The naked mole-rat (Heterocephalus glaber) is one of the most social mammals on the planet. These animals live in underground colonies consisting of a breeding female (the “queen”), 1 to 3 breeding males and up to 300 nonreproductive “workers” organized in a dominance hierarchy. In addition to their eusociality, naked mole-rats have evolved many extreme biological characteristics including an exquisite sense of touch and insensitivity to certain types of pain. However, the overlap between the social and somatosensory abilities of naked mole-rats remains mysterious. In this work, we show that naked mole-rats exhibit caste-like behavioral signatures linked to eusociality, predominantly utilize snout-to-snout interactions in social behavior and possess a somatosensory profile to mechanical stimuli distinct from mice.
In the first chapter of this work, we leveraged machine learning and molecular biology tools to create a behavioral atlas of naked mole-rat behavior. We first utilized a computational pipeline of pose-tracking using SLEAP and behavioral segmentation using keypoint-MoSeq to identify 20+ behavioral syllables. This showed that the queen naked mole-rat has a distinct behavioral phenotype from the workers, consisting of faster movements, less anxiety-like freezing, and less colony maintenance behaviors such as digging.
We next showed that behavioral differences exist between the workers and that the dominance rank of a given individual could be predicted by its spontaneous behaviors in an open field. Relative rank differential appeared to have relevance for social behaviors: during a tube test for dominance, pairings of a high-ranked and low-ranked animal occurred more quickly and were won more frequently by the dominant animal. Snout touch played an integral role in these dominance tests (perhaps in the communication of individual ID information). This prompted us to investigate snout-to-snout interactions in the open field. We found that two familiar naked mole-rats from the same colony engaged in hundreds of snout interactions in a 10-minute period, and the number of interactions was nearly twice as high between two foreign animals. Follow-up experiments explored the molecular basis of this snout touch and showed that mechanosensory channels (e.g. Piezo2) are likely involved in social snout-to-snout interactions. Furthermore, trimming the sensory whiskers of naked mole-rats disrupts their ability to recognize conspecifics and alters their relative dominance relationships. These findings uncover face touch as a prominent social behavior in naked mole-rats that is intimately linked to social recognition.
In the second chapter of this work, we more deeply investigated naked mole-rat somatosensation by using high-speed videography. We began by determining how naked mole-rats respond to both innocuous stimuli (cotton swab, dynamic brush) and noxious stimuli (light and heavy pinpricks) when given to the hindpaw. Compared to mice, naked mole-rats showed a distinct hindpaw phenotype, never responding to innocuous touch stimuli, responding to light pinprick, but rarely responding to heavy pinprick (normally the most noxious stimulus that elicits the strongest pain response in mice).
Interestingly, naked mole-rats do respond to brush stimuli to the back skin with a dorsiflexion posture. These animals also exhibit an idiosyncratic withdrawal response to a brush applied to the snout skin which appears to be highly aversive. Interestingly, the velocity of this aversive snout withdrawal appears to be socially modulated and is decreased in the presence of another naked mole-rat in the testing chamber. This phenotype does not occur in mice and provides additional evidence that the naked mole-rat snout is not only extremely sensitive but plays a role in processing socially relevant information.
| Identifer | oai:union.ndltd.org:columbia.edu/oai:academiccommons.columbia.edu:10.7916/9z73-8076 |
| Date | January 2024 |
| Creators | Schwark, Ryan William |
| Source Sets | Columbia University |
| Language | English |
| Detected Language | English |
| Type | Theses |
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