Robert M. Cox

Natural selection on thermal performance in a novel thermal environment.

Significance Tropical ectotherms are considered especially vulnerable to climate change because they have narrow thermal tolerance ranges, such that even small increases in environmental temperature are likely to be detrimental. Although evolutionary adaptation may prevent extinction, it is unclear whether climate change generates selection on thermal physiology in nature or whether the strength of this selection is sufficient for rapid evolution to occur. When we transplanted lizards from their preferred habitat to a warmer and more thermally variable site, strong natural selection favored individuals that ran faster at warmer temperatures and across a broader range of temperatures. If thermal performance traits are heritable, some tropical species may be capable of rapid evolutionary adaptation to changing climates. Tropical ectotherms are thought to be especially vulnerable to climate change because they are adapted to relatively stable temperature regimes, such that even small increases in environmental temperature may lead to large decreases in physiological performance. One way in which tropical organisms may mitigate the detrimental effects of warming is through evolutionary change in thermal physiology. The speed and magnitude of this response depend, in part, on the strength of climate-driven selection. However, many ectotherms use behavioral adjustments to maintain preferred body temperatures in the face of environmental variation. These behaviors may shelter individuals from natural selection, preventing evolutionary adaptation to changing conditions. Here, we mimic the effects of climate change by experimentally transplanting a population of Anolis sagrei lizards to a novel thermal environment. Transplanted lizards experienced warmer and more thermally variable conditions, which resulted in strong directional selection on thermal performance traits. These same traits were not under selection in a reference population studied in a less thermally stressful environment. Our results indicate that climate change can exert strong natural selection on tropical ectotherms, despite their ability to thermoregulate behaviorally. To the extent that thermal performance traits are heritable, populations may be capable of rapid adaptation to anthropogenic warming.

Hormones as Mediators of Phenotypic and Genetic Integration: an Evolutionary Genetics Approach

Evolutionary endocrinology represents a synthesis between comparative endocrinology and evolutionary genetics. This synthesis can be viewed through the breeders equation, a cornerstone of quantitative genetics that, in its univariate form, states that a populations evolutionary response is the product of the heritability of a trait and selection on that trait (R = h(2)S). Under this framework, evolutionary endocrinologists have begun to quantify the heritability of, and the strength of selection on, a variety of hormonal phenotypes. With specific reference to our work on testosterone and corticosterone in birds and lizards, we review these studies while emphasizing the challenges of applying this framework to hormonal phenotypes that are inherently plastic and mediate adaptive responses to environmental variation. Next, we consider the untapped potential of evolutionary endocrinology as a framework for exploring multivariate versions of the breeders equation, with emphasis on the role of hormones in structuring phenotypic and genetic correlations. As an extension of the familiar concepts of phenotypic integration and hormonal pleiotropy, we illustrate how the hormonal milieu of an individual acts as a local environment for the expression of genes and phenotypes, thereby influencing the quantitative genetic architecture of multivariate phenotypes. We emphasize that hormones are more than mechanistic links in the translation of genotype to phenotype: by virtue of their pleiotropic effects on gene expression, hormones structure the underlying genetic variances and covariances that determine a populations evolutionary response to selection.

Experimentally decoupling reproductive investment from energy storage to test the functional basis of a life-history trade-off

The ubiquitous life-history trade-off between reproduction and survival has long been hypothesized to reflect underlying energy-allocation trade-offs between reproductive investment and processes related to self-maintenance. Although recent work has questioned whether energy-allocation models provide sufficient explanations for the survival cost of reproduction, direct tests of this hypothesis are rare, especially in wild populations. This hypothesis was tested in a wild population of brown anole lizards (Anolis sagrei) using a two-step experiment. First, stepwise variation in reproductive investment was created using unilateral and bilateral ovariectomy (OVX) along with intact (SHAM) control. Next, this manipulation was decoupled from its downstream effects on energy storage by surgically ablating the abdominal fat stores from half of the females in each reproductive treatment. As predicted, unilateral OVX (intermediate reproductive investment) induced levels of growth, body condition, fat storage and breeding-season survival that were intermediate between the high levels of bilateral OVX (no reproductive investment) and the low levels of SHAM (full reproductive investment). Ablation of abdominal fat bodies had a strong and persistent effect on energy stores, but it did not influence post-breeding survival in any of the three reproductive treatments. This suggests that the energetic savings of reduced reproductive investment do not directly enhance post-breeding survival, with the caveat that only one aspect of energy storage was manipulated and OVX itself had no overall effect on post-breeding survival. This study supports the emerging view that simple energy-allocation models may often be insufficient as explanations for the life-history trade-off between reproduction and survival.

