Trait evolution under multiple selection pressures: Prey responses to predictable and unpredictable variation

Abstract

AbstractWhen a strong selection pressure, such as predation risk, varies widely in space and time, how should prey respond? When risk varies predictably, prey are hypothesized to respond in a risk-sensitive manner. It is less clear how prey should respond when risk varies unpredictably.Additionally, prey response may also depend on how predation risk interacts with other selection pressures. Our understanding of the complex action of multiple and variable selection pressures on prey traits is still comparatively poor. Here, we examine how predictable and unpredictable aspects of predation risk act together with another important selection pressure to influence prey behaviour in the rock pool breeding mosquito,Aedes vexans.Through the selection of sites for oviposition, female mosquitoes can influence the predation risk faced by their offspring. We tested how females select oviposition sites, when encountering pools that vary in larval predation risk and desiccation risk. We comprehensively quantified spatial and temporal variation in predation risk by measuring densities of predatory dragonfly nymphs in rock pools of different sizes, along the mosquito breeding season. We also measured hydroperiod length. We next conducted manipulative experiments in rock pools and measured female oviposition responses to variation in predation and desiccation risks. Predation risk varied widely in space and time. Desiccation risk only appeared important for the small pools. Ovipositing females appeared to respond to these multiple aspects of variation in selection pressures. Females seemed to respond to predictable variation by avoiding large pools that permanently harboured predators in natural settings. Female responses were more variable to medium-sized pools with naturally stochastic predator densities, highlighting the role of unpredictability in predation risk in shaping behaviour. Females did not clearly prefer small pools that were naturally devoid of predators but carried high desiccation risk, suggesting that they balance multiple risks – predation versus desiccation – when choosing oviposition sites. Our study suggests that wild populations may commonly experience multiple and variable selection pressures that can favour seemingly puzzling trait variation. We highlight the need to quantify variation in selection pressures and investigate how such variation, especially the unpredictable aspects, shapes prey traits.