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Developmental plasticity in thermal tolerance: Ontogenetic variation, persistence, and future directions

Understanding the factors affecting thermal tolerance is crucial for predicting the impact climate change will have on ectotherms. However, the role developmental plasticity plays in allowing populations to cope with thermal extremes is poorly understood. Here, we meta‐analyse how thermal tolerance...

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Autores principales: Pottier, Patrice, Burke, Samantha, Zhang, Rose Y., Noble, Daniel W. A., Schwanz, Lisa E., Drobniak, Szymon M., Nakagawa, Shinichi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9804923/
https://www.ncbi.nlm.nih.gov/pubmed/36006770
http://dx.doi.org/10.1111/ele.14083
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author Pottier, Patrice
Burke, Samantha
Zhang, Rose Y.
Noble, Daniel W. A.
Schwanz, Lisa E.
Drobniak, Szymon M.
Nakagawa, Shinichi
author_facet Pottier, Patrice
Burke, Samantha
Zhang, Rose Y.
Noble, Daniel W. A.
Schwanz, Lisa E.
Drobniak, Szymon M.
Nakagawa, Shinichi
author_sort Pottier, Patrice
collection PubMed
description Understanding the factors affecting thermal tolerance is crucial for predicting the impact climate change will have on ectotherms. However, the role developmental plasticity plays in allowing populations to cope with thermal extremes is poorly understood. Here, we meta‐analyse how thermal tolerance is initially and persistently impacted by early (embryonic and juvenile) thermal environments by using data from 150 experimental studies on 138 ectothermic species. Thermal tolerance only increased by 0.13°C per 1°C change in developmental temperature and substantial variation in plasticity (~36%) was the result of shared evolutionary history and species ecology. Aquatic ectotherms were more than three times as plastic as terrestrial ectotherms. Notably, embryos expressed weaker but more heterogenous plasticity than older life stages, with numerous responses appearing as non‐adaptive. While developmental temperatures did not have persistent effects on thermal tolerance overall, persistent effects were vastly under‐studied, and their direction and magnitude varied with ontogeny. Embryonic stages may represent a critical window of vulnerability to changing environments and we urge researchers to consider early life stages when assessing the climate vulnerability of ectotherms. Overall, our synthesis suggests that developmental changes in thermal tolerance rarely reach levels of perfect compensation and may provide limited benefit in changing environments.
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spelling pubmed-98049232023-01-06 Developmental plasticity in thermal tolerance: Ontogenetic variation, persistence, and future directions Pottier, Patrice Burke, Samantha Zhang, Rose Y. Noble, Daniel W. A. Schwanz, Lisa E. Drobniak, Szymon M. Nakagawa, Shinichi Ecol Lett Synthesis Understanding the factors affecting thermal tolerance is crucial for predicting the impact climate change will have on ectotherms. However, the role developmental plasticity plays in allowing populations to cope with thermal extremes is poorly understood. Here, we meta‐analyse how thermal tolerance is initially and persistently impacted by early (embryonic and juvenile) thermal environments by using data from 150 experimental studies on 138 ectothermic species. Thermal tolerance only increased by 0.13°C per 1°C change in developmental temperature and substantial variation in plasticity (~36%) was the result of shared evolutionary history and species ecology. Aquatic ectotherms were more than three times as plastic as terrestrial ectotherms. Notably, embryos expressed weaker but more heterogenous plasticity than older life stages, with numerous responses appearing as non‐adaptive. While developmental temperatures did not have persistent effects on thermal tolerance overall, persistent effects were vastly under‐studied, and their direction and magnitude varied with ontogeny. Embryonic stages may represent a critical window of vulnerability to changing environments and we urge researchers to consider early life stages when assessing the climate vulnerability of ectotherms. Overall, our synthesis suggests that developmental changes in thermal tolerance rarely reach levels of perfect compensation and may provide limited benefit in changing environments. John Wiley and Sons Inc. 2022-08-25 2022-10 /pmc/articles/PMC9804923/ /pubmed/36006770 http://dx.doi.org/10.1111/ele.14083 Text en © 2022 The Authors. Ecology Letters 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 Synthesis
Pottier, Patrice
Burke, Samantha
Zhang, Rose Y.
Noble, Daniel W. A.
Schwanz, Lisa E.
Drobniak, Szymon M.
Nakagawa, Shinichi
Developmental plasticity in thermal tolerance: Ontogenetic variation, persistence, and future directions
title Developmental plasticity in thermal tolerance: Ontogenetic variation, persistence, and future directions
title_full Developmental plasticity in thermal tolerance: Ontogenetic variation, persistence, and future directions
title_fullStr Developmental plasticity in thermal tolerance: Ontogenetic variation, persistence, and future directions
title_full_unstemmed Developmental plasticity in thermal tolerance: Ontogenetic variation, persistence, and future directions
title_short Developmental plasticity in thermal tolerance: Ontogenetic variation, persistence, and future directions
title_sort developmental plasticity in thermal tolerance: ontogenetic variation, persistence, and future directions
topic Synthesis
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9804923/
https://www.ncbi.nlm.nih.gov/pubmed/36006770
http://dx.doi.org/10.1111/ele.14083
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