Ecological and social constraints combine to promote evolution of non-breeding strategies in clownfish

Rebecca Branconi,Maya Srinivasan,Robin K Francis,Geoffrey P Jones,Peter M Buston,Tina A Barbasch

doi:10.1038/s42003-020-01380-8

Abstract

Individuals that forgo their own reproduction in animal societies represent an evolutionary paradox because it is not immediately apparent how natural selection can preserve the genes that underlie non-breeding strategies. Cooperative breeding theory provides a solution to the paradox: non-breeders benefit by helping relatives and/or inheriting breeding positions; non-breeders do not disperse to breed elsewhere because of ecological constraints. However, the question of why non-breeders do not contest to breed within their group has rarely been addressed. Here, we use a wild population of clownfish (Amphiprion percula), where non-breeders wait peacefully for years to inherit breeding positions, to show non-breeders will disperse when ecological constraints (risk of mortality during dispersal) are experimentally weakened. In addition, we show non-breeders will contest when social constraints (risk of eviction during contest) are experimentally relaxed. Our results show it is the combination of ecological and social constraints that promote the evolution of non-breeding strategies. The findings highlight parallels between, and potential for fruitful exchange between, cooperative breeding theory and economic bargaining theory: individuals will forgo their own reproduction and wait peacefully to inherit breeding positions (engage in cooperative options) when there are harsh ecological constraints (poor outside options) and harsh social constraints (poor inside options).

Highlights

Individuals that forgo their own reproduction in animal societies represent an evolutionary paradox because it is not immediately apparent how natural selection can preserve the genes that underlie non-breeding strategies
Individuals will be more likely to forego their own reproduction and engage in cooperative behaviors, if there is high relatedness between group members[2,3] such that they can pass on their genes by helping their relatives in the present[4,5,6] and/or if there is a high probability of inheriting a breeding position[7,8] such that they will pass on their genes in the future[9,10,11]
There is a real need to broaden the diversity of social taxa and types of cooperative behaviors considered, so that we may better understand the drivers of social group formation across taxa and along the continuum from simple to complex eusocial systems[21,22]

Summary

Introduction

Individuals that forgo their own reproduction in animal societies represent an evolutionary paradox because it is not immediately apparent how natural selection can preserve the genes that underlie non-breeding strategies. Individuals will be more likely to forego their own reproduction and engage in cooperative behaviors, if there are strong ecological constraints[12,13] such that there are no opportunities for breeding outside of the group[14,15,16] and/or if there are strong social constraints such that there are no immediate opportunities for breeding inside the group[17,18,19] (i.e., the right hand side of the Hamilton’s inequality is low). Within the size hierarchy subordinates tend to be 80% of the size of their immediate dominants[41] This factor likely reduces the payoff associated with contesting for breeding positions, suggesting that social constraints play a key role in social group formation. The aim of this study is to investigate why clownfish nonbreeders engage in the cooperative option, waiting peacefully in social groups to inherit breeding positions, rather than engaging in one of two, alternative, non-cooperative options: (i) the outside option—leaving to breed elsewhere; and ii) the inside option— contesting to breed at home (Fig. 1)

Objectives

Methods

Results

Conclusion