The Role of Individual Heterogeneity in Collective Animal Behaviour

Abstract

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...

Group-level patterns emerge from individual speed as revealed by an extremely social robotic fish

“…By testing all fish with a robot that used identical interaction rules and lacked any preferred movement speed and directionality, these results provide novel experimental evidence that suggests individual speed is a fundamental factor in the emergence of collective behavioural patterns, in line with existing theoretical and empirical work [4,8,12,13,23]. As individual differences in speed are associated with a broad range of phenotypic traits observed among grouping animals, this may also help provide a mechanistic explanation for the effect of phenotypic heterogeneity for group-level patterns [3], such as has been shown for size, hunger, and parasitism [24,25].…”

“…Indeed, both short-term changes and heterogeneity in speed have been linked to a range of group-level properties, such as group cohesion, structure, shape, coordination, and leadership by both theoretical analyses [8], simulations [1,4,9], and empirical work [6,[10][11][12][13][14]. Importantly, grouping individuals may differ in their preferred and optimal movement speeds yet must also coordinate and adjust their behaviour to successfully group together [3,15]. Such socially-induced changes in speed by individuals interacting with one another make it difficult to isolate the effects of individual speed for group-level properties.…”

Emergent behavioral organization in heterogeneous groups of a social insect

“…In turn, these patterns affect important processes such as collective decision-making (5), the transmission and evolution of disease (69, 70), and the evolution of cooperative behavior (71, 72). While different variants of threshold-based models have been employed to study several of these systems (73–76), we still lack a unified theoretical framework to understand the consequences of individual differences on collective dynamics (77). Thus, a comparative approach to the study of the basic organizing principles of heterogeneous systems across scales constitutes an important next step towards understanding the behavior of complex biological systems.…”

Collective decision making by rational agents with differing preferences

“…Conflicting preferences could also result from transient circumstances such as different hunger levels, creating 'leadership by need' [25]. Phenotypic and behavioural heterogeneity plays a important role in how social groups function [40], and the potential role of minority-preference groups as leaders adds another mechanism whereby individual-level variation can be translated into group-level behavioural differences.…”