Sex- and brain region-specific patterns of gene expression associated with socially-mediated puberty in a eusocial mammal

Abstract

The social environment can alter pubertal timing through neuroendocrine mechanisms that are not fully understood; it is thought that stress hormones (e.g., glucocorticoids or corticotropin-releasing hormone) influence the hypothalamic-pituitary-gonadal axis to inhibit puberty. Here, we use the eusocial naked mole-rat, a unique species in which social interactions in a colony (i.e. dominance of a breeding female) suppress puberty in subordinate animals. Removing subordinate naked mole-rats from this social context initiates puberty, allowing for experimental control of pubertal timing. The present study quantified gene expression for reproduction- and stress-relevant genes acting upstream of gonadotropin-releasing hormone in brain regions with reproductive and social functions in pre-pubertal, post-pubertal, and opposite sex-paired animals (which are in various stages of pubertal transition). Results indicate sex differences in patterns of neural gene expression. Known functions of genes in brain suggest stress as a key contributing factor in regulating male pubertal delay. Network analysis implicates neurokinin B (Tac3) in the arcuate nucleus of the hypothalamus as a key node in this pathway. Results also suggest an unappreciated role for the nucleus accumbens in regulating puberty.

Hormones do not make the mole-rat: no steroid hormone signatures of subordinate behavioral phenotypes

“…While multiple studies have looked at hormonal differences between reproductive and non-reproductive naked mole-rats, hormone differences within the non-reproductive caste have not been extensively explored. Generally, subordinate naked mole-rats have lower testosterone, estradiol, and progesterone levels than breeders (Clarke and Faulkes, 1997;Faulkes et al, 1990b;Faykoo-Martinez et al, 2018;Swift-Gallant et al, 2015). Urinary testosterone is strongly negatively correlated with dominance rank in both sexes, and subordinate females with the highest testosterone levels became reproductively active upon queen removal (Clarke and Faulkes, 1997).…”

Expression patterns of kiss2 and gpr54‐2 in Monopterus albus suggest these genes may play a role in sex reversal in fish

“…Kiss2 , however, was not highly expressed in any of the studied brain samples, which may be an indication of functional diversification. However, as the expression of these two genes varies strongly among different parts of the brain , so this may also be a reflection of the fact that we sampled (almost) entire brains, and failed to extract DNA from the pituitary gland, which may have skewed the overall expression results downwards.…”

Oxytocin Manipulation Alters Neural Activity in Response to Social Stimuli in Eusocial Naked Mole-Rats

“…The NAcc is also involved in reproductive behavior and social dominance in naked mole-rats. For example, OT receptor binding is higher in breeding male NAcc compared to breeding females ( Mooney et al, 2015a ) and expression of genes involved in social suppression of reproduction ( Kiss1 , Npvf , Gpr147 , Tac3r ) varies by sex and status ( Faykoo-Martinez et al, 2018 ). The current data demonstrate that the NAcc is a key node in all three behavioral paradigms (Figure 5 ).…”