Bumblebee colonies are characterized by profound phenotypic variability among genetically similar full-sister worker bees. We studied ADAR (Adenosine Deaminase Acting on RNA) mediated RNA editing, a posttranscriptional mechanisms that can increase phenotypic variation among genetically similar individuals in the bumblebee Bombus terrestris. We combined behavioral observations, RNA and DNA sequencing, RNA editing bioinformatics, and analyses of ADAR transcript abundance. We found that ADAR expression is enriched in the brain tissue that shows extensive RNA editing, with 1.15 million unique genomic sites. This high level of editing was unexpected given that the bumblebee genome encodes only a single ADAR enzyme. RNA editing sites were also found on 100 coding transcripts, some of which are conserved in other insects or even in cephalopods and mammals. Recoding was enriched for ion channels, transporters, and receptors that are predicted to affect brain function and behavior. This includes 14 editing sites, four of which conserved in other species, on the sequence of the Shab voltage gated potassium channel, and three on the ADAR sequence. One nonsynonymous auto-editing site on ADAR was positively correlated with editing level. Editing levels on protein coding and non-coding transcripts were influenced by task performance (brood care vs foraging), but not by dominance or juvenile hormone. Task-related RNA editing was not associated with variation in brain ADAR expression or level of auto-editing. Taken together our findings show that brain editing levels are high in naturally behaving bees that have only a single ADAR enzyme, and suggest that RNA editing can be regulated by relatively short-term effects associated with brood care or foraging activities.
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