species and 18 families. As predicted by the intrasexual selection hypothesis, male aggression and territoriality are correlated with SSD, but evolutionary shifts in these categorical variables each explain less than 2% of the inferred evolutionary change in SSD. We found stronger correlations between SSD and continuous estimates of intrasexual selection such as male to female home range ratio and female home range size. These results are consistent with the criticism that categorical variables may obscure much of the actual variation in intrasexual selection intensity needed to explain patterns in SSD. In accordance with the fecundity advantage hypothesis, SSD is correlated with clutch size, reproductive frequency, and reproductive mode (but not fecundity slope, reduced major axis estimator of fecundity slope, length of reproductive season, or latitude). However, evolutionary shifts in clutch size explain less than 8% of the associated change in SSD, which also varies significantly in the absence of evolutionary shifts in reproductive frequency and mode. A multiple regression model retained territoriality and clutch size as significant predictors of SSD, but only 16% of the variation in SSD is explained using these variables. Intrasexual selection for large male size and fecundity selection for large female size have undoubtedly helped to shape patterns of SSD across lizards, but the comparative data at present provide only weak support for these hypotheses as general explanations for SSD in this group. Future work would benefit from the consideration of alternatives to these traditional evolutionary hypotheses, and the elucidation of proximate mechanisms influencing growth and SSD within populations.

Experimentally assessing the relative importance of predation and competition as agents of selection

Field experiments that measure natural selection in response to manipulations of the selective regime are extremely rare, even in systems where the ecological basis of adaptation has been studied extensively. The adaptive radiation of Caribbean Anolis lizards has been studied for decades, leading to precise predictions about the influence of alternative agents of selection in the wild. Here we present experimental evidence for the relative importance of two putative agents of selection in shaping the adaptive landscape for a classic island radiation. We manipulated whole-island populations of the brown anole lizard, Anolis sagrei, to measure the relative importance of predation versus competition as agents of natural selection. We excluded or included bird and snake predators across six islands that ranged from low to high population densities of lizards, then measured subsequent differences in behaviour and natural selection in each population. Predators altered the lizards’ perching behaviour and increased mortality, but predation treatments did not alter selection on phenotypic traits. By contrast, experimentally increasing population density dramatically increased the strength of viability selection favouring large body size, long relative limb length and high running stamina. Our results from A. sagrei are consistent with the hypothesis that intraspecific competition is more important than predation in shaping the selective landscape for traits central to the adaptive radiation of Anolis ecomorphs.

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.

Sex-specific selection and intraspecific variation in sexual size dimorphism.

Sexual size dimorphism (SSD) is thought to evolve due to sex differences in selection on body size, but it is largely unknown whether intraspecific variation in SSD reflects differences in sex‐specific selection among populations. We addressed this question by comparing viability selection between two island populations of the brown anole lizard (Anolis sagrei) that differ in the magnitude of male‐biased SSD. On both islands, females experienced stabilizing selection favoring intermediate size whereas males experienced directional selection favoring larger size. Thus, sex‐specific selection matched the overall pattern of male‐biased SSD, but population differences in the magnitude of SSD were not associated with local differences in selection. Rather, population differences in SSD appear to result from underlying differences in the environmental potential for a rapid growth, coupled with sex‐specific phenotypic plasticity. Males grew more slowly on the island with low SSD whereas growth of females did not differ between islands. Both sexes had substantially lower mass per unit length on the island with low SSD, suggesting that they were in a relatively poorer energetic condition. We propose that this energetic constraint disproportionately impacts growth of males due to their greater absolute energy requirements, thus driving intraspecific variation in SSD.

Testosterone Regulates Sexually Dimorphic Coloration in the Eastern Fence Lizard, Sceloporus undulatus

Abstract Adult male Eastern Fence Lizards (Sceloporus undulatus) possess blue and black ventral patches that function in sex recognition and intrasexual social signaling, but this ventral coloration is absent or greatly reduced in females and juvenile males. Adult males also exhibit a relatively uniform, reddish brown dorsal coloration, while females and juvenile males are cryptically colored, with two rows of dark brown or black chevrons set against a background of gray and brown. In the present report, we show that sexual divergence in ventral coloration is temporally correlated with sexual divergence in plasma testosterone in free-living juvenile males and females, supporting the hypothesis that sexual dichromatism is regulated at least in part by testosterone. We experimentally tested this hypothesis by (1) removing the primary source of circulating testosterone in juvenile males via surgical castration, (2) restoring testosterone in castrated males with tonic-release implants, and (3) implanting intact juvenile females with exogenous testosterone. As predicted by our hypothesis, the development of blue and black ventral coloration in S. undulatus was (1) inhibited by castration in juvenile males, (2) restored by exogenous testosterone following castration in juvenile males, and (3) promoted by exogenous testosterone in juvenile females. The expression of male-specific dorsal coloration was also (1) inhibited by castration and (2) restored by exogenous testosterone following castration in juvenile males. Our results are consistent with established literature supporting the critical role of androgens in the mediation of sexually dimorphic coloration among phrynosomatid lizards.

