The evolution of distributed sensing and collective computation in animal populations

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Abstract

Many animal groups exhibit rapid, coordinated collective motion. Yet, the evolutionary forces that cause such collective responses to evolve are poorly understood. Here we develop analytical methods and evolutionary simulations based on experimental data from schooling fish. We use these methods to investigate how populations evolve within unpredictable, time-varying resource environments. We show that populations evolve toward a distinctive regime in behavioral phenotype space, where small responses of individuals to local environmental cues cause spontaneous changes in the collective state of groups. These changes resemble phase transitions in physical systems. Through these transitions, individuals evolve the emergent capacity to sense and respond to resource gradients (i.e. individuals perceive gradients via social interactions, rather than sensing gradients directly), and to allocate themselves among distinct, distant resource patches. Our results yield new insight into how natural selection, acting on selfish individuals, results in the highly effective collective responses evident in nature.

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Andrew M Hein

Department of Ecology and Evolutionary Biology, Princeton University, Princeton, United States

For correspondence
ahein@princeton.edu

Competing interests
No competing interests declared.
Sara Brin Rosenthal

Department of Physics, Princeton University, Princeton, United States

Competing interests
No competing interests declared.
George I Hagstrom

Department of Ecology and Evolutionary Biology, Princeton University, Princeton, United States

Competing interests
No competing interests declared.
Andrew Berdahl

Santa Fe Institute, Santa Fe, United States

Competing interests
No competing interests declared.
Colin J Torney

Centre for Mathematics and the Environment, University of Exeter, Cornwall Campus, Penryn, United Kingdom

Competing interests
No competing interests declared.
Iain D Couzin

Department of Collective Behaviour, Max Planck Institute for Ornithology, Konstanz, Germany

Competing interests
Iain D Couzin, Reviewing editor, eLife.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.