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Sex‐ and time‐specific parental effects of warming on reproduction and offspring quality in a coral reef fish

Global warming can disrupt reproduction or lead to fewer and poorer quality offspring, owing to the thermally sensitive nature of reproductive physiology. However, phenotypic plasticity may enable some animals to adjust the thermal sensitivity of reproduction to maintain performance in warmer condit...

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Autores principales: Spinks, Rachel K., Bonzi, Lucrezia C., Ravasi, Timothy, Munday, Philip L., Donelson, Jennifer M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8061261/
https://www.ncbi.nlm.nih.gov/pubmed/33897826
http://dx.doi.org/10.1111/eva.13187
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author Spinks, Rachel K.
Bonzi, Lucrezia C.
Ravasi, Timothy
Munday, Philip L.
Donelson, Jennifer M.
author_facet Spinks, Rachel K.
Bonzi, Lucrezia C.
Ravasi, Timothy
Munday, Philip L.
Donelson, Jennifer M.
author_sort Spinks, Rachel K.
collection PubMed
description Global warming can disrupt reproduction or lead to fewer and poorer quality offspring, owing to the thermally sensitive nature of reproductive physiology. However, phenotypic plasticity may enable some animals to adjust the thermal sensitivity of reproduction to maintain performance in warmer conditions. Whether elevated temperature affects reproduction may depend on the timing of exposure to warming and the sex of the parent exposed. We exposed male and female coral reef damselfish (Acanthochromis polyacanthus) during development, reproduction or both life stages to an elevated temperature (+1.5°C) consistent with projected ocean warming and measured reproductive output and newly hatched offspring performance relative to pairs reared in a present‐day control temperature. We found female development in elevated temperature increased the probability of breeding, but reproduction ceased if warming continued to the reproductive stage, irrespective of the male's developmental experience. Females that developed in warmer conditions, but reproduced in control conditions, also produced larger eggs and hatchlings with greater yolk reserves. By contrast, male development or pairs reproducing in higher temperature produced fewer and poorer quality offspring. Such changes may be due to alterations in sex hormones or an endocrine stress response. In nature, this could mean female fish developing during a marine heatwave may have enhanced reproduction and produce higher quality offspring compared with females developing in a year of usual thermal conditions. However, male development during a heatwave would likely result in reduced reproductive output. Furthermore, the lack of reproduction from an average increase in temperature could lead to population decline. Our results demonstrate how the timing of exposure differentially influences females and males and how this translates to effects on reproduction and population sustainability in a warming world.
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spelling pubmed-80612612021-04-23 Sex‐ and time‐specific parental effects of warming on reproduction and offspring quality in a coral reef fish Spinks, Rachel K. Bonzi, Lucrezia C. Ravasi, Timothy Munday, Philip L. Donelson, Jennifer M. Evol Appl Original Articles Global warming can disrupt reproduction or lead to fewer and poorer quality offspring, owing to the thermally sensitive nature of reproductive physiology. However, phenotypic plasticity may enable some animals to adjust the thermal sensitivity of reproduction to maintain performance in warmer conditions. Whether elevated temperature affects reproduction may depend on the timing of exposure to warming and the sex of the parent exposed. We exposed male and female coral reef damselfish (Acanthochromis polyacanthus) during development, reproduction or both life stages to an elevated temperature (+1.5°C) consistent with projected ocean warming and measured reproductive output and newly hatched offspring performance relative to pairs reared in a present‐day control temperature. We found female development in elevated temperature increased the probability of breeding, but reproduction ceased if warming continued to the reproductive stage, irrespective of the male's developmental experience. Females that developed in warmer conditions, but reproduced in control conditions, also produced larger eggs and hatchlings with greater yolk reserves. By contrast, male development or pairs reproducing in higher temperature produced fewer and poorer quality offspring. Such changes may be due to alterations in sex hormones or an endocrine stress response. In nature, this could mean female fish developing during a marine heatwave may have enhanced reproduction and produce higher quality offspring compared with females developing in a year of usual thermal conditions. However, male development during a heatwave would likely result in reduced reproductive output. Furthermore, the lack of reproduction from an average increase in temperature could lead to population decline. Our results demonstrate how the timing of exposure differentially influences females and males and how this translates to effects on reproduction and population sustainability in a warming world. John Wiley and Sons Inc. 2021-01-13 /pmc/articles/PMC8061261/ /pubmed/33897826 http://dx.doi.org/10.1111/eva.13187 Text en © 2020 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Spinks, Rachel K.
Bonzi, Lucrezia C.
Ravasi, Timothy
Munday, Philip L.
Donelson, Jennifer M.
Sex‐ and time‐specific parental effects of warming on reproduction and offspring quality in a coral reef fish
title Sex‐ and time‐specific parental effects of warming on reproduction and offspring quality in a coral reef fish
title_full Sex‐ and time‐specific parental effects of warming on reproduction and offspring quality in a coral reef fish
title_fullStr Sex‐ and time‐specific parental effects of warming on reproduction and offspring quality in a coral reef fish
title_full_unstemmed Sex‐ and time‐specific parental effects of warming on reproduction and offspring quality in a coral reef fish
title_short Sex‐ and time‐specific parental effects of warming on reproduction and offspring quality in a coral reef fish
title_sort sex‐ and time‐specific parental effects of warming on reproduction and offspring quality in a coral reef fish
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8061261/
https://www.ncbi.nlm.nih.gov/pubmed/33897826
http://dx.doi.org/10.1111/eva.13187
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