Female anoles retain responsiveness to testosterone despite the evolution of androgen‐mediated sexual dimorphism

Summary 1. The evolution of sexual dimorphism presents a challenge because males and females must express two phenotypes from the same underlying genome. In vertebrates, one solution to this challenge is to link the expression of shared traits to sex steroids. However, even ‘male-biased’ steroids such as testosterone (T) circulate at biologically significant levels in females, raising the question of whether sexual dimorphism evolves not only through the coupling of trait expression to T in males, but also through the decoupling of trait expression from T in females. 2. We tested these alternatives by asking whether male and female brown anoles (Anolis sagrei) respond to exogenous T in similar fashion with respect to a suite of sexually dimorphic traits: growth, skeletal morphology, resting metabolism, fat storage, dewlap size and dewlap colour. 3. First, we established the ontogeny of sexual dimorphism in a colony raised in a laboratory common garden. Next, we treated juveniles of each sex with either T implants or empty implants at 5–8 months of age, when sexual dimorphism first began to develop for most traits. 4. T stimulated growth in both sexes and largely abolished natural sex differences in growth. This effect was associated with the stimulation of resting metabolism and the diversion of energy from fat and liver stores in both sexes. T also enlarged the dewlap in both sexes, though females never developed dewlaps equal in size to those of males. Finally, T altered the brightness and saturation of the dewlap in both sexes, inducing coloration similar to that of adult males. 5. Female brown anoles retain many of the same tissue-specific responses to T that occur in males, suggesting that the evolution of androgen-mediated sexual dimorphism has been achieved largely through the coupling of trait expression to sex differences in circulating T, without an associated decoupling of trait expression from T in females.

An experimental test of the role of predators in the maintenance of a genetically based polymorphism.

Polymorphisms provide one of the most useful tools for understanding the maintenance of genetic and phenotypic variation in nature. We have previously described a genetically based polymorphism in dorsal patterning that is expressed by female brown anole lizards, Anolis sagrei, which occur in Bar, Diamond and intermediate Diamond–Bar morphs. Previous studies of island populations in The Bahamas support a role for selection in maintaining the polymorphism, but the agents responsible for this selection remain unclear. We tested two main hypotheses regarding the importance of predation as a selective agent that maintains the polymorphism within populations. First, we tested whether correlational selection favours different combinations of morph, locomotor performance and escape behaviour by measuring morph‐specific natural selection on sprint speed, running endurance and the propensity of females to either ‘freeze’ or ‘run’ in response to attempted capture. Morphs did not differ in any of these traits, nor did correlational selection consistently favour any particular combinations of morph and antipredator behaviour. Second, we experimentally excluded bird and snake predators from two entire island populations, allowed these predators access to two additional islands and then measured subsequent differences in natural selection on morphs in each population. Predators reduced the survival of Bar and Diamond females, but not of genetically intermediate Diamond–Bar females. These results provide limited evidence that predation may play a role in maintaining this polymorphism, although the functional traits that could account for differential susceptibility to predation remain unclear.

Survival of the fattest? Indices of body condition do not predict viability in the brown anole (Anolis sagrei)

Summary nMeasures of body mass and length are commonly used to derive indices of condition, which are often assumed to reflect the energetic state of an animal and, by extension, to predict its fitness. However, the relationship between condition and fitness is rarely quantified, and the appropriate method(s) for deriving indices of condition are frequently debated. nData from a decade of mark–recapture studies involving over 4,600 individual lizards (Anolis sagrei) and 41 replicates of selection across seven populations were used to test the common assumption that condition, as estimated from body mass and length, is a strong predictor of adult survival, an important component of fitness. Inferences about natural selection were compared between two alternative indices of condition: the popular residual index (Ri), and the scaled mass index (Mi), which was recently proposed as a more appropriate method. nLinear, quadratic and correlational selection gradients obtained using Ri and Mi were highly correlated with one another. Relative to variance in selection among replicates and to error associated with the estimation of selection gradients, variance due to the use of alternative condition indices was minor and effectively negligible. nContrary to the intuitive prediction that individuals in better condition should exhibit higher survival, there was no evidence for strong or consistent linear (directional) selection for higher condition indices in either males or females. Significant quadratic (stabilizing or disruptive) selection on condition was similarly rare in both sexes. Correlational selection favoured combinations of large size and high condition in males, but not females. nCollectively, these results indicate that inferences about natural selection may be robust to the choice between indices of condition but that indices of condition can be unreliable as proxies for fitness, particularly when relationships between fitness components and condition are contingent upon interactions with other traits.

Does adaptive radiation of a host lineage promote ecological diversity of its bacterial communities? A test using gut microbiota of Anolis lizards

Adaptive radiations provide unique opportunities to test whether and how recent ecological and evolutionary diversification of host species structures the composition of entire bacterial communities. We used 16S rRNA gene sequencing of faecal samples to test for differences in the gut microbiota of six species of Puerto Rican Anolis lizards characterized by the evolution of distinct ‘ecomorphs’ related to differences in habitat use. We found substantial variation in the composition of the microbiota within each species and ecomorph (trunk‐crown, trunk‐ground, grass‐bush), but no differences in bacterial alpha diversity among species or ecomorphs. Beta diversity analyses revealed subtle but significant differences in bacterial composition related to host phylogeny and species, but these differences were not consistently associated with Anolis ecomorph. Comparison of a trunk‐ground species from this clade (A. cristatellus) with a distantly related member of the same ecomorph class (A. sagrei) where the two species have been introduced and are now sympatric in Florida revealed pronounced differences in the alpha diversity and beta diversity of their microbiota despite their ecological similarity. Comparisons of these populations with allopatric conspecifics also revealed geographic differences in bacterial alpha diversity and beta diversity within each species. Finally, we observed high intraindividual variation over time and strong effects of a simplified laboratory diet on the microbiota of A. sagrei. Collectively, our results indicate that bacterial communities are only weakly shaped by the diversification of their lizard hosts due to the strikingly high levels of bacterial diversity and variation observed within Anolis species.

