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

Abstract

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.

Compiling forty years of guppy research to investigate the factors contributing to (non)parallel evolution

“…Previous studies have shown that trait type, sex, and rearing environment can influence (non)parallelism (e.g., Hendry et al, 2006; Langerhans, 2018; Oke et al, 2016, 2017; Vinterstare et al, 2021). In the current study, only trait type had a significant influence on the extent of parallelism, and only when sex was included in the model.…”

“…Previous studies have shown that trait type, sex, and rearing environment can influence (non)parallelism (e.g., Hendry et al, 2006;Langerhans, 2018;Oke et al, 2016Oke et al, , 2017Vinterstare et al, 2021).…”

A test of sexual dimorphism in deactivating plant defense and attraction of conspecifics in the four-eyed red milkweed beetle (Tetraopes tetrophthalmus)

“…Sexual dimorphism is the variability in traits between males and females of a species, including body size, pheromone production, and feeding behavior (Mori et al 2017;Brzozowski et al 2020;Gontijo 2013). Dimorphism is common in herbivorous insects, and often re ects sex differences in mate attraction and tolerance of certain stresses, such as avoiding predation or harsh abiotic conditions (Vinterstare et al 2021;Gontijo 2013;Verrell et al 2001). Here, we focus on two prominent examples of dimorphic behaviors: the attraction of conspeci cs and deactivation of plant defense.…”