Stephen P. De Lisle

Correlated Evolution of Allometry and Sexual Dimorphism across Higher Taxa

Empirical evidence suggests that Rensch’s rule of allometric scaling of male and female body size, which states that body size divergence is greater across males than across females of a clade, is not universal. In fact, quantitative genetic theory indicates that the sex under historically stronger directional selection will exhibit greater interspecific variance in size. Thus, the pattern of covariance between allometry of male and female body size and sexual size dimorphism (SSD) across related clades allows a test of this causal hypothesis for macroevolutionary trends in SSD. We compiled a data set of published body size estimates from the amphibians, a class with predominantly female-biased SSD, to examine variation in allometry and SSD among clades. Our results indicate that females become the more size-variant sex across species in a family as the magnitude of SSD in that family increases. This rejects Rensch’s rule and implicates selection on females as a driver of both amphibian allometry and SSD. Further, when we combine our data into a single analysis of allometry for the class, we find a significant nonlinear allometric relationship between female body size and male body size. These data suggest that allometry changes significantly as a function of size. Our results illustrate that the relationship between female size and male size varies with both the degree of sexual dimorphism and the body size of a clade.

Behavioral and physiological female responses to male sex ratio bias in a pond-breeding amphibian

IntroductionThe phenomenon of sexual conflict has been well documented, and in populations with biased operational sex ratios the consequences for the rarer sex can be severe. Females are typically a limited resource and males often evolve aggressive mating behaviors, which can improve individual fitness for the male while negatively impacting female condition and fitness. In response, females can adjust their behavior to minimize exposure to aggressive mating tactics or minimize the costs of mating harassment. While male-male competition is common in amphibian mating systems, little is known about the consequences or responses of females. The red-spotted newt (Notophthalmus viridescens) is a common pond-breeding amphibian with a complex, well-studied mating system where males aggressively court females. Breeding populations across much of its range have male-biased sex ratios and we predicted that female newts would have behavioral mechanisms to mitigate mating pressure from males. We conducted four experiments examining the costs and behavioral responses of female N. viridescens exposed to a male-biased environment.ResultsIn field enclosures, we found that female newts exposed to a male-biased environment during the five-month breeding season ended with lower body condition compared to those in a female-biased environment. Shorter-term exposure to a male-biased environment for five weeks caused a decrease in circulating total leukocyte and lymphocyte abundance in blood, which suggests females experienced physiological stress. In behavioral experiments, we found that females were more agitated in the presence of male chemical cues and females in a male-biased environment spent more time in refuge than those in a female-biased environment.ConclusionsOur results indicate that male-biased conditions can incur costs to females of decreased condition and potentially increased risk of infection. However, we found that females can also alter their behavior and microhabitat use under a male-biased sex ratio. Consistent with surveys showing reduced detection probabilities for females, our research suggests that females avoid male encounters using edge and substrate habitat. Our work illustrates the integrated suite of impacts that sexual conflict can have on the structure and ecology of a population.

Ecological Character Displacement between the Sexes

Theory suggests that the evolution of sexual dimorphism in ecologically relevant traits can evolve purely through competition between the sexes for a shared resource. Although more parsimonious hypotheses exist for the evolution of ecological sexual dimorphisms, there are some underappreciated reasons to expect that competition may often play some role in the evolution of sexual dimorphism. Here, we build on past work to outline a set of sufficient criteria to demonstrate a role for resource competition in the evolution of sexual dimorphism, the most critical of which is that resource competition can be directly linked to sexual divergence along the axis of ecologically relevant dimorphism. We then compare the geometry of fitness surfaces across experimental manipulations of density and sex ratio in a semiaquatic salamander (Notophthalmus viridescens). We find consistent disruptive selection on multivariate sexual dimorphism in feeding morphology, which increases in strength with density. Fitness and the strength of divergent selection are negative-frequency dependent in the manner expected under competition-driven divergence between the sexes. Our results constitute direct evidence of resource competition as a driver of sexually antagonist selection and consequently the evolution of sexual dimorphism, providing an illustration of how cause and effect can be separated in studies of sexual divergence in morphology and ecology. We suggest that resource competition may often contribute to sexual divergence jointly with other sources of sex-biased selection, especially when ecological opportunity is sex specific.

