Sociality sculpts similar patterns of molecular evolution in two independently evolved lineages of eusocial bees

Abstract

While it is well known that the genome can affect social behavior, recent models posit that social lifestyles can, in turn, influence genome evolution. Here, we perform the most phylogenetically comprehensive comparative analysis of 16 bee genomes to date: incorporating two published and four new carpenter bee genomes (Apidae: Xylocopinae) for a first-ever genomic comparison with a monophyletic clade containing solitary through advanced eusocial taxa. We find that eusocial lineages have undergone more gene family expansions, feature more signatures of positive selection, and have higher counts of taxonomically restricted genes than solitary and weakly social lineages. Transcriptomic data reveal that caste-affiliated genes are deeply-conserved; gene regulatory and functional elements are more closely tied to social phenotype than phylogenetic lineage; and regulatory complexity increases steadily with social complexity. Overall, our study provides robust empirical evidence that social evolution can act as a major and surprisingly consistent driver of macroevolutionary genomic change.

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

“…Our dataset afforded a first test of this idea in the wasps. We were surprised to find that the highest rates of gene evolution were detected in the wasp species with the simpler societies rather than the more complex societies; these results are in stark contrast with the findings of a recent study on a range of social complexity in bees 8 where (in keeping with previous studies), rapid gene evolution was most apparent among species with the most complex societies. There are several interpretations of these contrasting results.…”

“…Taken together, these results provide evidence that the molecular processes regulating caste differentiation vary depending on the level of social complexity. The finding of more rapid rates of protein evolution in the simpler societies (Supplementary Figure 3c) was unexpected since studies of gene evolution in social bees have found the higher rates of evolution in the more complex societies 8 .…”

“…There may be fundamental differences discriminating (near) superorganismal societies from non-superorganismal societies 54 . This highlights the importance of examining different stages in the major transition when attempting to elucidate its patterns and processes 8,10,33 .…”

“…Phenotypic innovations across the animal kingdom have been linked to genomic evolution: taxonomicallyrestricted genes [13][14][15][16] , rapid evolution of proteins 17,18 and regulatory elements 17,19 been found in most lineages of social insects 20 . Indeed, some recent studies have suggested that the processes regulating different levels of social complexity may be different 8,17,19,21 . The innovations in social complexity and the shift in the unit of selection (from individual-to group-level 22 ) that occur in a major transition may therefore be accompanied by shifts in genomic processes and evolution, throwing into question whether the concept of a universal conserved genomic toolkit that regulates social behaviours across the spectrum of the major transition may be too simplistic 23 .…”

“…Polistes wasps 7,[25][26][27] and incipiently social bees [28][29][30][31] ), the latter of which likely represent the first stages in the major transition. Recent studies have identified core gene sets underlying caste-differentiated brain gene expression across a range of ants 5 and bees 8 ; ants lack ancestrally non-superorganismal representatives and so may not be informative for studying simpler societies and, putatively, the process of social evolution 32 . Analyses of molecular evolution across two independently evolved lineages of sociality in bees showed increased levels of regulatory complexity with social complexity.…”