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Androgen Elevation Accelerates Reproductive Senescence in Three-Spined Stickleback

Costs of reproduction shape the life-history evolution of investment in current and future reproduction and thereby aging. Androgens have been proposed to regulate the physiology governing these investments. Furthermore, androgens are hypothesized to play a central role in carotenoid-dependent sexua...

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Autores principales: Simons, Mirre J. P., Sebire, Marion, Verhulst, Simon, Groothuis, Ton G. G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8718761/
https://www.ncbi.nlm.nih.gov/pubmed/34977010
http://dx.doi.org/10.3389/fcell.2021.752352
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author Simons, Mirre J. P.
Sebire, Marion
Verhulst, Simon
Groothuis, Ton G. G.
author_facet Simons, Mirre J. P.
Sebire, Marion
Verhulst, Simon
Groothuis, Ton G. G.
author_sort Simons, Mirre J. P.
collection PubMed
description Costs of reproduction shape the life-history evolution of investment in current and future reproduction and thereby aging. Androgens have been proposed to regulate the physiology governing these investments. Furthermore, androgens are hypothesized to play a central role in carotenoid-dependent sexual signaling, regulating how much carotenoids are diverted to ornamentation and away from somatic maintenance, increasing oxidative stress, and accelerating aging. We investigated these relationships in male three-spined stickleback in which we elevated 11-ketotestosterone and supplied vitamin E, an antioxidant, in a 2 × 2 design. Androgen elevation shortened the time stickleback maintained reproductive activities. We suspect that this effect is caused by 11-ketotestosterone stimulating investment in current reproduction, but we detected no evidence for this in our measurements of reproductive effort: nest building, body composition, and breeding coloration. Carotenoid-dependent coloration was even slightly decreased by 11-ketotestosterone elevation and was left unaffected by vitamin E. Red coloration correlated with life expectancy and reproductive capacity in a quadratic manner, suggesting overinvestment of the individuals exhibiting the reddest bellies. In contrast, blue iris color showed a negative relationship with survival, suggesting physiological costs of producing this aspect of nuptial coloration. In conclusion, our results support the hypothesis that androgens regulate investment in current versus future reproduction, yet the precise mechanisms remain elusive. The quadratic relationships between sexual signal expression and aspects of quality have wider consequences for how we view sexual selection on ornamentation and its relationship with aging.
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spelling pubmed-87187612022-01-01 Androgen Elevation Accelerates Reproductive Senescence in Three-Spined Stickleback Simons, Mirre J. P. Sebire, Marion Verhulst, Simon Groothuis, Ton G. G. Front Cell Dev Biol Cell and Developmental Biology Costs of reproduction shape the life-history evolution of investment in current and future reproduction and thereby aging. Androgens have been proposed to regulate the physiology governing these investments. Furthermore, androgens are hypothesized to play a central role in carotenoid-dependent sexual signaling, regulating how much carotenoids are diverted to ornamentation and away from somatic maintenance, increasing oxidative stress, and accelerating aging. We investigated these relationships in male three-spined stickleback in which we elevated 11-ketotestosterone and supplied vitamin E, an antioxidant, in a 2 × 2 design. Androgen elevation shortened the time stickleback maintained reproductive activities. We suspect that this effect is caused by 11-ketotestosterone stimulating investment in current reproduction, but we detected no evidence for this in our measurements of reproductive effort: nest building, body composition, and breeding coloration. Carotenoid-dependent coloration was even slightly decreased by 11-ketotestosterone elevation and was left unaffected by vitamin E. Red coloration correlated with life expectancy and reproductive capacity in a quadratic manner, suggesting overinvestment of the individuals exhibiting the reddest bellies. In contrast, blue iris color showed a negative relationship with survival, suggesting physiological costs of producing this aspect of nuptial coloration. In conclusion, our results support the hypothesis that androgens regulate investment in current versus future reproduction, yet the precise mechanisms remain elusive. The quadratic relationships between sexual signal expression and aspects of quality have wider consequences for how we view sexual selection on ornamentation and its relationship with aging. Frontiers Media S.A. 2021-12-17 /pmc/articles/PMC8718761/ /pubmed/34977010 http://dx.doi.org/10.3389/fcell.2021.752352 Text en Copyright © 2021 Simons, Sebire, Verhulst and Groothuis. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Simons, Mirre J. P.
Sebire, Marion
Verhulst, Simon
Groothuis, Ton G. G.
Androgen Elevation Accelerates Reproductive Senescence in Three-Spined Stickleback
title Androgen Elevation Accelerates Reproductive Senescence in Three-Spined Stickleback
title_full Androgen Elevation Accelerates Reproductive Senescence in Three-Spined Stickleback
title_fullStr Androgen Elevation Accelerates Reproductive Senescence in Three-Spined Stickleback
title_full_unstemmed Androgen Elevation Accelerates Reproductive Senescence in Three-Spined Stickleback
title_short Androgen Elevation Accelerates Reproductive Senescence in Three-Spined Stickleback
title_sort androgen elevation accelerates reproductive senescence in three-spined stickleback
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8718761/
https://www.ncbi.nlm.nih.gov/pubmed/34977010
http://dx.doi.org/10.3389/fcell.2021.752352
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