Cargando…

Thermal conditioning of quail embryos has transgenerational and reversible long-term effects

BACKGROUND: In the current context of global warming, thermal manipulation of avian embryos has received increasing attention as a strategy to promote heat tolerance in avian species by simply increasing the egg incubation temperature. However, because of their likely epigenetic origin, thermal mani...

Descripción completa

Detalles Bibliográficos
Autores principales: Vitorino Carvalho, Anaïs, Hennequet-Antier, Christelle, Rouger, Romuald, Delaveau, Joël, Bordeau, Thierry, Crochet, Sabine, Couroussé, Nathalie, Pitel, Frederique, Collin, Anne, Coustham, Vincent
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10546792/
https://www.ncbi.nlm.nih.gov/pubmed/37784159
http://dx.doi.org/10.1186/s40104-023-00924-2
_version_ 1785114935378837504
author Vitorino Carvalho, Anaïs
Hennequet-Antier, Christelle
Rouger, Romuald
Delaveau, Joël
Bordeau, Thierry
Crochet, Sabine
Couroussé, Nathalie
Pitel, Frederique
Collin, Anne
Coustham, Vincent
author_facet Vitorino Carvalho, Anaïs
Hennequet-Antier, Christelle
Rouger, Romuald
Delaveau, Joël
Bordeau, Thierry
Crochet, Sabine
Couroussé, Nathalie
Pitel, Frederique
Collin, Anne
Coustham, Vincent
author_sort Vitorino Carvalho, Anaïs
collection PubMed
description BACKGROUND: In the current context of global warming, thermal manipulation of avian embryos has received increasing attention as a strategy to promote heat tolerance in avian species by simply increasing the egg incubation temperature. However, because of their likely epigenetic origin, thermal manipulation effects may last more than one generation with consequences for the poultry industry. In this work, a multigenerational and transgenerational analysis of thermal manipulation during embryogenesis was performed to uncover the long-term effects of such procedure. RESULTS: Thermal manipulation repeated during 4 generations had an effect on hatchability, body weight, and weight of eggs laid in Japanese quails, with some effects increasing in importance over generations. Moreover, the effects on body weight and egg weight could be transmitted transgenerationally, suggesting non-genetic inheritance mechanisms. This hypothesis is reinforced by the observed reversion of the effect on growth after five unexposed generations. Interestingly, a beneficial effect of thermal manipulation on heat tolerance was observed a few days after hatching, but this effect was not transgenerational. CONCLUSIONS: Our multigenerational study showed that thermal conditioning of quail embryos has a beneficial effect on post-hatch heat tolerance hampered by transgenerational but reversible defects on growth. Assuming that no genetic variability underlies these changes, this study provides the first demonstration of epigenetic inheritance of traits induced by environmental temperature modification associated with long-term impacts in an avian species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40104-023-00924-2.
format Online
Article
Text
id pubmed-10546792
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-105467922023-10-04 Thermal conditioning of quail embryos has transgenerational and reversible long-term effects Vitorino Carvalho, Anaïs Hennequet-Antier, Christelle Rouger, Romuald Delaveau, Joël Bordeau, Thierry Crochet, Sabine Couroussé, Nathalie Pitel, Frederique Collin, Anne Coustham, Vincent J Anim Sci Biotechnol Research BACKGROUND: In the current context of global warming, thermal manipulation of avian embryos has received increasing attention as a strategy to promote heat tolerance in avian species by simply increasing the egg incubation temperature. However, because of their likely epigenetic origin, thermal manipulation effects may last more than one generation with consequences for the poultry industry. In this work, a multigenerational and transgenerational analysis of thermal manipulation during embryogenesis was performed to uncover the long-term effects of such procedure. RESULTS: Thermal manipulation repeated during 4 generations had an effect on hatchability, body weight, and weight of eggs laid in Japanese quails, with some effects increasing in importance over generations. Moreover, the effects on body weight and egg weight could be transmitted transgenerationally, suggesting non-genetic inheritance mechanisms. This hypothesis is reinforced by the observed reversion of the effect on growth after five unexposed generations. Interestingly, a beneficial effect of thermal manipulation on heat tolerance was observed a few days after hatching, but this effect was not transgenerational. CONCLUSIONS: Our multigenerational study showed that thermal conditioning of quail embryos has a beneficial effect on post-hatch heat tolerance hampered by transgenerational but reversible defects on growth. Assuming that no genetic variability underlies these changes, this study provides the first demonstration of epigenetic inheritance of traits induced by environmental temperature modification associated with long-term impacts in an avian species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40104-023-00924-2. BioMed Central 2023-10-03 /pmc/articles/PMC10546792/ /pubmed/37784159 http://dx.doi.org/10.1186/s40104-023-00924-2 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Vitorino Carvalho, Anaïs
Hennequet-Antier, Christelle
Rouger, Romuald
Delaveau, Joël
Bordeau, Thierry
Crochet, Sabine
Couroussé, Nathalie
Pitel, Frederique
Collin, Anne
Coustham, Vincent
Thermal conditioning of quail embryos has transgenerational and reversible long-term effects
title Thermal conditioning of quail embryos has transgenerational and reversible long-term effects
title_full Thermal conditioning of quail embryos has transgenerational and reversible long-term effects
title_fullStr Thermal conditioning of quail embryos has transgenerational and reversible long-term effects
title_full_unstemmed Thermal conditioning of quail embryos has transgenerational and reversible long-term effects
title_short Thermal conditioning of quail embryos has transgenerational and reversible long-term effects
title_sort thermal conditioning of quail embryos has transgenerational and reversible long-term effects
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10546792/
https://www.ncbi.nlm.nih.gov/pubmed/37784159
http://dx.doi.org/10.1186/s40104-023-00924-2
work_keys_str_mv AT vitorinocarvalhoanais thermalconditioningofquailembryoshastransgenerationalandreversiblelongtermeffects
AT hennequetantierchristelle thermalconditioningofquailembryoshastransgenerationalandreversiblelongtermeffects
AT rougerromuald thermalconditioningofquailembryoshastransgenerationalandreversiblelongtermeffects
AT delaveaujoel thermalconditioningofquailembryoshastransgenerationalandreversiblelongtermeffects
AT bordeauthierry thermalconditioningofquailembryoshastransgenerationalandreversiblelongtermeffects
AT crochetsabine thermalconditioningofquailembryoshastransgenerationalandreversiblelongtermeffects
AT couroussenathalie thermalconditioningofquailembryoshastransgenerationalandreversiblelongtermeffects
AT pitelfrederique thermalconditioningofquailembryoshastransgenerationalandreversiblelongtermeffects
AT collinanne thermalconditioningofquailembryoshastransgenerationalandreversiblelongtermeffects
AT cousthamvincent thermalconditioningofquailembryoshastransgenerationalandreversiblelongtermeffects