Social familiarity shapes collective decision-making in response to looming stimuli in Medaka fish

Abstract

Abstract Social familiarity within groups promotes behavioural synchrony and facilitates information transfer. Whether it shapes collective decision-making under predator threat is unknown. Here groups of six medaka ( Oryzias latipes ) familiarised for one month were used to test whether familiarisation promotes instantaneous collective decision-making in response to a looming stimulus (LS) mimicking a predator attack. First, we analysed behavioural transitions, defined as changes among three behavioural states: high-speed, normal and freezing-like before, during, and after LS in groups of six individuals. Individuals showing high-speed state in response to LS typically tended to shift to freezing-like state afterwards, whereas non-responders were more likely to maintain normal state. Group-level analysis revealed a bimodal distribution in the number of individuals exhibiting freezing-like state, with peaks at zero and six individuals, corresponding to ‘all non-freezing’ and ‘all-freezing’. Clustering analysis further identified three consistent group profiles: ‘freezing-dominant’, ‘non-freezing-dominant’, and ‘mixed-type’ based on behavioural tendencies across 10 trials. In contrast, in unfamiliar groups assembled immediately before testing, the ‘freezing-dominant’ profile was absent, and the distribution in the number of individuals exhibiting freezing-like state shifted to unimodal. In these groups, even at the individual level, responses more often showed a transition from high-speed state to normal state rather than freezing-like state. The results indicate that social familiarity promotes synchronous freezing-like state and consensus decisions under looming threat. Our study presents a behavioural assay for predator-evoked collective decision-making in a genetic model fish, providing a framework for future efforts to link behavioural ethology with neuroscience.