Social insects such as ants, termites, wasps and bees, provide excellent model systems for studying how a single genome (set of genes) can generate substantial functional diversity. Individual social insects typically show remarkable plasticity, switching between behavioral and physiological states along with the social environment they experience, during development, or even as fully formed adult insects. In many species, considerable variation in behavioral and physiological state is not associated with genetic variation among individuals in the same colony. This study focuses on the "model" bumblebee Bombus terrestris in which worker bees show significant phenotypic variability (up to ten-fold difference in body mass!!) among genetically similar sisters, suggesting a major role for epigenetic processes.

The research team investigated RNA editing, an epigenetic process that modifies nucleotides in pre-mRNA sequences. They specifically focused on RNA editing, that is mediated by the ADAR (adenosine deaminase acting on RNA) enzymes, the most common type of RNA editing known in animals. By contrast to mammals that have three ADAR enzymes, insects seem to have only a single ADAR. The experimental approach combined extensive RNA and DNA sequencing, measuring ADAR transcript abundance, behavioral observations, and bioinformatics.

The team found a high level of ADAR-mediated RNA editing in the bumblebee, despite the lack of an ADAR1-homolog that accounts for most brain RNA editing in mammals. They identified 1.15 million unique genomic sites, and 164 recoding sites residing in 100 protein-coding genes. The edited proteins include ion channels, transporters, and receptors predicted to affect brain function and behavior. Some edited sites are similarly edited in other insects, cephalopods (i.e., octopuses and squids) and even mammals. Remarkably, the global editing level of protein coding and non-coding transcripts weakly correlates with the task the worker performs (brood care vs. foraging).

This study is the first to explore RNA editing in bees, and only the second in any social insect. It reveals an unexpectedly high brain editing levels in naturally behaving bees. Moreover, it suggests that ADAR mediated RNA editing may be regulated by relatively short-term effects associated with brood care or foraging activities. These putative short-term effects contrast with the common view that RNA editing is primarily important for longer term effects such as development and acclimation to a new environment. Thus, differential RNA editing may account for at least some of the remarkable phenotypic plasticity among individuals, even if they are very similar genetically, such as in some insect societies.

Read full paper in Nature Communications