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

Peragine, Deane E.; Yousuf, Yusef; Fu, Yi; Swift‐Gallant, Ashlyn; Ginzberg, Keren; Holmes, Melissa M.

doi:10.1016/j.yhbeh.2016.03.005

Cited by 13 publications

(12 citation statements)

References 102 publications

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“…Circulating T and P were detected by ELISA at an absorbance of 405 nm, as per manufacturer's instructions. All samples were run in duplicate with a Synergy-HT-Bio-Tek 96-well microplate reader and measured as described (46,47).…”

Section: Methodsmentioning

confidence: 99%

“…In colonies of up to 300 individuals, breeding is restricted to one dominant female (the queen) and one to three males, with other colony members being socially subordinate and reproductively suppressed. Though pronounced alterations in neural and endocrine function accompany the change (37)(38)(39)(40)(41)(42)(43)(44)(45)(46)(47), male and female subordinates are capable of transitioning to breeding status following the death/removal of breeders or separation from the colony. Indeed, although colony-housed subordinates have low progesterone (P), testosterone (T), and luteinizing hormone (LH) concentrations compared with same-sex breeders (37,38), they show elevated urinary P and T levels within 1 wk of separation from the colony (37,40), with females developing a perforated vagina during that time (37).…”

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confidence: 99%

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RFamide-related peptide-3 (RFRP-3) suppresses sexual maturation in a eusocial mammal

Peragine

Pokarowski

Mendoza-Viveros

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Neuroendocrine mechanisms underlying social inhibition of puberty are not well understood. Here, we use a model exhibiting the most profound case of pubertal suppression among mammals to explore a role for RFamide-related peptide-3 [RFRP-3; mammalian ortholog to gonadotropin-inhibitory hormone (GnIH)] in neuroendocrine control of reproductive development. Naked mole rats (NMRs) live in sizable colonies where breeding is monopolized by two to four dominant animals, and no other members exhibit signs of puberty throughout their lives unless they are removed from the colony. Because of its inhibitory action on the reproductive axis in other vertebrates, we investigated the role of RFRP-3 in social reproductive suppression in NMRs. We report that RFRP-3 immunofluorescence expression patterns and RFRP-3/GnRH cross-talk are largely conserved in the NMR brain, with the exception of the unique presence of RFRP-3 cell bodies in the arcuate nucleus (Arc). Immunofluorescence comparisons revealed that central expression of RFRP-3 is altered by reproductive status, with RFRP-3 immunoreactivity enhanced in the paraventricular nucleus, dorsomedial nucleus, and Arc of reproductively quiescent NMRs. We further observed that exogenous RFRP-3 suppresses gonadal steroidogenesis and mating behavior in NMRs given the opportunity to undergo puberty. Together, our findings establish a role for RFRP-3 in preserving reproductive immaturity, and challenge the view that stimulatory peptides are the ultimate gatekeepers of puberty.eusocial | GnIH | naked mole rat | puberty | RFRP-3

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Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

RFamide-related peptide-3 (RFRP-3) suppresses sexual maturation in a eusocial mammal

Peragine

Pokarowski

Mendoza-Viveros

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…We employed a liberal, exploratory approach to generate a large amount of data which can serve as the foundation for future directed hypothesis testing. In addition to revealing an under-appreciated association of the nucleus accumbens with this reproductive transition, we identify sex-specific gene expression patterns associated with pubertal transition in a species with reduced sex differences in the brain and behavior [ 69 – 70 , 74 – 76 , 84 – 89 ]. For example, while we have identified neurokinin B ( Tac3 ) in the arcuate nucleus as a key node in both males and females, a sub-network of Tac3/Tac3r/Crhr1 signalling in the arcuate nucleus seems to be exclusive to males, suggesting sex-specific mechanisms for crosstalk between the HPA and HPG axes.…”

Section: Discussionmentioning

confidence: 99%

“…To identify candidate genes and circuits involved in socially-mediated pubertal suppression in naked mole-rats, we quantified expression of several reproduction- and stress-relevant genes that act upstream of GnRH (outlined in Fig 1 ). We compared subordinate and breeding animals, in addition to a transition group of reproductively-activated, non-breeding animals (opposite-sex paired; OS; described in [ 76 ]) ( Fig 1A ). OS animals are removed from the suppressive cues of the colony, but while they show evidence of reproductive maturation, they have yet to produce a litter.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2018

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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.

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“…To date, our work suggests that the DG, piriform cortex, and basolateral amygdala (BLA) have increased neurogenesis, based on doublecortin staining, in subordinate animals relative to dominants (Peragine et al, 2014 ). Interestingly, female animals removed from their colony and paired with a female show evidence of increased neurogenesis in the basolateral amygdala (BLA) relative to animals paired with males (Peragine et al, 2016 ). This might reflect the role of the BLA in mediating stress and threat in other mammals (Levinson et al, 1980 ; Fanselow and LeDoux, 1999 ; Jacobs et al, 2006 ) coupled with the unique female-dominant aspect of naked mole-rat social organization.…”

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confidence: 99%

Solving the Neurogenesis Puzzle: Looking for Pieces Outside the Traditional Box

2017

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The vast majority of what is considered fact about adult neurogenesis comes from research on laboratory mice and rats: where it happens, how it works, what it does. However, this relative exclusive focus on two rodent species has resulted in a bias on how we think about adult neurogenesis. While it might not prevent us from making conclusions about the evolutionary significance of the process or even prevent us from generalizing to diverse mammals, it certainly does not help us achieve these outcomes. Here, we argue that there is every reason to expect striking species differences in adult neurogenesis: where it happens, how it works, what it does. Species-specific adaptations in brain and behavior are paramount to survival and reproduction in diverse ecological niches and it is naive to think adult neurogenesis escaped these evolutionary pressures. A neuroethological approach to the study of adult neurogenesis is essential for a comprehensive understanding of the phenomenon. Furthermore, most of us are guilty of making strong assertions about our data in order to have impact yet this ultimately creates bias in how work is performed, interpreted, and applied. By taking a step back and actually placing our results in a much larger, non-biomedical context, we can help to reduce dogmatic thinking and create a framework for discovery.

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

Cited by 13 publications

References 102 publications

RFamide-related peptide-3 (RFRP-3) suppresses sexual maturation in a eusocial mammal

RFamide-related peptide-3 (RFRP-3) suppresses sexual maturation in a eusocial mammal

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

Solving the Neurogenesis Puzzle: Looking for Pieces Outside the Traditional Box

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