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Timing of increased temperature sensitivity coincides with nervous system development in winter moth embryos

Climate change is rapidly altering the environment and many species will need to genetically adapt their seasonal timing to keep up with these changes. Insect development rate is largely influenced by temperature, but we know little about the mechanisms underlying the temperature sensitivity of deve...

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Autores principales: van Dis, Natalie E., van der Zee, Maurijn, Hut, Roelof A., Wertheim, Bregje, Visser, Marcel E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8443866/
https://www.ncbi.nlm.nih.gov/pubmed/34378047
http://dx.doi.org/10.1242/jeb.242554
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author van Dis, Natalie E.
van der Zee, Maurijn
Hut, Roelof A.
Wertheim, Bregje
Visser, Marcel E.
author_facet van Dis, Natalie E.
van der Zee, Maurijn
Hut, Roelof A.
Wertheim, Bregje
Visser, Marcel E.
author_sort van Dis, Natalie E.
collection PubMed
description Climate change is rapidly altering the environment and many species will need to genetically adapt their seasonal timing to keep up with these changes. Insect development rate is largely influenced by temperature, but we know little about the mechanisms underlying the temperature sensitivity of development. Here, we investigate seasonal timing of egg hatching in the winter moth, one of the few species which has been found to genetically adapt to climate change, likely through selection on temperature sensitivity of egg development rate. To study when during development winter moth embryos are most sensitive to changes in ambient temperature, we gave eggs an increase or decrease in temperature at different moments during their development. We measured their developmental progression and time of egg hatching, and used fluorescence microscopy to construct a timeline of embryonic development for the winter moth. We found that egg development rate responded more strongly to temperature once embryos were in the fully extended germband stage. This is the phylotypic stage at which all insect embryos have developed a rudimentary nervous system. Furthermore, at this stage, timing of ecdysone signaling determines developmental progression, which could act as an environment dependent gateway. Intriguingly, this may suggest that, from the phylotypic stage onward, insect embryos can start to integrate internal and environmental stimuli to actively regulate important developmental processes. As we found evidence that there is genetic variation for temperature sensitivity of egg development rate in our study population, such regulation could be a target of selection imposed by climate change.
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spelling pubmed-84438662021-09-21 Timing of increased temperature sensitivity coincides with nervous system development in winter moth embryos van Dis, Natalie E. van der Zee, Maurijn Hut, Roelof A. Wertheim, Bregje Visser, Marcel E. J Exp Biol Research Article Climate change is rapidly altering the environment and many species will need to genetically adapt their seasonal timing to keep up with these changes. Insect development rate is largely influenced by temperature, but we know little about the mechanisms underlying the temperature sensitivity of development. Here, we investigate seasonal timing of egg hatching in the winter moth, one of the few species which has been found to genetically adapt to climate change, likely through selection on temperature sensitivity of egg development rate. To study when during development winter moth embryos are most sensitive to changes in ambient temperature, we gave eggs an increase or decrease in temperature at different moments during their development. We measured their developmental progression and time of egg hatching, and used fluorescence microscopy to construct a timeline of embryonic development for the winter moth. We found that egg development rate responded more strongly to temperature once embryos were in the fully extended germband stage. This is the phylotypic stage at which all insect embryos have developed a rudimentary nervous system. Furthermore, at this stage, timing of ecdysone signaling determines developmental progression, which could act as an environment dependent gateway. Intriguingly, this may suggest that, from the phylotypic stage onward, insect embryos can start to integrate internal and environmental stimuli to actively regulate important developmental processes. As we found evidence that there is genetic variation for temperature sensitivity of egg development rate in our study population, such regulation could be a target of selection imposed by climate change. The Company of Biologists Ltd 2021-09-01 /pmc/articles/PMC8443866/ /pubmed/34378047 http://dx.doi.org/10.1242/jeb.242554 Text en © 2021. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
van Dis, Natalie E.
van der Zee, Maurijn
Hut, Roelof A.
Wertheim, Bregje
Visser, Marcel E.
Timing of increased temperature sensitivity coincides with nervous system development in winter moth embryos
title Timing of increased temperature sensitivity coincides with nervous system development in winter moth embryos
title_full Timing of increased temperature sensitivity coincides with nervous system development in winter moth embryos
title_fullStr Timing of increased temperature sensitivity coincides with nervous system development in winter moth embryos
title_full_unstemmed Timing of increased temperature sensitivity coincides with nervous system development in winter moth embryos
title_short Timing of increased temperature sensitivity coincides with nervous system development in winter moth embryos
title_sort timing of increased temperature sensitivity coincides with nervous system development in winter moth embryos
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8443866/
https://www.ncbi.nlm.nih.gov/pubmed/34378047
http://dx.doi.org/10.1242/jeb.242554
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