Predation and Resource Availability Interact to Drive Life-History Evolution in an Adaptive Radiation of Livebearing Fish

Abstract

Predation risk and resource availability are two primary factors predicted by theory to drive the evolution of life histories. Yet, disentangling their roles in life-history evolution in the wild is challenging because (1) the two factors often co-vary across environments, and (2) environmental effects on phenotypes can mask patterns of genotypic evolution. Here, we use the model system of the post-Pleistocene radiation of Bahamas mosquitofish (Gambusia hubbsi) inhabiting blue holes to provide a strong test of the roles of predation and resources in life-history evolution, as the two factors do not co-vary in this system and we attempted to minimize environmental effects by raising eight populations under common laboratory conditions. We tested a priori predictions of predation- and resource-driven evolution in five life-history traits. We found that life-history evolution in Bahamas mosquitofish largely reflected complex interactions in the effects of predation and resource availability. High predation risk has driven the evolution of higher fecundity, smaller offspring size, more frequent reproduction, and slower growth rate—but this predation-driven divergence primarily occurred in environments with relatively high resource availability, and the effects of resources on life-history evolution was generally greater within environments having high predation risk. This implies that resource-driven selection on life histories overrides selection from predators when resources are particularly scarce. While several results matched a priori predictions, with the added nuance of interdependence among selective agents, some did not. For instance, only resource levels, not predation risk, explained evolutionary change in male age at maturity, with more rapid sexual maturation in higher-resource environments. We also found faster (not slower) juvenile growth rates within low-resource and low-predation environments, probably caused by selection in these high-competition scenarios favoring greater growth efficiency. Our approach, using common-garden experiments with a natural system of low- and high-predation populations that span a continuum of resource availability, provides a powerful way to deepen our understanding of life-history evolution. Overall, it appears that life-history evolution in this adaptive radiation has resulted from a complex interplay between predation and resources, underscoring the need for increased attention on more sophisticated interactions among selective agents in driving phenotypic diversification.

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

“…Avoiding wasteful energy expenditure may be even more important in high-predation localities, where fecundity is higher (Hulthén et al, 2021;Riesch et al, 2013) and energy-demanding rapid locomotor performance is critical for surviving predatory threats (Langerhans, 2009). Similar patterns were recently described in the foraging behaviour of mosquitofish, with stronger divergence between predation regimes in females than males (Pärssinen et al, 2021).…”

“…Whereas prior work has shown temporal repeatability in primary productivity and resource availability in the Bahamian blue holes (e.g. Hulthén et al, 2021), these factors do show some variation over time, and food quality and quantity surely differed between the wild and the laboratory, suggesting that resource-related factors may partially explain these findings. One potential phenomenon that could be involved is counter-gradient variation, and future studies could directly examine this hypothesis.…”

“…Despite varying resource availability (e.g. food and nutrients), there is a lack of covariation between known environmental parameters and the presence or absence of the predatory bigmouth sleeper (Björnerås et al, 2020;Hulthén et al, 2021). After collection, each experimental subject was immediately transferred to a transparent plastic cube (5 × 5 × 5 cm; approximately 1.5-2.0 × fish body length) filled to a depth of 2 cm with water from the same blue hole as the focal fish was captured from (cubes were always rinsed and fresh blue hole water added between trials).…”

“…ms) consistently varies among blue holes (e.g. Hulthén et al, 2021;Sha et al, 2020) and has led to population variation in male coloration (Martin et al, 2014) and evolutionary divergence in some life-history traits, such as juvenile growth rate (Hulthén et al, 2021). Zooplankton density was estimated using a 60-m tow of a zooplankton net (20-cm diameter, 153μm mesh) at 0.5-m depth within habitat where Bahamas mosquitofish were abundant within all sites .…”

“…Here, we hypothesized that efficient energy utilization would be more important to females than to males, as female Bahamas mosquitofish bear live young and allocate more time towards foraging , and, hence, efficient energy utilization would be more important to females than to males. We predicted (3) a lower overall ventilation frequency and a lower stress reactivity in females compared with males, and, in addition, that sex differences should be larger in fish from high-predation populations with females in these environments showing the smallest stress reactivity given the increased fecundity females have evolved in highpredation populations (Hulthén et al, 2021;Riesch et al, 2013Riesch et al, , 2020.…”