Size-selective mortality induces evolutionary changes in group risk-taking behavior and the circadian system in a fish

1. Intensive and trait-selective mortality of fish and wildlife can cause evolutionary changes in a range of life-history and behavioral traits. These changes might in turn alter the circadian system due to coevolutionary mechanisms or correlated selection responses both at behavioral and molecular levels, with knock-on effects on daily physiological processes and behavioral outputs. 2. We examined the evolutionary impact of size-selective harvesting on group risk-taking behavior and the circadian system in a model fish species. We exposed zebrafish (Danio rerio) to either large or small size-selective harvesting relative to a control over five generations, followed by eight generations during which harvesting halted to remove maternal effects. 3. Size-selective mortality affected fine-scale timing of behaviors. In particular, small size-selective mortality, typical of specialized fisheries and gape-limited predators targeting smaller size classes, increased group risk-taking behavior during feeding and after simulated predator attacks. Moreover, small size-selective mortality increased early peaks of daily activity as well as extended self-feeding daily activity to the photophase compared to controls. By contrast large size-selective mortality, typical of most wild capture fisheries, only showed an almost significant effect of decreasing group risk-taking behavior during the habituation phase and no clear changes in fine-scale timing of daily behavioral rhythms compared to controls. 4. We also found changes in the molecular circadian core clockwork in response to both size selective mortality treatments. These changes disappeared in the clock output pathway because both size-selected lines showed similar transcription profiles. This switch downstream to the molecular circadian core clockwork also resulted in similar overall behavioral rhythms (diurnal swimming and self-feeding in the last hours of darkness) independent of the underlying molecular clock. 5. To conclude, our experimental harvest left an asymmetrical evolutionary legacy in group risk-taking behavior and in fine-scale daily behavioral rhythms. Yet, the overall timing of activity showed evolutionary resistance probably maintained by a molecular switch. Our experimental findings suggest that size-selective mortality can have consequences for behavior and physiological processes.