Size-dependent harvest mortality indirectly affects boldness, feeding rate, and behaviour-linked gene expression in a decade-long selection experiment on guppies

Fisheries-induced mortality is size-selective, commonly targeting large individuals, which leads to evolution towards smaller size and early maturation. However, little is known on whether behaviour is affected. Here we aimed at testing whether size-dependent harvest indirectly affects behavioural traits that might have ecological consequences. Specifically, we assessed feeding rate - which affects prey abundance -, boldness - which determines a fish vulnerability to predators -, and sociability - which determines how a fish interacts with conspecifics and ultimately affects foraging and predation avoidance. In addition, we tested whether the differences in behaviour were associated to differences in selected key genes expression, to understand its molecular regulation. With a decade-long selection experiment on guppies Poecilia reticulata, we created populations with life histories adapted to positively size-dependent harvest, i.e., like that induced by fishing (fast life history). For comparison, we also created populations adapted to the opposite size-selection, and populations experiencing no size-selection. Fish exposed to positively size-dependent harvest were bolder, more likely to feed, were more social/aggressive, and expressed less brain avt (arginine vasotocin) relative to those exposed to negatively size-dependent harvest. In addition, higher expression of th and th2 (tyrosine hydroxylase 1 and 2), and neuroD2 (neuronal differentiation factor 2) were linked with bolder behaviour and higher feeding in normal (no-threat) conditions, while higher avt, th, and neuroD2 were associated with higher sociability/aggression after a threat. Fish exposed to positively size-dependent harvest presented behaviours linked to faster life histories as theoretically expected. Therefore, harvest selection does not only affect fish size and life history, but indirectly leads to boldness and higher feeding rates, which potentially results in higher vulnerability to predators and higher pressure on prey abundance, respectively. Our results suggest that size-dependent mortality have further consequences to the ecosystem, beyond the target species.