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

Abstract 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 warm...

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Main Authors: Rachel K. Spinks, Lucrezia C. Bonzi, Timothy Ravasi, Philip L. Munday, Jennifer M. Donelson
Format: Article
Language:English
Published: Wiley 2021-04-01
Series:Evolutionary Applications
Subjects:
Online Access:https://doi.org/10.1111/eva.13187
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author Rachel K. Spinks
Lucrezia C. Bonzi
Timothy Ravasi
Philip L. Munday
Jennifer M. Donelson
author_facet Rachel K. Spinks
Lucrezia C. Bonzi
Timothy Ravasi
Philip L. Munday
Jennifer M. Donelson
author_sort Rachel K. Spinks
collection DOAJ
description Abstract 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 doaj.art-431c5abf705149e6b1aa19c41ef6188a2022-12-21T17:14:59ZengWileyEvolutionary Applications1752-45712021-04-011441145115810.1111/eva.13187Sex‐ and time‐specific parental effects of warming on reproduction and offspring quality in a coral reef fishRachel K. Spinks0Lucrezia C. Bonzi1Timothy Ravasi2Philip L. Munday3Jennifer M. Donelson4ARC Centre of Excellence for Coral Reef Studies James Cook University Townsville Queensland AustraliaRed Sea Research Center Division of Biological and Environmental Sciences and Engineering King Abdullah University of Science and Technology Thuwal Saudi ArabiaARC Centre of Excellence for Coral Reef Studies James Cook University Townsville Queensland AustraliaARC Centre of Excellence for Coral Reef Studies James Cook University Townsville Queensland AustraliaARC Centre of Excellence for Coral Reef Studies James Cook University Townsville Queensland AustraliaAbstract 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.https://doi.org/10.1111/eva.13187climate changedevelopmental plasticitymaternal effectspaternal effectsphenotypic plasticitytiming of exposure
spellingShingle Rachel K. Spinks
Lucrezia C. Bonzi
Timothy Ravasi
Philip L. Munday
Jennifer M. Donelson
Sex‐ and time‐specific parental effects of warming on reproduction and offspring quality in a coral reef fish
Evolutionary Applications
climate change
developmental plasticity
maternal effects
paternal effects
phenotypic plasticity
timing of exposure
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 climate change
developmental plasticity
maternal effects
paternal effects
phenotypic plasticity
timing of exposure
url https://doi.org/10.1111/eva.13187
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