Contrasting effects of opposite- versus same-sex housing on hormones, behavior and neurogenesis in a eusocial mammal

Abstract

Competitive interactions can have striking and enduring effects on behavior, but the mechanisms underlying this experience-induced plasticity are unclear, particularly in females. Naked mole-rat (NMR) colonies are characterized by the strictest social and reproductive hierarchy among mammals, and represent an ideal system for studies of social competition. In large matriarchal colonies, breeding is monopolized by one female and 1–3 males, with other colony members being socially subordinate and reproductively suppressed. To date, competition for breeding status has been examined in-colony, with female, but not male, aggression observed following the death/removal of established queens. To determine whether this sex difference extends to colony-founding contexts, and clarify neural and endocrine mechanisms underlying behavioral change in females competing for status, we examined neurogenesis and steroid hormone concentrations in colony-housed subordinates, and NMRs given the opportunity to transition status via pair-housing. To this end, Ki-67 and doublecortin immunoreactivity were compared in the hippocampal dentate gyrus (DG) and basolateral amygdala (BLA) of colony-housed subordinates, and subordinates housed with a same-sex (SS) or opposite-sex (OS) conspecific. Results suggest that OS pairing in eusocial mammals promotes cooperation and enhances hippocampal plasticity, while SS pairing is stressful, resulting in enhanced HPA activation and muted hippocampal neurogenesis relative to OS pairs. Data further indicate that competition for status is confined to females, with female-female housing exerting contrasting effects on hippocampal and amygdalar neurogenesis. These findings advance understanding of social stress effects on neuroplasticity and behavior, and highlight the importance of including female-dominated species in research on aggression and intrasexual competition.