Parents exposed to warming produce offspring lower in weight and condition

Abstract The parental environment can alter offspring phenotypes via the transfer of non‐genetic information. Parental effects may be viewed as an extension of (within‐generation) phenotypic plasticity. Smaller size, poorer physical condition, and skewed sex ratios are common responses of organisms...

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Main Authors: Rachel K. Spinks, Jennifer M. Donelson, Lucrezia C. Bonzi, Timothy Ravasi, Philip L. Munday
Format: Article
Language:English
Published: Wiley 2022-07-01
Series:Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1002/ece3.9044
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author Rachel K. Spinks
Jennifer M. Donelson
Lucrezia C. Bonzi
Timothy Ravasi
Philip L. Munday
author_facet Rachel K. Spinks
Jennifer M. Donelson
Lucrezia C. Bonzi
Timothy Ravasi
Philip L. Munday
author_sort Rachel K. Spinks
collection DOAJ
description Abstract The parental environment can alter offspring phenotypes via the transfer of non‐genetic information. Parental effects may be viewed as an extension of (within‐generation) phenotypic plasticity. Smaller size, poorer physical condition, and skewed sex ratios are common responses of organisms to global warming, yet whether parental effects alleviate, exacerbate, or have no impact on these responses has not been widely tested. Further, the relative non‐genetic influence of mothers and fathers and ontogenetic timing of parental exposure to warming on offspring phenotypes is poorly understood. Here, we tested how maternal, paternal, and biparental exposure of a coral reef fish (Acanthochromis polyacanthus) to elevated temperature (+1.5°C) at different ontogenetic stages (development vs reproduction) influences offspring length, weight, condition, and sex. Fish were reared across two generations in present‐day and projected ocean warming in a full factorial design. As expected, offspring of parents exposed to present‐day control temperature that were reared in warmer water were shorter than their siblings reared in control temperature; however, within‐generation plasticity allowed maintenance of weight, resulting in a higher body condition. Parental exposure to warming, irrespective of ontogenetic timing and sex, resulted in decreased weight and condition in all offspring rearing temperatures. By contrast, offspring sex ratios were not strongly influenced by their rearing temperature or that of their parents. Together, our results reveal that phenotypic plasticity may help coral reef fishes maintain performance in a warm ocean within a generation, but could exacerbate the negative effects of warming between generations, regardless of when mothers and fathers are exposed to warming. Alternatively, the multigenerational impact on offspring weight and condition may be a necessary cost to adapt metabolism to increasing temperatures. This research highlights the importance of examining phenotypic plasticity within and between generations across a range of traits to accurately predict how organisms will respond to climate change.
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spelling doaj.art-58cf68b04f4543ff9321f72a7442ada12022-12-22T00:58:58ZengWileyEcology and Evolution2045-77582022-07-01127n/an/a10.1002/ece3.9044Parents exposed to warming produce offspring lower in weight and conditionRachel K. Spinks0Jennifer M. Donelson1Lucrezia C. Bonzi2Timothy Ravasi3Philip L. Munday4ARC 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 AustraliaDivision of Biological and Environmental Sciences and Engineering, Red Sea Research Center 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 AustraliaAbstract The parental environment can alter offspring phenotypes via the transfer of non‐genetic information. Parental effects may be viewed as an extension of (within‐generation) phenotypic plasticity. Smaller size, poorer physical condition, and skewed sex ratios are common responses of organisms to global warming, yet whether parental effects alleviate, exacerbate, or have no impact on these responses has not been widely tested. Further, the relative non‐genetic influence of mothers and fathers and ontogenetic timing of parental exposure to warming on offspring phenotypes is poorly understood. Here, we tested how maternal, paternal, and biparental exposure of a coral reef fish (Acanthochromis polyacanthus) to elevated temperature (+1.5°C) at different ontogenetic stages (development vs reproduction) influences offspring length, weight, condition, and sex. Fish were reared across two generations in present‐day and projected ocean warming in a full factorial design. As expected, offspring of parents exposed to present‐day control temperature that were reared in warmer water were shorter than their siblings reared in control temperature; however, within‐generation plasticity allowed maintenance of weight, resulting in a higher body condition. Parental exposure to warming, irrespective of ontogenetic timing and sex, resulted in decreased weight and condition in all offspring rearing temperatures. By contrast, offspring sex ratios were not strongly influenced by their rearing temperature or that of their parents. Together, our results reveal that phenotypic plasticity may help coral reef fishes maintain performance in a warm ocean within a generation, but could exacerbate the negative effects of warming between generations, regardless of when mothers and fathers are exposed to warming. Alternatively, the multigenerational impact on offspring weight and condition may be a necessary cost to adapt metabolism to increasing temperatures. This research highlights the importance of examining phenotypic plasticity within and between generations across a range of traits to accurately predict how organisms will respond to climate change.https://doi.org/10.1002/ece3.9044climate changecoral reef fishmaternal effectsontogenetic timingpaternal effectstransgenerational plasticity
spellingShingle Rachel K. Spinks
Jennifer M. Donelson
Lucrezia C. Bonzi
Timothy Ravasi
Philip L. Munday
Parents exposed to warming produce offspring lower in weight and condition
Ecology and Evolution
climate change
coral reef fish
maternal effects
ontogenetic timing
paternal effects
transgenerational plasticity
title Parents exposed to warming produce offspring lower in weight and condition
title_full Parents exposed to warming produce offspring lower in weight and condition
title_fullStr Parents exposed to warming produce offspring lower in weight and condition
title_full_unstemmed Parents exposed to warming produce offspring lower in weight and condition
title_short Parents exposed to warming produce offspring lower in weight and condition
title_sort parents exposed to warming produce offspring lower in weight and condition
topic climate change
coral reef fish
maternal effects
ontogenetic timing
paternal effects
transgenerational plasticity
url https://doi.org/10.1002/ece3.9044
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AT lucreziacbonzi parentsexposedtowarmingproduceoffspringlowerinweightandcondition
AT timothyravasi parentsexposedtowarmingproduceoffspringlowerinweightandcondition
AT philiplmunday parentsexposedtowarmingproduceoffspringlowerinweightandcondition