The Right Tools for the Job: Cooperative Breeding Theory and an Evaluation of the Methodological Approaches to Understanding the Evolution and Maintenance of Sociality

Abstract

Why do we observe so many examples in nature in which individuals routinely delay or completely forgo their own reproductive opportunities in order to join and remain within a group? Cooperative breeding theory provides a rich framework with which to study the factors that may influence the costs and benefits of remaining philopatric as a non-breeder. This is often viewed as an initial step in the development of costly helping behavior provided by non-breeding subordinates. Despite many excellent empirical studies testing key concepts of the theory, there is still debate regarding the relative importance of various evolutionary forces, suggesting that there may not be a general explanation but rather a dynamic and taxonomically varied combination of factors influencing the evolution and maintenance of sociality. Here, we explore two potential improvements in the study of sociality that could aid in the progress of this field. The first addresses the fact that empirical studies of social evolution are typically conducted using either comparative, observational or manipulative methodologies. Instead, we suggest a holistic approach, whereby observational and experimental studies are designed with the explicit view of advancing comparative analyses of sociality for the taxon, and in tandem, where comparative work informs targeted research effort on specific (usually understudied) species within the lineage. A second improvement relates to the broadening of tests of cooperative breeding theory to include taxa where subordinates do not necessarily provide active cooperation within the group. The original bias toward "helpful subordinates" arose from a focus on terrestrial taxa. However, recent consideration of other taxa, especially marine taxa, is slowly revealing that the theory can and should encompass a continuum of cooperative social systems, including those Hing et al.Methodological Approaches to Study Sociality where subordinates do not actively help. This review summarizes the major hypotheses of cooperative breeding theory, one of the dominant frameworks to examine social evolution, and highlights the potential benefits that a combined methodological approach and a broader application could provide to the study of sociality.

Repeated cyclone events reveal potential causes of sociality in coral-dwelling Gobiodon fishes

“…Of the marine taxa tested so far, habitat-specialist coral-reef fishes are emerging as a useful model species to study theories of social evolution and maintenance [20, 27, 28] and have shown similar responses to habitat manipulation as terrestrial species (e.g. [23]).…”

“…These two hypotheses are often viewed as two sides of the same coin as they both look at aspects of ecology to explain social evolution and maintenance [ 20 ]. The benefits of philopatry hypothesis focuses on the benefits conferred from residing in a high-quality habitat (e.g.…”

“…While these hypotheses have been well studied in terrestrial organisms, they have only recently been tested in marine environments [ 20 , 26 – 28 ]. Of the marine taxa tested so far, habitat-specialist coral-reef fishes are emerging as a useful model species to study theories of social evolution and maintenance [ 20 , 27 , 28 ] and have shown similar responses to habitat manipulation as terrestrial species (e.g. [ 23 ]).…”

“…Many social fishes have a pelagic larval phase which suggests low levels of kinship within groups, reducing the potential confounding factor of relatedness (e.g. [ 20 , 29 , 30 ] but see [ 31 ]). Given the apparent influence of ecological factors on the formation and maintenance of social groups, we would expect that disturbances capable of altering a species’ habitat, such as severe weather events, would have a strong impact on social organization [ 23 , 32 ].…”

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

“…While there is extensive observational and experimental evidence demonstrating that high relatedness, future benefits and ecological constraints help explaining non-breeding behaviors in animal societies, relatively limited work has been done to investigate the roles of social constraints 20 . Furthermore, 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 .

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