The direct response of the gonads to cues of stress in a temperate songbird species is season-dependent

The gonadotropin releasing hormone (GnRH) system in the hypothalamus is often considered the final point in integration of environmental cues as they pertain to the reproductive axis. However, cues such as stress and food availability are detectable in the plasma (as glucocorticoid and metabolic fue...

Full description

Bibliographic Details
Main Authors: Nicolette L. McGuire, Annie Koh, George E. Bentley
Format: Article
Language:English
Published: PeerJ Inc. 2013-08-01
Series:PeerJ
Subjects:
Online Access:https://peerj.com/articles/139.pdf
_version_ 1827611064158650368
author Nicolette L. McGuire
Annie Koh
George E. Bentley
author_facet Nicolette L. McGuire
Annie Koh
George E. Bentley
author_sort Nicolette L. McGuire
collection DOAJ
description The gonadotropin releasing hormone (GnRH) system in the hypothalamus is often considered the final point in integration of environmental cues as they pertain to the reproductive axis. However, cues such as stress and food availability are detectable in the plasma (as glucocorticoid and metabolic fuel fluctuations). Vertebrate gonads express glucocorticoid receptor, therefore we hypothesized that the gonads can detect and respond directly to cues of stress. We provide evidence here that, in addition to regulation by the brain, the gonads of European starlings (Sturnus vulgaris) respond directly to fluctuations in corticosterone and metabolic fuels by modulating sex steroid secretion. Using a 4-h gonad culture, we show that physiologically-relevant concentrations of corticosterone and metabolic stress (via use of the glucose utilization inhibitor 2-deoxy-D-glucose and the fatty acid oxidation inhibitor ethyl 2-mercaptoacetate (2DG/MA)) can directly decrease testosterone and estradiol secretion from luteinizing hormone and follicle-stimulating hormone (LH/FSH)-stimulated testes and ovaries. This effect is regulated seasonally. Prior to the breeding season, testes and ovaries respond to corticosterone and 2DG/MA by significantly decreasing gonadal steroid release. Within the breeding season, the testes do not respond to these cues of stress, while the ovaries respond only to corticosterone. This seasonal difference in response may be due in part to the influence of these cues of stress on gonadal neuropeptide expression: corticosterone upregulates GnIH expression in the testes while metabolic stress upregulates GnIH in the ovaries. Thus the gonads can directly respond to fluctuations in corticosterone and metabolic fuels during a time of critical importance to the onset of breeding.
first_indexed 2024-03-09T08:00:44Z
format Article
id doaj.art-95f622c457474bc0ada6ea571baeb077
institution Directory Open Access Journal
issn 2167-8359
language English
last_indexed 2024-03-09T08:00:44Z
publishDate 2013-08-01
publisher PeerJ Inc.
record_format Article
series PeerJ
spelling doaj.art-95f622c457474bc0ada6ea571baeb0772023-12-03T00:47:38ZengPeerJ Inc.PeerJ2167-83592013-08-011e13910.7717/peerj.139139The direct response of the gonads to cues of stress in a temperate songbird species is season-dependentNicolette L. McGuire0Annie Koh1George E. Bentley2Laboratory of Reproductive Neuroendocrinology, Department of Integrative Biology, University of California at Berkeley, USALaboratory of Reproductive Neuroendocrinology, Department of Integrative Biology, University of California at Berkeley, USALaboratory of Reproductive Neuroendocrinology, Department of Integrative Biology, University of California at Berkeley, USAThe gonadotropin releasing hormone (GnRH) system in the hypothalamus is often considered the final point in integration of environmental cues as they pertain to the reproductive axis. However, cues such as stress and food availability are detectable in the plasma (as glucocorticoid and metabolic fuel fluctuations). Vertebrate gonads express glucocorticoid receptor, therefore we hypothesized that the gonads can detect and respond directly to cues of stress. We provide evidence here that, in addition to regulation by the brain, the gonads of European starlings (Sturnus vulgaris) respond directly to fluctuations in corticosterone and metabolic fuels by modulating sex steroid secretion. Using a 4-h gonad culture, we show that physiologically-relevant concentrations of corticosterone and metabolic stress (via use of the glucose utilization inhibitor 2-deoxy-D-glucose and the fatty acid oxidation inhibitor ethyl 2-mercaptoacetate (2DG/MA)) can directly decrease testosterone and estradiol secretion from luteinizing hormone and follicle-stimulating hormone (LH/FSH)-stimulated testes and ovaries. This effect is regulated seasonally. Prior to the breeding season, testes and ovaries respond to corticosterone and 2DG/MA by significantly decreasing gonadal steroid release. Within the breeding season, the testes do not respond to these cues of stress, while the ovaries respond only to corticosterone. This seasonal difference in response may be due in part to the influence of these cues of stress on gonadal neuropeptide expression: corticosterone upregulates GnIH expression in the testes while metabolic stress upregulates GnIH in the ovaries. Thus the gonads can directly respond to fluctuations in corticosterone and metabolic fuels during a time of critical importance to the onset of breeding.https://peerj.com/articles/139.pdfStressGonadotropin inhibitory hormone (GnIH)CorticosteroneGonadotropin releasing hormone (GnRH)TestesEstradiol
spellingShingle Nicolette L. McGuire
Annie Koh
George E. Bentley
The direct response of the gonads to cues of stress in a temperate songbird species is season-dependent
PeerJ
Stress
Gonadotropin inhibitory hormone (GnIH)
Corticosterone
Gonadotropin releasing hormone (GnRH)
Testes
Estradiol
title The direct response of the gonads to cues of stress in a temperate songbird species is season-dependent
title_full The direct response of the gonads to cues of stress in a temperate songbird species is season-dependent
title_fullStr The direct response of the gonads to cues of stress in a temperate songbird species is season-dependent
title_full_unstemmed The direct response of the gonads to cues of stress in a temperate songbird species is season-dependent
title_short The direct response of the gonads to cues of stress in a temperate songbird species is season-dependent
title_sort direct response of the gonads to cues of stress in a temperate songbird species is season dependent
topic Stress
Gonadotropin inhibitory hormone (GnIH)
Corticosterone
Gonadotropin releasing hormone (GnRH)
Testes
Estradiol
url https://peerj.com/articles/139.pdf
work_keys_str_mv AT nicolettelmcguire thedirectresponseofthegonadstocuesofstressinatemperatesongbirdspeciesisseasondependent
AT anniekoh thedirectresponseofthegonadstocuesofstressinatemperatesongbirdspeciesisseasondependent
AT georgeebentley thedirectresponseofthegonadstocuesofstressinatemperatesongbirdspeciesisseasondependent
AT nicolettelmcguire directresponseofthegonadstocuesofstressinatemperatesongbirdspeciesisseasondependent
AT anniekoh directresponseofthegonadstocuesofstressinatemperatesongbirdspeciesisseasondependent
AT georgeebentley directresponseofthegonadstocuesofstressinatemperatesongbirdspeciesisseasondependent