ABSTRACT
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 functions associated with social evolution are facilitated by lineage-specific function of microRNAs (miRNAs). Genome scans across 12 bee species 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 that exhibit varying types of sociality revealed a substantial proportion (20-35%) of detected miRNAs with lineage-specific expression in the brain, 24-72% of which did not have any known homologs in 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 the earlier hypothesis that many new miRNAs are quickly purged by selection due to slightly deleterious effects on mRNA targets, and suggest genome structure is not as influential in regulating bee miRNA evolution as has been shown for mammalian miRNAs.