Joel W. McGlothlin

Natural Variation in a Testosterone‐Mediated Trade‐Off between Mating Effort and Parental Effort

Male birds frequently face a trade‐off between acquiring mates and caring for offspring. Hormone manipulation studies indicate that testosterone often mediates this trade‐off, increasing mating effort while decreasing parental effort. Little is known, however, about individual covariation between testosterone and relevant behavior on which selection might act. Using wild, male dark‐eyed juncos (Junco hyemalis), we measured individual variation in testosterone levels before and after standardized injections of gonadotropin‐releasing hormone (GnRH). The GnRH challenges have been shown to produce short‐term testosterone increases that are similar to those produced naturally in response to social stimuli, repeatable in magnitude, and greater in males with more attractive ornaments. We correlated these testosterone increases with behavioral measures of mating and parental effort (aggressive response to a simulated territorial intrusion and nestling feeding, respectively). Males that showed higher postchallenge testosterone displayed more territorial behavior, and males that produced higher testosterone increases above initial levels displayed reduced parental behavior. Initial testosterone levels were positively but nonsignificantly correlated with aggression but did not predict parental behavior. These relationships suggest that natural variation in testosterone, specifically the production of short‐term increases, may underlie individual variation in the mating effort/parental effort trade‐off. We discuss the implications of these results for the evolution of hormonally mediated trade‐offs.

Hormone-mediated suites as adaptations and evolutionary constraints

Hormones mediate the expression of suites of correlated traits and hence may act both to facilitate and constrain adaptive evolution. Selection on one trait within a hormone-mediated suite may, for example, lead to a change in the strength of the hormone signal, causing either beneficial or detrimental changes in correlated traits. Theory and empirical methods for studying correlated trait evolution have been developed by the field of evolutionary quantitative genetics, and here we suggest that their application to the study of hormone-mediated suites may prove fruitful. We present hypotheses for how selection shapes the evolution of hormone-mediated suites and argue that correlational selection, which arises when traits interact in their effects on fitness, may act to alter or conserve the composition of hormone-mediated suites. Next, we advocate using quantitative genetic methods to assess natural covariation among hormone-mediated traits and to measure the strength of natural selection acting on them. Finally, we present illustrative examples from our own work on the evolution of testosterone-mediated suites in male and female dark-eyed juncos. We conclude that future work on hormone-mediated suites, if motivated by quantitative genetic theory, may provide important insights into their dual roles as adaptations and evolutionary constraints.

INTERACTING PHENOTYPES AND THE EVOLUTIONARY PROCESS. III. SOCIAL EVOLUTION

Interactions among conspecifics influence social evolution through two distinct but intimately related paths. First, they provide the opportunity for indirect genetic effects (IGEs), where genes expressed in one individual influence the expression of traits in others. Second, interactions can generate social selection when traits expressed in one individual influence the fitness of others. Here, we present a quantitative genetic model of multivariate trait evolution that integrates the effects of both IGEs and social selection, which have previously been modeled independently. We show that social selection affects evolutionary change whenever the breeding value of one individual covaries with the phenotype of its social partners. This covariance can be created by both relatedness and IGEs, which are shown to have parallel roles in determining evolutionary response. We show that social selection is central to the estimation of inclusive fitness and derive a version of Hamiltons rule showing the symmetrical effects of relatedness and IGEs on the evolution of altruism. We illustrate the utility of our approach using altruism, greenbeards, aggression, and weapons as examples. Our model provides a general predictive equation for the evolution of social phenotypes that encompasses specific cases such as kin selection and reciprocity. The parameters can be measured empirically, and we emphasize the importance of considering both IGEs and social selection, in addition to relatedness, when testing hypotheses about social evolution.

