Social modularity: conserved genes and regulatory elements underlie caste-antecedent behavioural states in an incipiently social bee

Abstract

The evolutionary origins of advanced eusociality, one of the most complex forms of phenotypic plasticity in nature, have long been a focus within the field of sociobiology. Although eusocial insects are known to have evolved from solitary ancestors, sociogenomic research among incipiently social taxa has only recently provided empirical evidence supporting theories that modular regulation and deeply conserved genes may play important roles in both the evolutionary emergence and elaboration of insect sociality. There remains, however, a paucity of data to further test the biological reality of these and other evolutionary theories among taxa in the earliest stages of social evolution. Here, we present brain transcriptomic data from the incipiently social small carpenter bee, Ceratina calcarata , which captures patterns of cis -regulation and gene expression associated with female maturation, and underlying two well-defined behavioural states, foraging and guarding, concurrently demonstrated by mothers and daughters during early autumn. We find that an incipiently social nest environment may dramatically affect gene expression. We further reveal foraging and guarding behaviours to be putatively caste-antecedent states in C. calcarata , and offer strong empirical support for the operation of modular regulation, involving deeply conserved and differentially expressed genes in the expression of early social forms.

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

“…gt , prd , and z ). Gt , prd , and z are functionally associated with neural development (including chemosensation) and epigenetic regulation of gene expression and have all been previously associated with guarding behavior in C. calcarata 34 . Non-foraging individuals often act as nest guards, either while waiting to supersede the nest, or to ensure the survival of their own brood 28 , 57 , 58 .…”

“…5). Further, six TFs from this set were previously associated with prereproductive foraging in C. calcarata 34 including Egr1, GATA3, NFYA, and Tal1_Gata1, associated with learning, memory, and immune function. Of particular note from this set is early growth response protein 1 (Egr1), previously found to have a widelyconserved role in socially responsive gene regulation 60 including a critical role in honey bee foraging 61 , and recently proposed as a candidate TF for tasks involving time-memory 62 .…”

“…17,23,[26][27][28] ). To date, published genomic and transcriptomic resources for the Xylocopinae have been limited but highly informative resources for comparative studies of early social evolution [29][30][31][32][33][34][35] . Here we present four newly sequenced xylocopine genomes and transcriptomes and combine these with published genomic and transcriptomic data from 12 additional bee species to address three main questions.…”

Functional genomics of parental care of insects

“…TRNs are a major target to evolve new phenotypes as they define the sets of genes expressed within a cell and therefore the identity and function of a cell (Simola et al, 2013;Halfon, 2017). Some work has detailed transcription factor networks of parental are and other behaviors in the honey bee (Chandrasekaran et al, 2011;Ament et al, 2012;Khamis et al, 2015;Hamilton et al, 2019) and carpenter bee (Shell and Rehan, 2019). That research has produced some interesting conclusions, such as, some transcription factors are shared across behaviors, relatively few transcription factors can regulate behavioral transitions, and that there seems to be a strong hierarchical nature to the TRNs in honey bee behavior (Chandrasekaran et al, 2011;Khamis et al, 2015;Hamilton et al, 2019).…”

Genetic toolkit for sociality predicts castes across the spectrum of social complexity in wasps

“…ants or honeybees 23 ), or the simplest levels of social complexity as non-superorganisms that likely represent the first stages in the major transition (e.g. Polistes wasps 7,[24][25][26] and incipiently social bees [27][28][29][30] ). We lack data on the intermediary stages of the major transition and thus lack a comprehensive analysis of if and how molecular mechanism change across any single evolutionary transition to superorganismality.…”