Socially regulated reproductive development: Analysis of GnRH-1 and kisspeptin neuronal systems in cooperatively breeding naked mole-rats (Heterocephalus glaber)

• Published in: Journal of comparative neurology (1911) Vol. 521; no. 13; pp. 3003 - 3029
• Main Authors: Zhou, Shuzhi, Holmes, Melissa M., Forger, Nancy G., Goldman, Bruce D., Lovern, Matthew B., Caraty, Alain, Kalló, Imre, Faulkes, Christopher G., Coen, Clive W.
• Format: Journal Article
• Language: English
• Published: United States Blackwell Publishing Ltd 01.09.2013; Wiley Subscription Services, Inc; Wiley
• Subjects: Animals; anteroventral periventricular nucleus; arcuate nucleus; Body Weight; Brain - cytology; Breeding; Castration; Cell Count; cooperation; Cooperative Behavior; dorsomedial hypothalamic nucleus; estradiol; Estradiol - blood; eusociality; Female; GnRH-1; Heterocephalus glaber; kisspeptin; Kisspeptins - metabolism; Life Sciences; Male; Mole Rats; naked mole-rat; Neurons - metabolism; Other; progesterone; Progesterone - blood; Radioimmunoassay; Receptors, LHRH - metabolism; reproductive suppression; RP3V; Sexual Behavior, Animal - physiology; social behavior; social status; testosterone; Testosterone - blood; dorsomedial hypothalamic nucleus; testosterone; kisspeptin; social behavior; RP3V; progesterone; social status; reproductive suppression; arcuate nucleus; naked mole-rat; eusociality; Heterocephalus glaber; GnRH-1; anteroventral periventricular nucleus; cooperation; estradiol; gnrh 1; heterocephalus glaber; rp3v
• ISSN: 0021-9967; 1096-9861
• DOI: 10.1002/cne.23327

ABSTRACT In naked mole‐rat (NMR) colonies, breeding is monopolized by the queen and her consorts. Subordinates experience gonadal development if separated from the queen. To elucidate the neuroendocrine factors underlying reproductive suppression/development in NMRs, we quantified plasma gonadal steroids and GnRH‐1‐ and kisspeptin‐immunoreactive (ir) neurons in subordinate adults and in those allowed to develop into breeders, with or without subsequent gonadectomy. In males and females, respectively, plasma testosterone and progesterone are higher in breeders than in subordinates. No such distinction occurs for plasma estradiol; its presence after gonadectomy and its positive correlation with adrenal estradiol suggest an adrenal source. Numbers of GnRH‐1‐ir cell bodies do not differ between gonad‐intact breeders and subordinates within or between the sexes. As in phylogenetically related guinea pigs, kisspeptin‐ir processes pervade the internal and external zones of the median eminence. Their distribution is consistent with actions on GnRH‐1 neurons at perikaryal and/or terminal levels. In previously investigated species, numbers of kisspeptin‐ir cell bodies vary from substantial to negligible according to sex and/or reproductive state. NMRs are exceptional: irrespective of sex, reproductive state, or presence of gonads, substantial numbers of kisspeptin‐ir cell bodies are detected in the rostral periventricular region of the third ventricle (RP3V) and in the anterior periventricular (PVa), arcuate, and dorsomedial hypothalamic nuclei. Nevertheless, the greater number in the RP3V/PVa of female breeders compared with female subordinates or male breeders suggests that emergence from a hypogonadotrophic state in females may involve kisspeptin‐related mechanisms similar to those underlying puberty or seasonal breeding in other species. J. Comp. Neurol. 521: 3003–3029, 2013. © 2013 Wiley Periodicals, Inc. In naked mole‐rat (NMR) colonies, the queen and her consorts monopolize breeding. This study has quantified GnRH‐1‐ and kisspeptin‐immunoreactive (ir) neurons and plasma gonadal steroids in breeders and subordinates. Extensive species comparisons show NMRs to be novel: substantial numbers of kisspeptin‐ir cell bodies are detected in the rostral periventricular region (including the AVPV) and arcuate and dorsomedial hypothalamic nuclei, irrespective of reproductive status, plasma gonadal steroids or sex. Nevertheless, rostral periventricular kisspeptin‐ir cell bodies are more numerous in female breeders than female subordinates.