SEVERE COSTS OF REPRODUCTION PERSIST IN ANOLIS LIZARDS DESPITE THE EVOLUTION OF A SINGLE-EGG CLUTCH

A central tenet of life‐history theory is that investment in reproduction compromises survival. We tested for costs of reproduction in wild brown anoles (Anolis sagrei) by eliminating reproductive investment via surgical ovariectomy and/or removal of oviductal eggs. Anoles are unusual among lizards in that females lay single‐egg clutches at frequent intervals throughout a lengthy reproductive season. This evolutionary reduction in clutch size is thought to decrease the physical burden of reproduction, but our results show that even a single egg significantly impairs stamina and sprint speed. Reproductive females also suffered a reduction in growth, suggesting that the cumulative energetic cost of successive clutches constrains the allocation of energy to other important functions. Finally, in each of two separate years, elimination of reproductive investment increased breeding‐season survival by 56%, overwinter survival by 96%, and interannual survival by 200% relative to reproductive controls. This extreme fitness cost of reproduction may reflect a combination of intrinsic (i.e., reduced allocation of energy to maintenance) and extrinsic (i.e., increased susceptibility to predators) sources of mortality. Our results provide clear experimental support for a central tenet of life‐history theory and show that costs of reproduction persist in anoles despite the evolution of a single‐egg clutch.

FITNESS CONSEQUENCES OF SEX-SPECIFIC SELECTION

Theory suggests that sex‐specific selection can facilitate adaptation in sexually reproducing populations. However, sexual conflict theory and recent experiments indicate that sex‐specific selection is potentially costly due to sexual antagonism: alleles harmful to one sex can accumulate within a population because they are favored in the other sex. Whether sex‐specific selection provides a net fitness benefit or cost depends, in part, on the relative frequency and strength of sexually concordant versus sexually antagonistic selection throughout a species’ genome. Here, we model the net fitness consequences of sex‐specific selection while explicitly considering both sexually concordant and sexually antagonistic selection. The model shows that, even when sexual antagonism is rare, the fitness costs that it imposes will generally overwhelm fitness benefits of sexually concordant selection. Furthermore, the cost of sexual antagonism is, at best, only partially resolved by the evolution of sex‐limited gene expression. To evaluate the key parameters of the model, we analyze an extensive dataset of sex‐specific selection gradients from wild populations, along with data from the experimental evolution literature. The model and data imply that sex‐specific selection may likely impose a net cost on sexually reproducing species, although additional research will be required to confirm this conclusion.

Testosterone Inhibits Growth in Juvenile Male Eastern Fence Lizards (Sceloporus undulatus): Implications for Energy Allocation and Sexual Size Dimorphism

In the eastern fence lizard, Sceloporus undulatus, female‐larger sexual size dimorphism develops because yearling females grow faster than males before first reproduction. This sexual growth divergence coincides with maturational increases in male aggression, movement, and ventral coloration, all of which are influenced by the sex steroid testosterone (T). These observations suggest that male growth may be constrained by energetic costs of activity and implicate T as a physiological regulator of this potential trade‐off. To test this hypothesis, we used surgical castration and subsequent administration of exogenous T to alter the physiological and behavioral phenotypes of field‐active males during the period of sexual growth divergence. As predicted, T inhibited male growth, while castration promoted long‐term growth. Males treated with T also exhibited increased daily activity period, movement, and home range area. Food consumption did not differ among male treatments or sexes, suggesting that the inhibitory effects of T on growth are mediated by patterns of energy allocation rather than acquisition. On the basis of estimates derived from published data, we conclude that the energetic cost of increased daily activity period following T manipulation is sufficient to explain most (79%) of the associated reduction in growth. Further, growth may have been constrained by additional energetic costs of increased ectoparasite load following T manipulation. Similar studies of the proximate behavioral, ecological, and physiological mechanisms involved in growth regulation should greatly improve our understanding of sexual size dimorphism.

Cryptic Sex-Ratio Bias Provides Indirect Genetic Benefits Despite Sexual Conflict

The Size of the Father Evolutionary biologists have recently discovered an intriguing phenomenon: High-fitness males often sire low-fitness daughters. The emerging consensus is that this sexual conflict overwhelms the benefits of mate choice for “good genes,” thus challenging a central tenet of evolutionary theory. Cox and Calsbeek (p. 92, published online 4 March) provide a counterpoint by showing that female brown anole lizards can obtain genetic benefits by biasing offspring sex to produce disproportionately more sons with high-fitness (large) sires. The advantage of this sex-ratio bias was confirmed by tracking the fitness of sons and daughters in their natural environment, illustrating the importance of sexual conflict in the wild. Thus, because maximal fitness payoffs can be achieved by shifting offspring production from daughters to sons as sire size increases, mate choice can overcome antagonistic fitness effects. Female lizards improve their fitness by biasing the sex ratio of their progeny on the basis of sire body size. When selection favors sexual dimorphism, high-fitness parents often produce low-fitness progeny of the opposite sex. This sexual conflict is thought to overwhelm the genetic benefits of mate choice because preferred males incur a cost through the production of low-fitness daughters. We provide a counterpoint in a lizard (Anolis sagrei) that exhibits sexual conflict over body size. By using mate-choice experiments, we show that female brown anoles produce more sons than daughters via large sires but more daughters than sons via small sires. Measures of progeny fitness in the wild suggest that maximal fitness payoffs can be achieved by shifting offspring production from daughters to sons as sire size increases. These results illustrate how the resolution of sexual conflict can restore the genetic benefits of mate choice.