Evolutionary forces on A-to-I RNA editing revealed by sequencing individual honeybee drones

Social insects exhibit extensive phenotypic diversities among the genetically similar individuals, suggesting a role for the epigenetic regulations beyond the genome level. Recent studies propose that the ADAR-mediated adenosine-to-inosine (A-to-I) RNA editing, an evolutionarily conserved mechanism, facilitates adaptive evolution by expanding proteomic diversities temporally and spatially. Here, we characterize the A-to-I RNA editome honeybees (Apis mellifera). We collected heads, thoraxes, and abdomens of four haploid drone individuals, and deep sequenced the genomes and transcriptomes. We systematically identified 464 A-to-I editing sites and found that editing events in honeybees, especially in heads, are positively selected. There are four recoding and one synonymous editing site highly conserved between honeybee, bumblebee, and Drosophila. We discovered a diverged auto-editing site in Adar mRNA in bees and flies, which might play an auto-regulatory role in the two clades. We also found a recoding site in honeybee gene tipE that was reported to be task-related in bumblebee. Besides, although only a few editing sites are conserved between bees and flies, the species-specific editing sites exhibit convergent adaptation. We also detected thousands of hyper-editing sites in the lowly expressed regions, which possibly represents the non-specific targeting by ADAR.