Neuroendocrine regulation of individual differences in social phenotype

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The overarching objective of this proposal is to understand how neuroendocrine circuits regulate stable individual differences in social behaviour. Naked mole-rats provide a powerful opportunity to study neural control of social phenotype. They are small rodents that exhibit the most rigidly organized social and reproductive hierarchy among mammals, living in large colonies of up to 300 individuals in which reproduction is restricted to a single breeding female (called the queen) and one to three breeding males. Breeders are socially dominant over all other members of the colony, called subordinates, which are kept non-reproductive by the presence of the queen. A transition in social status from subordinate to breeder triggers morphological and functional changes in their brains, including regions that control social behaviours. We have discovered that RFamide-related peptide-3 (RFRP-3) is the hormone responsible for keeping animals suppressed but that stress hormones and oxytocin, a hormone involved in social behaviour, also differ between subordinate and breeding animals. The experiments in Aim 1 will identify interactions between RFRP-3, stress hormones, and oxytocin by manipulating hormone levels and measuring changes in behaviour and gene expression in brain. Next, we will capitalize on the fact that subordinates can be further sub-divided into workers and soldiers though almost nothing is known about how their brains differ. Aim 2 will characterize neuroendocrine differences between subcastes and test a causal role for oxytocin in whether individuals are prosocial workers or aggressive soldiers. Finally, naked mole-rats can transition to any social phenotype though individual predispositions for particular roles exist. Using both a behavioural and mechanistic approach, Aim 3 will explore how early environment influences the developmental trajectory of differing subcastes. Collectively, the work proposed herein seeks to tease apart how neuroendocrine systems interact in a bidirectional manner and how these effects are further influenced by epigenetic and environmental factors. By capitalizing on the remarkable sociality of naked mole-rats to reveal how neuroendocrine systems are involved in social phenotype, this work will help reveal how specialized neural circuits control the expression of social behaviours in mammals and, in turn, how the social environment affects development and plasticity in the mammalian brain.