Independent evolution of the sexes promotes amphibian diversification

Classic ecological theory predicts that the evolution of sexual dimorphism constrains diversification by limiting morphospace available for speciation. Alternatively, sexual selection may lead to the evolution of reproductive isolation and increased diversification. We test contrasting predictions of these hypotheses by examining the relationship between sexual dimorphism and diversification in amphibians. Our analysis shows that the evolution of sexual size dimorphism (SSD) is associated with increased diversification and speciation, contrary to the ecological theory. Further, this result is unlikely to be explained by traditional sexual selection models because variation in amphibian SSD is unlikely to be driven entirely by sexual selection. We suggest that relaxing a central assumption of classic ecological models—that the sexes share a common adaptive landscape—leads to the alternative hypothesis that independent evolution of the sexes may promote diversification. Once the constraints of sexual conflict are relaxed, the sexes can explore morphospace that would otherwise be inaccessible. Consistent with this novel hypothesis, the evolution of SSD in amphibians is associated with reduced current extinction threat status, and an historical reduction in extinction rate. Our work reconciles conflicting predictions from ecological and evolutionary theory and illustrates that the ability of the sexes to evolve independently is associated with a spectacular vertebrate radiation.

On the standardization of fitness and traits in comparative studies of phenotypic selection

Comparisons of the strength and form of phenotypic selection among groups provide a powerful approach for testing adaptive hypotheses. A central and largely unaddressed issue is how fitness and phenotypes are standardized in such studies; standardization across or within groups can qualitatively change conclusions whenever mean fitness differs between groups. We briefly reviewed recent relevant literature, and found that selection studies vary widely in their scale of standardization, but few investigators motivated their rationale for chosen standardization approaches. Here, we propose that the scale at which fitness should be relativized should reflect whether selection is likely to be hard or soft; that is, the scale at which populations (or hypothetical populations in the case of a contrived experiment) are regulated. We argue that many comparative studies of selection are implicitly or explicitly focused on soft selection (i.e., frequency and density‐dependent selection). In such studies, relative fitness should preferably be calculated using within‐group means, although this approach is taken only occasionally. Related difficulties arise for the standardization of phenotypes. The appropriate scale at which standardization should take place depends on whether groups are considered to be fixed or random. We emphasize that the scale of standardization is a critical decision in empirical studies of selection that should always warrant explicit justification.

Parasitism and the expression of sexual dimorphism

Although a negative covariance between parasite load and sexually selected trait expression is a requirement of few sexual selection models, such a covariance may be a general result of life-history allocation trade-offs. If both allocation to sexually selected traits and to somatic maintenance (immunocompetence) are condition dependent, then in populations where individuals vary in condition, a positive covariance between trait expression and immunocompetence, and thus a negative covariance between trait and parasite load, is expected. We test the prediction that parasite load is generally related to the expression of sexual dimorphism across two breeding seasons in a wild salamander population and show that males have higher trematode parasite loads for their body size than females and that a key sexually selected trait covaries negatively with parasite load in males. We found evidence of a weaker negative relationship between the analogous female trait and parasite infection. These results underscore that parasite infection may covary with expression of sexually selected traits, both within and among species, regardless of the model of sexual selection, and also suggest that the evolution of condition dependence in males may affect the evolution of female trait expression.

Disruptive natural selection predicts divergence between the sexes during adaptive radiation

Abstract Evolution of sexual dimorphism in ecologically relevant traits, for example, via resource competition between the sexes, is traditionally envisioned to stall the progress of adaptive radiation. An alternative view is that evolution of ecological sexual dimorphism could in fact play an important positive role by facilitating sex‐specific adaptation. How competition‐driven disruptive selection, ecological sexual dimorphism, and speciation interact during real adaptive radiations is thus a critical and open empirical question. Here, we examine the relationships between these three processes in a clade of salamanders that has recently radiated into divergent niches associated with an aquatic life cycle. We find that morphological divergence between the sexes has occurred in a combination of head shape traits that are under disruptive natural selection within breeding ponds, while divergence among species means has occurred independently of this disruptive selection. Further, we find that adaptation to aquatic life is associated with increased sexual dimorphism across taxa, consistent with the hypothesis of clade‐wide character displacement between the sexes. Our results suggest the evolution of ecological sexual dimorphism may play a key role in niche divergence among nascent species and demonstrate that ecological sexual dimorphism and ecological speciation can and do evolve concurrently in the early stages of adaptive radiation.

Habitat partitioning during character displacement between the sexes

Ecological differences between the sexes are often interpreted as evidence of within-species ecological character displacement (ECD), a hypothesis with almost no direct tests. Here, we experimentally test two predictions that are direct corollaries of ECD between the sexes, in a salamander. First, we find support for the prediction that each sex has a growth rate advantage in the aquatic microhabitat where it is most commonly found. Second, we test the prediction that selection for ECD in the breeding environment may affect partial migration out of this environment. We found that phenotype-dependent migration resulted in a shift in the phenotypic distribution across treatments, with the highest sexual dimorphism occurring among residents at high founding density, suggesting that migration and ECD can both be driven by competition. Our work illustrates how complex patterns of habitat partitioning evolve during ECD between the sexes and suggest ECD and partial migration can interact to effect both ecological dynamics and evolution of sexual dimorphism.