Predicting multifarious behavioural divergence in the wild

Abstract

Many animals show complex behaviours that can have important ecological and evolutionary consequences. Environmental variation can lead to divergent selection that consistently favours particular behaviours in different environments; but how predictably multiple aspects of animal behaviour diverge in response to different environmental conditions remains unclear. We tested whether populations evolving under different levels of predation risk show predictable and repeatable population-level behavioural differences in all five primary components of animal personality: aggression, sociability, boldness, activity and exploration. We formulated and tested a priori predictions of divergence for each behaviour using the adaptive radiation of Bahamas mosquitofish, Gambusia hubbsi (family Poeciliidae), inhabiting vertical water-filled caves (blue holes) where they have evolved for thousands of years in either the presence or absence of predatory fish. Mosquitofish behaviours differed consistently, and largely predictably, between predation regimes: low-predation mosquitofish showed reduced sociability and greater exploration of a novel environment compared to high-predation counterparts. However, some differences were sex dependent: only females showed greater boldness and only males displayed reduced aggressiveness in low-predation populations. Activity levels did not differ between predation regimes. All populations showed a behavioural syndrome characteristic of either proactive or reactive stress-coping styles with regard to exploration. Exploration behavioural syndromes were more similar among populations that evolved in similar predation regimes, regardless of genetic relatedness. Using laboratory-born, high-predation mosquitofish, we confirmed that exploratory behaviours have a genetic basis and show significant within-individual repeatability. Our results suggest that environmental variation, such as chronic predation risk, can lead to repeatable, and often predictable, changes in multifarious animal behaviours, and that various aspects of behaviour can diversify more or less independently of one another. Considering the ecological importance of these behaviours, the ability to forecast behavioural shifts in a rapidly changing world could serve as a valuable conservation tool.