Consistent individual differences drive collective behaviour and group functioning of schooling fish

Abstract

The ubiquity of consistent inter-individual differences in behaviour (‘animal personalities ’) [1, 2] suggests that they might play a fundamental role in driving the movements and functioning of animal groups [3, 4], including their collective decision-making, foraging performance, and predator avoidance. Despite increasing evidence that highlights their importance [5–16], we still lack a unified mechanistic framework to explain and to predict how consistent inter-individual differences may drive collective behaviour. Here we investigate how the structure, leadership, movement dynamics, and foraging performance of groups can emerge from inter-individual differences by high-resolution tracking of known behavioural types in free-swimming stickleback (Gasterosteus aculeatus) shoals. We show that individual’s propensity to stay close to others, measured by a classic ‘sociability’ assay, was negatively linked to swim speed across a range of contexts, and predicted spatial positioning and leadership within groups as well as differences in structure and movement dynamics between groups. In turn, this trait in combination with individual’s exploratory tendency, measured by a classic ‘boldness’ assay, explained individual and group foraging performance. These effects of consistent individual differences on group-level states emerged naturally from a generic model of self-organising groups composed of individuals differing in speed and goal-orientedness. Our study provides experimental and theoretical evidence for a simple mechanism to explain the emergence of collective behaviour from consistent individual differences, including variation in the structure, leadership, movement dynamics, and functional capabilities of groups, across social and ecological scales. In addition, we demonstrate individual performance is conditional on group composition, indicating how social selection may drive behavioural differentiation between individuals.