A single-cell transcriptomic atlas of paper wasp brains highlights Kenyon cells' role in social behavior

Abstract

Social insects provide unique opportunities for studying social interactions, but the cellular and molecular mechanisms underlying these behaviors are poorly understood. Here, we performed single-cell sequencing to profile the transcriptomes of 96,310 cells across four phenotypes of Polistes fuscatus paper wasps: foundresses, workers, gynes, and males, to determine how social states and social interactions are encoded in the physiology of the central brain. We characterized the cellular diversity of the Polistes brain and demonstrate that a substantial portion of the brain is composed of diverse populations of Kenyon cell neurons. The composition and gene-expression profiles of these Kenyon cells, as well other neural and non-neural cell populations, vary across sex, caste, and season. We also demonstrate that social interactions, and even the mere observation of a social interaction, induce significant transcriptomic responses, including signatures of neural activation, across populations of Kenyon cell neurons. Notably, the transcriptional and activational signatures elicited by observing a social interaction frequently overlapped with those induced by direct social interaction, suggesting that a shared neural program underlies both direct social interactions and social observation.