Collective predator evasion: Putting the criticality hypothesis to the test

TL;DR

This study tests the criticality hypothesis in animal groups using a spatial model, finding that criticality enhances school structure but is not an evolutionarily stable state due to spatial self-sorting effects.

Contribution

It provides the first spatially-explicit model analysis showing criticality's effects on prey schools and challenges the idea that self-organization towards criticality is driven by evolution.

Findings

Schools at criticality have optimal spatial structure.

Criticality is not evolutionarily stable due to spatial self-sorting.

Spatial phenomena are crucial in understanding collective behavior.

Abstract

According to the criticality hypothesis, collective biological systems should operate in a special parameter region, close to so-called critical points, where the collective behavior undergoes a qualitative change between different dynamical regimes. Critical systems exhibit unique properties, which may benefit collective information processing such as maximal responsiveness to external stimuli. Besides neuronal and gene-regulatory networks, recent empirical data suggests that also animal collectives may be examples of self-organized critical systems. However, open questions about self-organization mechanisms in animal groups remain: Evolutionary adaptation towards a group-level optimum (group-level selection), implicitly assumed in the "criticality hypothesis", appears in general not reasonable for fission-fusion groups composed of non-related individuals. Furthermore, previous theoretical work relies on non-spatial models, which ignore potentially important self-organization and spatial sorting effects. Using a generic, spatially-explicit model of schooling prey being attacked by a predator, we show first that schools operating at criticality perform best. However, this is not due to optimal response of the prey to the predator, as suggested by the "criticality hypothesis", but rather due to the spatial structure of the prey school at criticality. Secondly, by investigating individual-level evolution, we show that strong spatial self-sorting effects at the critical point lead to strong selection gradients, and make it an evolutionary unstable state. Our results demonstrate the decisive role of spatio-temporal phenomena in collective behavior, and that individual-level selection is in general not a viable mechanism for self-tuning of unrelated animal groups towards criticality.