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.
Highlights
Predation is a major evolutionary force that has selected for a plethora of anti-predator adaptations in prey (Langerhans 2007; Vamosi 2005)
This analysis revealed that fish from high-predation populations tended to show a dampened stress reactivity (Predation Regime × Time interaction; Table 1; Figure 2), in line with our first prediction
Whereas this analysis did not identify any strong evidence that the stress response differed between the wild and the laboratory within either predation regime (i.e. Predation regime (PR) × ENV × Time interaction), consistent with our second prediction, inspection of the time-course stress reactivity curves (Figure 2) suggested that some variation may have occurred: (1) in the laboratory, females appeared to show little difference between predation regimes in their average time-course curves even though they exhibited strong differences in the wild (Figure 2a) and (2) males in low-predation populations seemed to show differences between the wild and laboratory, resulting in a shift of the time-points in which the greatest differences between predation regimes occurred
Summary
Predation is a major evolutionary force that has selected for a plethora of anti-predator adaptations in prey (Langerhans 2007; Vamosi 2005). The vertebrate stress response involves a complex endocrinological pathway that leads to enhanced glucocorticoid secretion, followed by increased blood glucose levels, as well as enhanced cardiovascular activity and ventilation rate, i.e. the necessities of the fight-or-flight response for predator evasion (Clinchy et al, 2013; Hawlena & Schmitz, 2010; Sapolsky, 1990; Sapolsky et al, 2000). Predation as a driver of stress response differentiation is a topic that has garnered considerable attention, but comparatively few studies have focused on the role of local variation in selection regimes for intraspecific divergence by examining both phenotypic (wild-caught) and genetic (laboratory-reared) patterns, or investigated potential sex differences in this context, even though this could prove important
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