CORRELATIONAL SELECTION LEADS TO GENETIC INTEGRATION OF BODY SIZE AND AN ATTRACTIVE PLUMAGE TRAIT IN DARK‐EYED JUNCOS

Abstract When a traits effect on fitness depends on its interaction with other traits, the resultant selection is correlational and may lead to the integration of functionally related traits. In relation to sexual selection, when an ornamental trait interacts with phenotypic quality to determine mating success, correlational sexual selection should generate genetic correlations between the ornament and quality, leading to the evolution of honest signals. Despite its potential importance in the evolution of signal honesty, correlational sexual selection has rarely been measured in natural populations. In the dark‐eyed junco (Junco hyemalis), males with experimentally elevated values of a plumage trait (whiteness in the tail or “tail white”) are more attractive to females and dominant in aggressive encounters over resources. We used restricted maximum‐likelihood analysis of a long‐term dataset to measure the heritability of tail white and two components of body size (wing length and tail length), as well as genetic correlations between pairs of these traits. We then used multiple regression to assess directional, quadratic, and correlational selection as they acted on tail white and body size via four components of lifetime fitness (juvenile and adult survival, mating success, and fecundity). We found a positive genetic correlation between tail white and body size (as measured by wing length), which indicates past correlational selection. Correlational selection, which was largely due to sexual selection on males, was also found to be currently acting on the same pair of traits. Larger males with whiter tails sired young with more females, most likely due to a combination of female choice, which favors males with whiter tails, and male‐male competition, which favors both tail white and larger body size. To our knowledge, this is the first study to show both genetic correlations between sexually selected traits and currently acting correlational sexual selection, and we suggest that correlational sexual selection frequently may be an important mechanism for maintaining the honesty of sexual signals.

Natural Selection on Testosterone Production in a Wild Songbird Population

Because of their role in mediating life‐history trade‐offs, hormones are expected to be strongly associated with components of fitness; however, few studies have examined how natural selection acts on hormonal variation in the wild. In a songbird, the dark‐eyed junco (Junco hyemalis), field experiments have shown that exogenous testosterone alters individuals’ resolution of the survival‐reproduction trade‐off, enhancing reproduction at the expense of survival. Here we used standardized injections of gonadotropin‐releasing hormone (GnRH) to assay variation in the testosterone production of males. Using measurements of annual survival and reproduction, we found evidence of strong natural selection acting on GnRH‐induced increases in testosterone. Opposite to what would be predicted from the survival‐reproduction trade‐off, patterns of selection via survival and reproduction were remarkably similar. Males with GnRH‐induced testosterone production levels that were slightly above the population mean were more likely to survive and also produced more offspring, leading to strong stabilizing selection. Partitioning reproduction into separate components revealed positive directional selection via within‐pair siring success and stabilizing selection via extrapair mating success. Our data represent the most complete demonstration of natural selection on hormones via multiple fitness components, and they complement previous experiments to illuminate testosterone’s role in the evolution of life‐history trade‐offs.

Hormones and honest signals: males with larger ornaments elevate testosterone more when challenged.

When male investment in mating varies with quality, reliable sexual signals may evolve. In many songbirds, testosterone mediates mating investment, suggesting that signals should be linked to testosterone production. However, because testosterone may change rapidly during behaviour such as territorial aggression and courtship, efforts to establish such a relationship have proved challenging. In a population of dark‐eyed juncos, we measured individual variation in the production of short‐term testosterone increases by injecting gonadotropin‐releasing hormone (GnRH). We found a positive correlation between the magnitude of these increases and the size of a plumage ornament (‘tail white’) previously shown to be important for female choice and male–male competition. We then measured naturally elevated testosterone levels produced during male–male competition and found that they covaried with those induced by GnRH. We suggest that the association between tail white and testosterone increases may allow conspecifics to assess potential mates and competitors reliably using tail white.

