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Male frequency in Caenorhabditis elegans increases in response to chronic irradiation

Outcrossing can be advantageous in a changing environment because it promotes the purge of deleterious mutations and increases the genetic diversity within a population, which may improve population persistence and evolutionary potential. Some species may, therefore, switch their reproductive mode f...

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Autores principales: Quevarec, Loïc, Réale, Denis, Dufourcq‐Sekatcheff, Elizabeth, Car, Clément, Armant, Olivier, Dubourg, Nicolas, Adam‐Guillermin, Christelle, Bonzom, Jean‐Marc
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/PMC9488675/
https://www.ncbi.nlm.nih.gov/pubmed/36187185
http://dx.doi.org/10.1111/eva.13420
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author Quevarec, Loïc
Réale, Denis
Dufourcq‐Sekatcheff, Elizabeth
Car, Clément
Armant, Olivier
Dubourg, Nicolas
Adam‐Guillermin, Christelle
Bonzom, Jean‐Marc
author_facet Quevarec, Loïc
Réale, Denis
Dufourcq‐Sekatcheff, Elizabeth
Car, Clément
Armant, Olivier
Dubourg, Nicolas
Adam‐Guillermin, Christelle
Bonzom, Jean‐Marc
author_sort Quevarec, Loïc
collection PubMed
description Outcrossing can be advantageous in a changing environment because it promotes the purge of deleterious mutations and increases the genetic diversity within a population, which may improve population persistence and evolutionary potential. Some species may, therefore, switch their reproductive mode from inbreeding to outcrossing when under environmental stress. This switch may have consequences on the demographic dynamics and evolutionary trajectory of populations. For example, it may directly influence the sex ratio of a population. However, much remains to be discovered about the mechanisms and evolutionary implications of sex ratio changes in a population in response to environmental stress. Populations of the androdioecious nematode Caenorhabditis elegans, are composed of selfing hermaphrodites and rare males. Here, we investigate the changes in the sex ratio of C. elegans populations exposed to radioactive pollution for 60 days or around 20 generations. We experimentally exposed populations to three levels of ionizing radiation (i.e., 0, 1.4, and 50 mGy.h(−1)). We then performed reciprocal transplant experiments to evaluate genetic divergence between populations submitted to different treatments. Finally, we used a mathematical model to examine the evolutionary mechanisms that could be responsible for the change in sex ratio. Our results showed an increase in male frequency in irradiated populations, and this effect increased with the dose rate. The model showed that an increase in male fertilization success or a decrease in hermaphrodite self‐fertilization could explain this increase in the frequency of males. Moreover, males persisted in populations after transplant back into the control conditions. These results suggested selection favoring outcrossing under irradiation conditions. This study shows that ionizing radiation can sustainably alter the reproductive strategy of a population, likely impacting its long‐term evolutionary history. This study highlights the need to evaluate the impact of pollutants on the reproductive strategies of populations when assessing the ecological risks.
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spelling pubmed-94886752022-09-30 Male frequency in Caenorhabditis elegans increases in response to chronic irradiation Quevarec, Loïc Réale, Denis Dufourcq‐Sekatcheff, Elizabeth Car, Clément Armant, Olivier Dubourg, Nicolas Adam‐Guillermin, Christelle Bonzom, Jean‐Marc Evol Appl Original Articles Outcrossing can be advantageous in a changing environment because it promotes the purge of deleterious mutations and increases the genetic diversity within a population, which may improve population persistence and evolutionary potential. Some species may, therefore, switch their reproductive mode from inbreeding to outcrossing when under environmental stress. This switch may have consequences on the demographic dynamics and evolutionary trajectory of populations. For example, it may directly influence the sex ratio of a population. However, much remains to be discovered about the mechanisms and evolutionary implications of sex ratio changes in a population in response to environmental stress. Populations of the androdioecious nematode Caenorhabditis elegans, are composed of selfing hermaphrodites and rare males. Here, we investigate the changes in the sex ratio of C. elegans populations exposed to radioactive pollution for 60 days or around 20 generations. We experimentally exposed populations to three levels of ionizing radiation (i.e., 0, 1.4, and 50 mGy.h(−1)). We then performed reciprocal transplant experiments to evaluate genetic divergence between populations submitted to different treatments. Finally, we used a mathematical model to examine the evolutionary mechanisms that could be responsible for the change in sex ratio. Our results showed an increase in male frequency in irradiated populations, and this effect increased with the dose rate. The model showed that an increase in male fertilization success or a decrease in hermaphrodite self‐fertilization could explain this increase in the frequency of males. Moreover, males persisted in populations after transplant back into the control conditions. These results suggested selection favoring outcrossing under irradiation conditions. This study shows that ionizing radiation can sustainably alter the reproductive strategy of a population, likely impacting its long‐term evolutionary history. This study highlights the need to evaluate the impact of pollutants on the reproductive strategies of populations when assessing the ecological risks. John Wiley and Sons Inc. 2022-09-02 /pmc/articles/PMC9488675/ /pubmed/36187185 http://dx.doi.org/10.1111/eva.13420 Text en © 2022 The Authors. Evolutionary Applications 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 Original Articles
Quevarec, Loïc
Réale, Denis
Dufourcq‐Sekatcheff, Elizabeth
Car, Clément
Armant, Olivier
Dubourg, Nicolas
Adam‐Guillermin, Christelle
Bonzom, Jean‐Marc
Male frequency in Caenorhabditis elegans increases in response to chronic irradiation
title Male frequency in Caenorhabditis elegans increases in response to chronic irradiation
title_full Male frequency in Caenorhabditis elegans increases in response to chronic irradiation
title_fullStr Male frequency in Caenorhabditis elegans increases in response to chronic irradiation
title_full_unstemmed Male frequency in Caenorhabditis elegans increases in response to chronic irradiation
title_short Male frequency in Caenorhabditis elegans increases in response to chronic irradiation
title_sort male frequency in caenorhabditis elegans increases in response to chronic irradiation
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9488675/
https://www.ncbi.nlm.nih.gov/pubmed/36187185
http://dx.doi.org/10.1111/eva.13420
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