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Breeding status and social environment differentially affect the expression of sex steroid receptor and aromatase mRNA in the brain of female Damaraland mole-rats

INTRODUCTION: The Damaraland mole-rat (Fukomys damarensis) is a eusocial, subterranean mammal, which exhibits an extreme reproductive skew with a single female (queen) monopolizing reproduction in each colony. Non-reproductive females in the presence of the queen are physiologically suppressed to th...

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Autores principales: Voigt, Cornelia, Gahr, Manfred, Leitner, Stefan, Lutermann, Heike, Bennett, Nigel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4024188/
https://www.ncbi.nlm.nih.gov/pubmed/24839456
http://dx.doi.org/10.1186/1742-9994-11-38
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author Voigt, Cornelia
Gahr, Manfred
Leitner, Stefan
Lutermann, Heike
Bennett, Nigel
author_facet Voigt, Cornelia
Gahr, Manfred
Leitner, Stefan
Lutermann, Heike
Bennett, Nigel
author_sort Voigt, Cornelia
collection PubMed
description INTRODUCTION: The Damaraland mole-rat (Fukomys damarensis) is a eusocial, subterranean mammal, which exhibits an extreme reproductive skew with a single female (queen) monopolizing reproduction in each colony. Non-reproductive females in the presence of the queen are physiologically suppressed to the extent that they are anovulatory. This blockade is thought to be caused by a disruption in the normal gonadotropin-releasing hormone (GnRH) secretion from the hypothalamus. In order to understand the underlying physiological mechanisms of reproductive suppression in subordinate females we studied the expression of steroid hormone receptors and the androgen-converting enzyme aromatase in forebrain regions involved in the control of reproductive behaviour in female breeders and non-breeders from intact colonies. Additionally, we included in our analysis females that experienced the release from social suppression by being removed from the presence of the queen. RESULTS: We found expression of androgen receptor, estrogen receptor α and aromatase in several forebrain regions of female Damaraland mole-rats. Their distribution matches previous findings in other mammals. Quantification of the hybridisation signal revealed that queens had increased expression of androgen receptors compared to non-breeders and removed non-breeders in most brain regions examined, which include the medial preoptic area (MPOA), the principal nucleus of the bed nucleus of the stria terminalis (BSTp), the ventromedial nucleus of the hypothalamus (VMH), the arcuate nucleus (ARC) and the medial amygdala (MeA). Furthermore, breeders had increased estrogen receptor α expression in the anteroventral periventricular nucleus (AVPV) and in the MeA, while aromatase expression in the AVPV was significantly reduced compared to non-breeders. Absence of social suppression was associated with increased androgen receptor expression in the ARC, increased estrogen receptor α expression in the MeA and BSTp and reduced aromatase expression in the AVPV. CONCLUSION: This study shows that social suppression and breeding differentially affect the neuroendocrine phenotype of female Damaraland mole-rats. The differential expression pattern of estrogen receptor α and aromatase in the AVPV between breeders and non-breeders supports the view that this region plays an important role in mediating the physiological suppression in subordinate females.
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spelling pubmed-40241882014-05-18 Breeding status and social environment differentially affect the expression of sex steroid receptor and aromatase mRNA in the brain of female Damaraland mole-rats Voigt, Cornelia Gahr, Manfred Leitner, Stefan Lutermann, Heike Bennett, Nigel Front Zool Research INTRODUCTION: The Damaraland mole-rat (Fukomys damarensis) is a eusocial, subterranean mammal, which exhibits an extreme reproductive skew with a single female (queen) monopolizing reproduction in each colony. Non-reproductive females in the presence of the queen are physiologically suppressed to the extent that they are anovulatory. This blockade is thought to be caused by a disruption in the normal gonadotropin-releasing hormone (GnRH) secretion from the hypothalamus. In order to understand the underlying physiological mechanisms of reproductive suppression in subordinate females we studied the expression of steroid hormone receptors and the androgen-converting enzyme aromatase in forebrain regions involved in the control of reproductive behaviour in female breeders and non-breeders from intact colonies. Additionally, we included in our analysis females that experienced the release from social suppression by being removed from the presence of the queen. RESULTS: We found expression of androgen receptor, estrogen receptor α and aromatase in several forebrain regions of female Damaraland mole-rats. Their distribution matches previous findings in other mammals. Quantification of the hybridisation signal revealed that queens had increased expression of androgen receptors compared to non-breeders and removed non-breeders in most brain regions examined, which include the medial preoptic area (MPOA), the principal nucleus of the bed nucleus of the stria terminalis (BSTp), the ventromedial nucleus of the hypothalamus (VMH), the arcuate nucleus (ARC) and the medial amygdala (MeA). Furthermore, breeders had increased estrogen receptor α expression in the anteroventral periventricular nucleus (AVPV) and in the MeA, while aromatase expression in the AVPV was significantly reduced compared to non-breeders. Absence of social suppression was associated with increased androgen receptor expression in the ARC, increased estrogen receptor α expression in the MeA and BSTp and reduced aromatase expression in the AVPV. CONCLUSION: This study shows that social suppression and breeding differentially affect the neuroendocrine phenotype of female Damaraland mole-rats. The differential expression pattern of estrogen receptor α and aromatase in the AVPV between breeders and non-breeders supports the view that this region plays an important role in mediating the physiological suppression in subordinate females. BioMed Central 2014-05-08 /pmc/articles/PMC4024188/ /pubmed/24839456 http://dx.doi.org/10.1186/1742-9994-11-38 Text en Copyright © 2014 Voigt et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/4.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Voigt, Cornelia
Gahr, Manfred
Leitner, Stefan
Lutermann, Heike
Bennett, Nigel
Breeding status and social environment differentially affect the expression of sex steroid receptor and aromatase mRNA in the brain of female Damaraland mole-rats
title Breeding status and social environment differentially affect the expression of sex steroid receptor and aromatase mRNA in the brain of female Damaraland mole-rats
title_full Breeding status and social environment differentially affect the expression of sex steroid receptor and aromatase mRNA in the brain of female Damaraland mole-rats
title_fullStr Breeding status and social environment differentially affect the expression of sex steroid receptor and aromatase mRNA in the brain of female Damaraland mole-rats
title_full_unstemmed Breeding status and social environment differentially affect the expression of sex steroid receptor and aromatase mRNA in the brain of female Damaraland mole-rats
title_short Breeding status and social environment differentially affect the expression of sex steroid receptor and aromatase mRNA in the brain of female Damaraland mole-rats
title_sort breeding status and social environment differentially affect the expression of sex steroid receptor and aromatase mrna in the brain of female damaraland mole-rats
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4024188/
https://www.ncbi.nlm.nih.gov/pubmed/24839456
http://dx.doi.org/10.1186/1742-9994-11-38
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