Central administration of oxytocin increases social interaction and shoaling behaviour in guppies

The nonapeptides vasotocin, oxytocin and their homologues regulate a wide range of social behaviours such as mating, aggression, social recognition and parental care across vertebrates. These varied influences across diverse taxa suggest a highly-conserved, ancestral role for nonapeptides in animal social behaviour. Here, we address the role of nonapeptides in a foundational social behaviour, the tendency of individuals to group with conspecifics. We investigated the effects of administration of nonapeptides on shoaling behaviour in the guppy (Poecilia reticulata), a small freshwater fish that is a model system for studying the evolution of social behaviour in the wild. We conducted two experiments using intracerebroventricular administration in wild-origin guppies to investigate the effects of nonapeptides and their antagonists on grouping behaviour, focusing first on oxytocin, and then on vasotocin. We monitored shoaling behaviour for 2.5 h after each administration and found that after 90 min, oxytocin significantly increased social interaction, with a similar effect on shoaling behaviour. Vasotocin did not produce significant changes in social interaction or shoaling preferences, and putative receptor antagonists for oxytocin and vasotocin did not have clear behavioural effects. These findings show that central administration of oxytocin increases shoaling tendencies in guppies, suggesting it influences this fundamental social behaviour. We also found that effects were time-dependent, highlighting the importance of studying the temporal dynamics of nonapeptide actions on behaviour. Our work also demonstrates the feasibility of intracerebroventricular injections for central pharmacological manipulations in small fish, opening new potential avenues for behavioural neuroscience in non-model species.