Social complexity, life-history and lineage influence the molecular basis of caste in a major transition in evolution

Abstract Major evolutionary transitions describe how biological complexity arises; e.g. in the evolution of complex multicellular bodies, and superorganismal insect societies. Such transitions involve the evolution of division of labour, e.g. as queen and worker castes in insect societies. A key mechanistic hypothesis for the evolution of division of labour is that a shared set of genes co-opted from a common solitary ancestral ground plan - a so-called genetic toolkit for sociality - regulate insect castes across different levels of social complexity. The vespid wasps represent an excellent system in which to test this. Here, using conventional and machine learning analyses of brain transcriptome data from nine species of vespid wasps, we find evidence of a shared genetic toolkit across species representing different levels of social complexity, with a large suite of genes classifying castes correctly across species. However, we also found evidence of additional fine-scale differences in predictive gene sets, functional enrichment and rates of gene evolution that were related to level of social complexity, but also life-history traits (e.g. mode of colony founding). Thus, there appear to be shifts in the gene networks regulating social behaviour and rates of gene evolution that are influenced by innovations in both social complexity and life-history. These results suggest that the concept of a shared genetic toolkit for sociality may be too simplistic to fully describe the process of the major transition to sociality, even within a single lineage. Diversity in lineage, social complexity and life-history traits must be taken into account in the quest to uncover the molecular bases of the major transition to sociality.