HOW TO MEASURE INDIRECT GENETIC EFFECTS: THE CONGRUENCE OF TRAIT-BASED AND VARIANCE-PARTITIONING APPROACHES

Indirect genetic effects (IGEs), which occur when phenotypic expression in one individual is influenced by genes in another conspecific individual, may have a drastic effect on evolutionary response to selection. General evolutionary models of IGEs have been developed using two distinct theoretical frameworks derived from maternal effects theory. The first framework is trait-based and focuses on how phenotypes are influenced by specific traits in a social partner, with the strength of interactions defined by the matrix Ö. The second framework partitions total genetic variance into components representing direct effects, indirect effects, and the covariance between them, without identifying specific social traits responsible for IGEs. The latter framework has been employed more commonly by empiricists because the methods for estimating variance components are relatively straightforward. Here, we show how these two theoretical frameworks are related to each other and derive equations that can be used to translate between them. This translation leads to a generalized method that can be used to estimate &PSgr; via standard quantitative genetic breeding designs or pedigrees from natural populations. This method can be used in a very general set of circumstances and is widely applicable to all IGEs, including maternal effects and other interactions among relatives.

Contribution of direct and maternal genetic effects to life-history evolution

Maternal effects are ubiquitous in nature. In plants, most work has focused on the effects of maternal environments on offspring trait expression. Less is known about the prevalence of genetic maternal effects and how they influence adaptive evolution. Here, we used multivariate genetic models to estimate the contributions of maternal and direct genetic (co)variance, the cross-generation direct-maternal covariance, and M, the matrix of maternal effect coefficients, for life-history traits in Campanulastrum americanum, a monocarpic herb. Following a three-generation breeding design, we grew paternal half-sib families with full-sib relatives of each parent and measured juvenile and adult traits. Seed size was influenced exclusively by maternal environmental effects, whereas maternal genetic effects influenced traits throughout the life cycle, including strong direct and maternal additive genetic correlations within and between generations for phenological and size traits. Examination of M suggested that both juvenile and adult traits in maternal plants influenced the expression of offspring traits. This study reveals substantial potential for genetic maternal effects to contribute to adaptive evolution including cross-generation direct-maternal correlations that may slow selection response, maternal effects on phenology that reinforce genetic correlations, and within- and between-generation genetic correlations that may influence life-history polymorphism.

PHENOTYPIC ASSORTMENT MEDIATES THE EFFECT OF SOCIAL SELECTION IN A WILD BEETLE POPULATION

Social interactions often have major fitness consequences, but little is known about how specific interacting phenotypes affect the strength of natural selection. Social influences on the evolutionary process can be assessed using a multilevel selection approach that partitions the effects of social partner phenotypes on fitness (referred to as social or group selection) from those of the traits of a focal individual (nonsocial or individual selection). To quantify the contribution of social selection to total selection affecting a trait, the patterns of phenotypic association among interactants must also be considered. We estimated selection gradients on male body size in a wild population of forked fungus beetles (Bolitotherus cornutus). We detected positive nonsocial selection and negative social selection on body size operating through differences in copulation success, indicating that large males with small social partners had highest fitness. In addition, we found that, in low‐density demes, the phenotypes of focal individuals were negatively correlated with those of their social partners. This pattern reversed the negative effect of group selection on body size and led to stronger positive selection for body size. Our results demonstrate multilevel selection in nature and stress the importance of considering social selection whenever conspecific interactions occur nonrandomly.

CONVERGENT EVOLUTION OF SEXUAL DIMORPHISM IN SKULL SHAPE USING DISTINCT DEVELOPMENTAL STRATEGIES

Studies integrating evolutionary and developmental analyses of morphological variation are of growing interest to biologists as they promise to shed fresh light on the mechanisms of morphological diversification. Sexually dimorphic traits tend to be incredibly divergent across taxa. Such diversification must arise through evolutionary modifications to sex differences during development. Nevertheless, few studies of dimorphism have attempted to synthesize evolutionary and developmental perspectives. Using geometric morphometric analysis of head shape for 50 Anolis species, we show that two clades have converged on extreme levels of sexual dimorphism through similar, male‐specific changes in facial morphology. In both clades, males have evolved highly elongate faces whereas females retain faces of more moderate proportion. This convergence is accomplished using distinct developmental mechanisms; one clade evolved extreme dimorphism through the exaggeration of a widely shared, potentially ancestral, developmental strategy whereas the other clade evolved a novel developmental strategy not observed elsewhere in the genus. Together, our analyses indicate that both shared and derived features of development contribute to macroevolutionary patterns of morphological diversity among Anolis lizards.