Hormonally Mediated Increases in Sex-Biased Gene Expression Accompany the Breakdown of Between-Sex Genetic Correlations in a Sexually Dimorphic Lizard

The evolution of sexual dimorphism is predicted to occur through reductions in between-sex genetic correlations (rmf) for shared traits, but the physiological and genetic mechanisms that facilitate these reductions remain largely speculative. Here, we use a paternal half-sibling breeding design in captive brown anole lizards (Anolis sagrei) to show that the development of sexual size dimorphism is mirrored by the ontogenetic breakdown of rmf for body size and growth rate. Using transcriptome data from the liver (which integrates growth and metabolism), we show that sex-biased gene expression also increases dramatically between ontogenetic stages bracketing this breakdown of rmf. Ontogenetic increases in sex-biased expression are particularly evident for genes involved in growth, metabolism, and cell proliferation, suggesting that they contribute to both the development of sexual dimorphism and the breakdown of rmf. Mechanistically, we show that treatment of females with testosterone stimulates the expression of male-biased genes while inhibiting the expression of female-biased genes, thereby inducing male-like phenotypes at both organismal and transcriptomic levels. Collectively, our results suggest that sex-specific modifiers such as testosterone can orchestrate sex-biased gene expression to facilitate the phenotypic development of sexual dimorphism while simultaneously reducing genetic correlations that would otherwise constrain the independent evolution of the sexes.

Correlated evolution between targets of pre- and postcopulatory sexual selection across squamate reptiles.

Abstract Sexual selection reflects the joint contributions of precopulatory selection, which arises from variance in mating success, and postcopulatory selection, which arises from variance in fertilization success. The relative importance of each episode of selection is variable among species, and comparative evidence suggests that traits targeted by precopulatory selection often covary in expression with those targeted by postcopulatory selection when assessed across species, although the strength and direction of this association varies considerably among taxa. We tested for correlated evolution between targets of pre‐ and postcopulatory selection using data on sexual size dimorphism (SSD) and testis size from 151 species of squamate reptiles (120 lizards, 31 snakes). In squamates, male–male competition for mating opportunities often favors large body size, such that the degree of male‐biased SSD is associated with the intensity of precopulatory selection. Likewise, competition for fertilization often favors increased sperm production, such that testis size (relative to body size) is associated with the intensity of postcopulatory selection. Using both conventional and phylogenetically based analyses, we show that testis size consistently decreases as the degree of male‐biased SSD increases across lizards and snakes. This evolutionary pattern suggests that strong precopulatory selection may often constrain the opportunity for postcopulatory selection and that the relative importance of each selective episode may determine the optimal resolution of energy allocation trade‐offs between traits subject to each form of sexual selection.

Evolutionary Endocrinology: Hormones as Mediators of Evolutionary Phenomena.

Hormones are agents of biological coordination that circulate systemically to signal diverse cells and tissues, thereby influencing nearly all aspects of the phenotype, including behavior, morphology, physiology, and life history. Hormonal phenotypes can be both heritable and subject to natural selection (Bonier et al. 2009; McGlothlin et al. 2010; Ouyang et al. 2011; Pavitt et al. 2014; Cox et al. 2016, this issue), yet hormones and endocrine pathways have rarely been integrated into evolutionary models and analyses. As Garland et al. (2016, this issue) note this issue, ‘‘the seminal papers in modern evolutionary physiology scarcely mentioned the endocrine system.’’ Nevertheless, over the past two decades, the field of evolutionary endocrinology (Zera et al. 2007; Nepomnaschy et al. 2009) has emerged not only as a means of understanding the evolution of the endocrine system itself (Denver et al. 2009), but also as a framework for exploring the roles of hormones in shaping other evolutionary phenomena (Ketterson and Nolan 1999; Adkins-Regan 2008; Husak et al. 2009; Williams 2012). Originally centered on classic quantitative genetic approaches to the study of hormonal phenotypes themselves (Zera and Zhang 1995; Zera and Huang 1999), this field has expanded to include new ideas about the diverse roles of hormones as mediators of a variety of fundamental evolutionary phenomena. This theme of ‘‘hormones as mediators of evolutionary phenomena’’ serves as the organizing concept for this issue and can be illustrated by several examples drawn from the papers that follow. Hormones as mediators of phenotypic and genetic integration