Socially Induced Infertility in Naked and Damaraland Mole-Rats: A Tale of Two Mechanisms of Social Suppression

SIMPLE SUMMARY: The naked and Damaraland mole-rats are group-living, subterranean mammals in which reproduction is distributed unequally among members of a social group, also referred to as reproductive skew. Only a single female per group, called the queen, produces offspring with the most dominant males of the group. The non-reproductive colony members are physiologically suppressed by the presence of the queen. This is reflected in their low concentration of luteinising hormone released from the pituitary and in their reduced responsiveness of the pituitary to stimulation with gonadotropin releasing hormone. Removal of the queen reverses these effects and leads to endocrine conditions in these females that are similar to those in reproductively active females. Regarding males, the extent of reproductive suppression is different between the two species. Non-reproductive male Damaraland mole-rats show hormonal profiles similar to the breeding males, whereas non-reproductive male naked mole-rats are physiologically suppressed similar to non-reproductive females. Thus, the two species represent ideal models to unravel the physiological, behavioural and neuroendocrine mechanisms regulating the hypothalamic-pituitary-gonadal axis. The recently discovered neuropeptides kisspeptin and RFamide-related peptide-3 are likely candidates to play an important role in the regulation of reproductive functions in the two mole-rat species. ABSTRACT: The naked mole-rat (Heterocephalus glaber) and the Damaraland mole-rat (Fukomys damarensis) possess extreme reproductive skew with a single reproductive female responsible for reproduction. In this review, we synthesize advances made into African mole-rat reproductive patterns and physiology within the context of the social control of reproduction. Non-reproductive female colony members have low concentrations of luteinising hormone (LH) and a reduced response of the pituitary to a challenge with gonadotropin releasing hormone (GnRH). If the reproductive female is removed from the colony, an increase in the basal plasma LH and increased pituitary response to a GnRH challenge arises in the non-reproductive females, suggesting the reproductive female controls reproduction. Non-reproductive male Damaraland mole-rats have basal LH concentrations and elevated LH concentrations in response to a GnRH challenge comparable to the breeding male, but in non-breeding male naked mole-rats, the basal LH concentrations are low and there is a muted response to a GnRH challenge. This renders these two species ideal models to investigate physiological, behavioural and neuroendocrine mechanisms regulating the hypothalamic-pituitary-gonadal axis. The recently discovered neuropeptides kisspeptin and RFamide-related peptide-3 are likely candidates to play an important role in the regulation of reproductive functions in the two mole-rat species.