Predation risk and the evolution of a vertebrate stress response: Parallel evolution of stress reactivity and sexual dimorphism.

Predation risk is often invoked to explain variation in stress responses. Yet, the answers to several key questions remain elusive, including the following: (1) how predation risk influences the evolution of stress phenotypes, (2) the relative importance of environmental versus genetic factors in stress reactivity and (3) sexual dimorphism in stress physiology. To address these questions, we explored variation in stress reactivity (ventilation frequency) in a post-Pleistocene radiation of live-bearing fish, where Bahamas mosquitofish (Gambusia hubbsi) inhabit isolated blue holes that differ in predation risk. Individuals of populations coexisting with predators exhibited similar, relatively low stress reactivity as compared to low-predation populations. We suggest that this dampened stress reactivity has evolved to reduce energy expenditure in environments with frequent and intense stressors, such as piscivorous fish. Importantly, the magnitude of stress responses exhibited by fish from high-predation sites in the wild changed very little after two generations of laboratory rearing in the absence of predators. By comparison, low-predation populations exhibited greater among-population variation and larger changes subsequent to laboratory rearing. These low-predation populations appear to have evolved more dampened stress responses in blue holes with lower food availability. Moreover, females showed a lower ventilation frequency, and this sexual dimorphism was stronger in high-predation populations. This may reflect a greater premium placed on energy efficiency in live-bearing females, especially under high-predation risk where females show higher fecundities. Altogether, by demonstrating parallel adaptive divergence in stress reactivity, we highlight how energetic trade-offs may mould the evolution of the vertebrate stress response under varying predation risk and resource availability.

Predictability and Parallelism of Multitrait Adaptation.

Environments shape the traits of organisms. Environmental variation may rarely alter selection on only a few traits, but instead precipitate wholesale changes of the multidimensional selective regime-many traits might experience divergent selection across divergent environments. Such changes in selection can elicit multifarious evolution. How predictable (from theory) and how parallel (consistent occurrences) is multitrait divergence across replicated environments? Here, I address this question using the post-Pleistocene radiation of Bahamas mosquitofish (Gambusia hubbsi) inhabiting blue holes on Andros Island. These fish independently colonized numerous blue holes, some that harbor a major fish predator (bigmouth sleeper, Gobiomorus dormitor) and some that lack any major predators. I used 5 approaches to quantitatively explore the predictability and parallelism of multitrait divergence between predation regimes in Bahamas mosquitofish. Synthesizing data for 90 traits from 13 different types of character suites (e.g., body morphology, life history, genital morphology, coloration, mating preference, habitat use), I found widespread evidence for strong, predictable, and parallel divergence between predation regimes. Yet despite the great majority of traits showing predictable trajectories of change, and the majority of traits showing significant parallelism and strong magnitudes of predictable divergence, I uncovered that over half of the overall phenotypic variation among populations was not driven by variation in predation regime. Results suggest that focusing on few traits, or focusing on parallel aspects of divergence, can provide a misleading picture of adaptation, and nonparallel divergence appears widespread and warrants greater attention. Taking a multitrait perspective, and quantifying predictability and parallelism, can yield important insights.

Rapid human-induced divergence of life-history strategies in Bahamian livebearing fishes (family Poeciliidae).

Human-induced rapid environmental change (HIREC) can have dramatic impacts on ecosystems, leading to rapid trait changes in some organisms and extinction in others. Such changes in traits signify that human actions can lead to cases of increased phenotypic diversity and consequently can strongly impact population-, community- and ecosystem-level dynamics. Here, we examine whether the ecological consequences of habitat fragmentation have led to changes in the life histories of three native species of mosquitofish (Gambusia spp.) inhabiting tidal creeks on six different Bahamian islands. We address two important questions: (i) How predictable and parallel are life-history changes in response to HIREC across islands and species, and (ii) what is the relative importance of shared (i.e. parallel) responses to fragmentation, differences between species or islands and species- or island-specific responses to fragmentation? Phenotypic differences between fragmentation regimes were as great or greater than differences between species or islands. While some adult life histories (lean weight and fat content) showed strong, shared responses to fragmentation, offspring-related life histories (embryo fat and fecundity) exhibited idiosyncratic, island-specific responses. While shared responses to fragmentation appeared largely driven by a reduction in piscivorous fish density, increased conspecific density and changes in salinity, we found some evidence that among-population variation in male reproductive investment and embryo fat content may have arisen via variation in conspecific density. Our results suggest that phenotypic responses to HIREC can be complex, with the predictability of response varying across traits. We therefore emphasize the need for more theoretical and empirical work to better understand the predictability of phenotypic responses to human-induced disturbances.