Evolution of non-kin cooperation: social assortment by cooperative phenotype in guppies.

Josefine Bohr Brask,Safi K Darden,Bronwyn H Bleakley,Robert J P Heathcote,Patrick B Hamilton,Torben Dabelsteen,Darren P Croft,Richard James,Charles R Tyler,Indar W Ramnarine,Mathew Edenbrow

doi:10.1098/rsos.181493

Abstract

Cooperation among non-kin constitutes a conundrum for evolutionary biology. Theory suggests that non-kin cooperation can evolve if individuals differ consistently in their cooperative phenotypes and assort socially by these, such that cooperative individuals interact predominantly with one another. However, our knowledge of the role of cooperative phenotypes in the social structuring of real-world animal populations is minimal. In this study, we investigated cooperative phenotypes and their link to social structure in wild Trinidadian guppies (Poecilia reticulata). We first investigated whether wild guppies are repeatable in their individual levels of cooperativeness (i.e. have cooperative phenotypes) and found evidence for this in seven out of eight populations, a result which was mostly driven by females. We then examined the social network structure of one of these populations where the expected fitness impact of cooperative contexts is relatively high, and found assortment by cooperativeness, but not by genetic relatedness. By contrast, and in accordance with our expectations, we did not find assortment by cooperativeness in a population where the expected fitness impact of cooperative contexts is lower. Our results provide empirical support for current theory and suggest that assortment by cooperativeness is important for the evolution and persistence of non-kin cooperation in real-world populations.

Highlights

Cooperation has for many years constituted a puzzle for evolutionary theory
Cooperativeness shown by individuals in trials with mirror-image partners was significantly correlated with their cooperativeness in live-partner trials, validating the use of mirror trials as a means to measure cooperativeness in guppies
The evolution and persistence of cooperation in structured populations has been investigated extensively with individual-based computer models that use a game-theoretic framework. This body of research demonstrates that certain social network topologies and dynamics can maintain cooperation, by giving rise to assortment of cooperative acts (e.g. [39,40,41,42,43,44,45])

Summary

Introduction

Cooperation has for many years constituted a puzzle for evolutionary theory. Cooperative behaviours, defined as acts that benefit a receiver with a net cost to the actor, are found in many taxa but seemingly contradict the central prediction in classic evolutionary theory that behaviours must be fitness-increasing for actors in order to be selected for and maintained. Numerous studies have demonstrated that animal social network structures are nonrandom, with significant within-population heterogeneity in social tie strengths documented across species [12]. These findings suggest that assortment of individuals in social space based on their cooperativeness could potentially be promoting cooperation among non-kin in many species. Direct empirical investigations of social assortment by cooperativeness in natural populations of animals are essential to understanding non-kin cooperation, but knowledge regarding the link between social structure and individual cooperativeness in animals is currently minimal

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Conclusion