Discrete but variable structure of animal societies leads to the false perception of a social continuum.

Dustin R Rubenstein,Eileen A Lacey,Carlos A Botero

doi:10.1098/rsos.160147

Abstract

Animal societies are typically divided into those in which reproduction within a group is monopolized by a single female versus those in which it is shared among multiple females. It remains controversial, however, whether these two forms of social structure represent distinct evolutionary outcomes or endpoints along a continuum of reproductive options. To address this issue and to determine whether vertebrates and insects exhibit the same patterns of variation in social structure, we examined the demographic and reproductive structures of 293 species of wasps, ants, birds and mammals. Using phylogenetically informed comparative analyses, we found strong evidence indicating that not all reproductive arrangements within social groups are viable in nature and that in societies with multiple reproductives, selection favours instead taxon-specific patterns of decrease in the proportion of breeders as a function of group size. These outcomes suggest that the selective routes to sociality differ depending upon whether monopolization of reproduction by one individual is possible and that variation within and among taxonomic groups may lead to the false perception of a continuum of social structures. Thus, the occurrence of very large societies may require either complete reproductive monopolization (monogyny/singular breeding) or the maintenance of a taxon-specific range of values for the proportional decrease in the number of breeders within a group (polygyny/plural breeding), both of which may reduce reproductive conflict among females.

Highlights

The fundamental link between kin selection and altruistic behaviour is well established [22], the importance of lifetime monogamy is less universally accepted [23]
Using the predominant pattern of reproductive behaviour observed in mature groups, we identified each species as (i) monogynous or singular breeding if they were characterized by a mean of one breeding female per group, or (ii) polygynous or plural breeding if they were characterized by a mean of more than one breeding female per group
The proportion of breeders in societies with more than one reproductive female appeared to be dependent upon the total number of females in the group; when societies with multiple breeding females from all taxa were pooled, we found that the proportion of breeders decreased significantly with the total number of females in the group (MCMCglmm with taxonomic class as a random variable: β = −0.36, 95% credible interval (CI) = −0.42 to −0.28, p Markov chain Monte Carlo (MCMC) < 0.001; figure 1)

Summary

Introduction

The fundamental link between kin selection and altruistic behaviour is well established [22], the importance of lifetime monogamy is less universally accepted [23]. Societies with one versus multiple breeding females have been described as distinct evolutionary outcomes that are shaped by different selective pressures [29], it has been suggested that the structure of animal societies represents a continuum that ranges from completely egalitarian to completely despotic reproduction [11]. Distinguishing between these competing perspectives—discrete outcomes versus continuous variation in social structure—is fundamental to understanding the evolution of reproductive altruism in animals. To control for shared evolutionary history, our analyses for each taxonomic group were phylogenetically informed using molecular trees compiled from the literature or assembled de novo for each lineage

Methods

Results

Conclusion