Brain microRNA expression associated with social evolution in bees

Evolutionary transitions to a social lifestyle in insects are associated with lineage-specific changes in gene expression, but the key nodes that drive these regulatory changes are largely unknown. We tested the hypothesis that changes in gene regulatory function associated with social evolution are facilitated by lineage-specific microRNA (miRNA) regulatory function. Genome scans across 12 bees showed that miRNA copy number is highly conserved and is not associated with variation in social organization. However, deep sequencing of small RNAs of six bee species revealed a substantial proportion (20-35%) of miRNAs are expressed in the brains of a single species, and many of these do not have identifiable homologs in any other species. Lineage-specific miRNAs disproportionately target lineage-specific genes, and have lower expression levels than more evolutionarily conserved miRNAs. Consistent with our hypothesis, the predicted targets of lineage-specific miRNAs are enriched for genes related to social behavior, such as caste-biased genes, in social species, but they are either not enriched for or significantly depleted of genes under positive selection. Together, these results suggest that novel miRNAs may contribute to lineage-specific patterns of molecular evolution associated with the origins and elaborations of eusociality. Our analyses also lend support to earlier hypotheses concerning miRNA origins from a relatively understudied taxonomic group, and reveal important differences in the evolution and assimilation of novel miRNAs between mammals and insects.