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Population transcriptogenomics highlights impaired metabolism and small population sizes in tree frogs living in the Chernobyl Exclusion Zone

BACKGROUND: Individual functional modifications shape the ability of wildlife populations to cope with anthropogenic environmental changes. But instead of adaptive response, human-altered environments can generate a succession of deleterious functional changes leading to the extinction of the popula...

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Autores principales: Car, Clément, Gilles, André, Goujon, Elen, Muller, Marie-Laure Delignette, Camoin, Luc, Frelon, Sandrine, Burraco, Pablo, Granjeaud, Samuel, Baudelet, Emilie, Audebert, Stéphane, Orizaola, Germán, Armengaud, Jean, Tenenhaus, Arthur, Garali, Imène, Bonzom, Jean-Marc, Armant, Olivier
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10391870/
https://www.ncbi.nlm.nih.gov/pubmed/37525144
http://dx.doi.org/10.1186/s12915-023-01659-2
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author Car, Clément
Gilles, André
Goujon, Elen
Muller, Marie-Laure Delignette
Camoin, Luc
Frelon, Sandrine
Burraco, Pablo
Granjeaud, Samuel
Baudelet, Emilie
Audebert, Stéphane
Orizaola, Germán
Armengaud, Jean
Tenenhaus, Arthur
Garali, Imène
Bonzom, Jean-Marc
Armant, Olivier
author_facet Car, Clément
Gilles, André
Goujon, Elen
Muller, Marie-Laure Delignette
Camoin, Luc
Frelon, Sandrine
Burraco, Pablo
Granjeaud, Samuel
Baudelet, Emilie
Audebert, Stéphane
Orizaola, Germán
Armengaud, Jean
Tenenhaus, Arthur
Garali, Imène
Bonzom, Jean-Marc
Armant, Olivier
author_sort Car, Clément
collection PubMed
description BACKGROUND: Individual functional modifications shape the ability of wildlife populations to cope with anthropogenic environmental changes. But instead of adaptive response, human-altered environments can generate a succession of deleterious functional changes leading to the extinction of the population. To study how persistent anthropogenic changes impacted local species’ population status, we characterised population structure, genetic diversity and individual response of gene expression in the tree frog Hyla orientalis along a gradient of radioactive contamination around the Chernobyl nuclear power plant. RESULTS: We detected lower effective population size in populations most exposed to ionizing radiation in the Chernobyl Exclusion Zone that is not compensated by migrations from surrounding areas. We also highlighted a decreased body condition of frogs living in the most contaminated area, a distinctive transcriptomics signature and stop-gained mutations in genes involved in energy metabolism. While the association with dose will remain correlational until further experiments, a body of evidence suggests the direct or indirect involvement of radiation exposure in these changes. CONCLUSIONS: Despite ongoing migration and lower total dose rates absorbed than at the time of the accident, our results demonstrate that Hyla orientalis specimens living in the Chernobyl Exclusion Zone are still undergoing deleterious changes, emphasizing the long-term impacts of the nuclear disaster. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01659-2.
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spelling pubmed-103918702023-08-02 Population transcriptogenomics highlights impaired metabolism and small population sizes in tree frogs living in the Chernobyl Exclusion Zone Car, Clément Gilles, André Goujon, Elen Muller, Marie-Laure Delignette Camoin, Luc Frelon, Sandrine Burraco, Pablo Granjeaud, Samuel Baudelet, Emilie Audebert, Stéphane Orizaola, Germán Armengaud, Jean Tenenhaus, Arthur Garali, Imène Bonzom, Jean-Marc Armant, Olivier BMC Biol Research Article BACKGROUND: Individual functional modifications shape the ability of wildlife populations to cope with anthropogenic environmental changes. But instead of adaptive response, human-altered environments can generate a succession of deleterious functional changes leading to the extinction of the population. To study how persistent anthropogenic changes impacted local species’ population status, we characterised population structure, genetic diversity and individual response of gene expression in the tree frog Hyla orientalis along a gradient of radioactive contamination around the Chernobyl nuclear power plant. RESULTS: We detected lower effective population size in populations most exposed to ionizing radiation in the Chernobyl Exclusion Zone that is not compensated by migrations from surrounding areas. We also highlighted a decreased body condition of frogs living in the most contaminated area, a distinctive transcriptomics signature and stop-gained mutations in genes involved in energy metabolism. While the association with dose will remain correlational until further experiments, a body of evidence suggests the direct or indirect involvement of radiation exposure in these changes. CONCLUSIONS: Despite ongoing migration and lower total dose rates absorbed than at the time of the accident, our results demonstrate that Hyla orientalis specimens living in the Chernobyl Exclusion Zone are still undergoing deleterious changes, emphasizing the long-term impacts of the nuclear disaster. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01659-2. BioMed Central 2023-07-31 /pmc/articles/PMC10391870/ /pubmed/37525144 http://dx.doi.org/10.1186/s12915-023-01659-2 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 Article
Car, Clément
Gilles, André
Goujon, Elen
Muller, Marie-Laure Delignette
Camoin, Luc
Frelon, Sandrine
Burraco, Pablo
Granjeaud, Samuel
Baudelet, Emilie
Audebert, Stéphane
Orizaola, Germán
Armengaud, Jean
Tenenhaus, Arthur
Garali, Imène
Bonzom, Jean-Marc
Armant, Olivier
Population transcriptogenomics highlights impaired metabolism and small population sizes in tree frogs living in the Chernobyl Exclusion Zone
title Population transcriptogenomics highlights impaired metabolism and small population sizes in tree frogs living in the Chernobyl Exclusion Zone
title_full Population transcriptogenomics highlights impaired metabolism and small population sizes in tree frogs living in the Chernobyl Exclusion Zone
title_fullStr Population transcriptogenomics highlights impaired metabolism and small population sizes in tree frogs living in the Chernobyl Exclusion Zone
title_full_unstemmed Population transcriptogenomics highlights impaired metabolism and small population sizes in tree frogs living in the Chernobyl Exclusion Zone
title_short Population transcriptogenomics highlights impaired metabolism and small population sizes in tree frogs living in the Chernobyl Exclusion Zone
title_sort population transcriptogenomics highlights impaired metabolism and small population sizes in tree frogs living in the chernobyl exclusion zone
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10391870/
https://www.ncbi.nlm.nih.gov/pubmed/37525144
http://dx.doi.org/10.1186/s12915-023-01659-2
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