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The size-complexity hypothesis is a leading explanation for the evolution of complex life on earth. It predicts that in lineages that have undergone a major transition in organismality, larger numbers of lower-level subunits select for increased division of labour. Current data from multicellular organisms and social insects support a positive correlation between the number of cells and number of cell types and between colony size and the number of castes. However, the implication of these results is unclear, because colony size and number of cells are correlated with other variables which may also influence selection for division of labour, and causality could be in either direction. Here, to resolve this problem, we tested multiple causal hypotheses using data from 794 ant species. We found that larger colony sizes favoured the evolution of increased division of labour, resulting in more worker castes and greater variation in worker size. By contrast, our results did not provide consistent support for alternative hypotheses regarding either queen mating frequency or number of queens per colony explaining variation in division of labour. Overall, our results provide strong support for the size-complexity hypothesis., (© 2024. The Author(s).)

Group-living species show a diversity of social organization, from simple mated pairs to complex communities of interdependent individuals performing specialized tasks. The advantages of living in cooperative groups are well understood, but why some species breed in small aggregations while others evolve large, complex groups with clearly divided roles is unclear. We address this problem by reconstructing the evolutionary pathways to cooperative breeding across 4,730 bird species. We show that differences in the way groups form at the origin of cooperative breeding predicts the level of group complexity that emerges. Groups that originate through the retention of offspring have a clear reproductive divide with distinct breeder and helper roles. This is associated with reproductive specialization, where breeders invest more in fecundity and less in care. In contrast, groups formed through the aggregation of unrelated adults are smaller and lack specialization. These results help explain why some species have not transitioned beyond simple groups while others have taken the pathway to increased group complexity.

Animals living in harsh environments, where temperatures are hot and rainfall is unpredictable, are more likely to breed in cooperative groups. As a result, harsh environmental conditions have been accepted as a key factor explaining the evolution of cooperation. However, this is based on evidence that has not investigated the order of evolutionary events, so the inferred causality could be incorrect. We resolved this problem using phylogenetic analyses of 4,707 bird species and found that causation was in the opposite direction to that previously assumed. Rather than harsh environments favouring cooperation, cooperative breeding has facilitated the colonization of harsh environments. Cooperative breeding was, in fact, more likely to evolve from ancestors occupying relatively cool environmental niches with predictable rainfall, which had low levels of polyandry and hence high within-group relatedness. We also found that polyandry increased after cooperative breeders invaded harsh environments, suggesting that when helpers have limited options to breed independently, polyandry no longer destabilizes cooperation. This provides an explanation for the puzzling cases of polyandrous cooperative breeding birds. More generally, this illustrates how cooperation can play a key role in invading ecological niches, a pattern observed across all levels of biological organization from cells to animal societies.