Behavioral fingerprinting of the naked mole-rat uncovers signatures of eusociality and social touch

Abstract

SummaryThe East African naked mole-rat (Heterocephalus glaber) lives in large and extremely cooperative subterranean colonies. However, both the biology that drives their social interactions and the behaviors that define their social hierarchy are poorly understood. Here, we study the spontaneous solitary and social behaviors of naked mole-rats using automated animal tracking coupled with unbiased behavior discovery and experimenter-determined behavior quantification. With this approach, we find that reproductive and non-reproductive castes engage in distinct spontaneous behaviors. Further, the relative usage frequencies of a specific animal’s spontaneous behavior can be used to estimate its rank in the colony’s dominance hierarchy. Strikingly, we discovered that face touch is a prominent form of social interaction—naked mole-rats actively engage in face-to-face contact hundreds of times in a single 10-minute social pairing. We speculate that face-to-face contact might be related to social recognition, as we observe it performed during interactions in which naked mole-rats need to identify each other. Lastly, to demonstrate the specific importance of face-to-face contact, we show that social housing conditions lead to widespread activation of the mechanosensory ion channel Piezo2 in neurons that innervate the face, but not the rest of the body. Together, these findings support the importance of both caste and rank for the organization of spontaneous behavior in naked mole-rats, and they show that face-to-face contact is a prominent social behavior in these animals.