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

Abstract

The ubiquity of consistent inter-individual differences in behavior (“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 behavior. 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 behavioral types in free-swimming stickleback (Gasterosteus aculeatus) shoals. We show that individual’s propensity to stay near 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, together 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-organizing 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 behavior 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 behavioral differentiation between individuals.We acknowledge financial support from the Biotechnology and Biological Sciences Research Council (Graduate Research Fellowship to J.W.J), the Association for the Study of Animal Behaviour (Research Grants to J.W.J and N.J.B), the Royal Society (Dorothy Hodgkin Fellowship to N.J.B), the National Science Foundation (PHY-0848755, IOS-1355061, EAGER-IOS- 1251585 to I.D.C), the Office of Naval Research (N00014-09-1-1074, N00014-14-1-0635 to I.D.C), the Army Research Office (W911NG-11-1-0385, W911NF-14-1-0431 to I.D.C), the Human Frontier Science Program (RGP0065/2012 to I.D.C), the Ministerium für Wissenschaft, Forschung und Kunst Baden- Württemberg (SI-BW to I.D.C), and the Max Planck Institute for Ornithology. Open Access funded by Biotechnology and Biological Sciences Research Counci