SummaryThe 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, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 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.

Social grouping is omnipresent in the animal kingdom. Considerable research has focused on understanding how animal groups form and function, including how collective behaviour emerges via self-organising mechanisms and how phenotypic variation drives the behaviour and functioning of animal groups. However, we still lack a mechanistic understanding of the role of phenotypic variation in collective animal behaviour. Here we present a common framework to quantify individual heterogeneity and synthesise the literature to systematically explain and predict its role in collective behaviour across species, contexts, and traits. We show that individual heterogeneity provides a key intermediary mechanism with broad consequences for sociality (e.g., group structure, functioning), ecology (e.g., response to environmental change), and evolution. We also outline a roadmap for future research. The Effects of Phenotypic Variation in Collective Animal Behaviour: A Rising Topic Social grouping (see Glossary) is ubiquitous across the animal kingdom, ranging from pairs of individuals to enormous aggregations and structured communities, and short-lived and unstable group membership to long-lasting and fixed group compositions. Animals time and coordinate their behaviour with others to gain potential benefits, including increased mating opportunities, improved foraging efficiency, lower predation risk, and reduced energetic costs [1,2]. These benefits are realised through individual-level behavioural processes that shape and are shaped by the social structure, leadership, movement dynamics, and collective performance of groups [2-4]. A key goal of collective behaviour research is therefore to understand and predict how collective patterns emerge from the behaviour and social interactions of individuals. Scientists have long focused on identifying universal mechanisms underlying collective behaviour. Through a combination of theoretical and experimental work it has become clear that many complex collective behavioural patterns can emerge via self-organising processes from individuals using simple interaction rules [3-5]. However, individuals in groups are not all equal, and the phenotypic variation that is selectively maintained in populations results in individual heterogeneity within and among groups. Considerable theoretical (Box 1) and empirical evidence, from a broad range of taxa, suggests that such heterogeneity plays a fundamental role in collective animal behaviour. For example, the synchronised movements and social structure of fish schools and bird flocks [6,7], the leadership and collective decision-making of whale pods and primate troops [8,9], the colony performance of social spiders and honey bees [10,11], and the among-group assortment of ungulates [12] are all mediated by within-group individual heterogeneity. While previous theoretical work discusses the important evolutionary implications of phenotypic variation among grouping animals [13], we still lack a unified mechanistic understanding of individual heterogenei...