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Genotype‐by‐environment interactions drive the maintenance of genetic variation in a Salmo trutta L. hybrid zone

Allopatric gene pools can evolve in different directions through adaptive and nonadaptive processes and are therefore a source of intraspecific diversity. The connection of these previously isolated gene pools through human intervention can lead to intraspecific diversity loss, through extirpation o...

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Autores principales: Folio, Dorinda Marie, Gil, Jordi, Caudron, Arnaud, Labonne, Jacques
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8591331/
https://www.ncbi.nlm.nih.gov/pubmed/34815748
http://dx.doi.org/10.1111/eva.13307
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author Folio, Dorinda Marie
Gil, Jordi
Caudron, Arnaud
Labonne, Jacques
author_facet Folio, Dorinda Marie
Gil, Jordi
Caudron, Arnaud
Labonne, Jacques
author_sort Folio, Dorinda Marie
collection PubMed
description Allopatric gene pools can evolve in different directions through adaptive and nonadaptive processes and are therefore a source of intraspecific diversity. The connection of these previously isolated gene pools through human intervention can lead to intraspecific diversity loss, through extirpation of native populations or hybridization. However, the mechanisms leading to these situations are not always explicitly documented and are thus rarely used to manage intraspecific diversity. In particular, genotype‐by‐environment (GxE) interactions can drive postzygotic reproductive isolation mechanisms that may result in a mosaic of diversity patterns, depending on the local environment. We test this hypothesis using a salmonid species (Salmo trutta) in the Mediterranean (MED) area, where intensive stocking from non‐native Atlantic (ATL) origins has led to various outcomes of hybridization with the native MED lineage, going from MED resilience to total extirpation via full hybridization. We investigate patterns of offspring survival at egg stage in natural environments, based on parental genotypes in interaction with river temperature, to detect potential GxE interactions. Our results show a strong influence of maternal GxE interaction on embryonic survival, mediated by maternal effect through egg size, and a weak influence of paternal GxE interaction. In particular, when egg size is large and temperature is cold, the survival rate of offspring originating from MED females is three times higher than that of ATL females’ offspring. Because river temperatures show contrast at small scale, this cold adaptation for MED females’ offspring constitutes a potent postzygotic mechanism to explain small‐scale spatial heterogeneity in diversity observed in MED areas where ATL fish have been stocked. It also indicates that management efforts could be specifically targeted at the environments that actively favor native intraspecific diversity through eco‐evolutionary processes such as postzygotic selection.
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spelling pubmed-85913312021-11-22 Genotype‐by‐environment interactions drive the maintenance of genetic variation in a Salmo trutta L. hybrid zone Folio, Dorinda Marie Gil, Jordi Caudron, Arnaud Labonne, Jacques Evol Appl Original Articles Allopatric gene pools can evolve in different directions through adaptive and nonadaptive processes and are therefore a source of intraspecific diversity. The connection of these previously isolated gene pools through human intervention can lead to intraspecific diversity loss, through extirpation of native populations or hybridization. However, the mechanisms leading to these situations are not always explicitly documented and are thus rarely used to manage intraspecific diversity. In particular, genotype‐by‐environment (GxE) interactions can drive postzygotic reproductive isolation mechanisms that may result in a mosaic of diversity patterns, depending on the local environment. We test this hypothesis using a salmonid species (Salmo trutta) in the Mediterranean (MED) area, where intensive stocking from non‐native Atlantic (ATL) origins has led to various outcomes of hybridization with the native MED lineage, going from MED resilience to total extirpation via full hybridization. We investigate patterns of offspring survival at egg stage in natural environments, based on parental genotypes in interaction with river temperature, to detect potential GxE interactions. Our results show a strong influence of maternal GxE interaction on embryonic survival, mediated by maternal effect through egg size, and a weak influence of paternal GxE interaction. In particular, when egg size is large and temperature is cold, the survival rate of offspring originating from MED females is three times higher than that of ATL females’ offspring. Because river temperatures show contrast at small scale, this cold adaptation for MED females’ offspring constitutes a potent postzygotic mechanism to explain small‐scale spatial heterogeneity in diversity observed in MED areas where ATL fish have been stocked. It also indicates that management efforts could be specifically targeted at the environments that actively favor native intraspecific diversity through eco‐evolutionary processes such as postzygotic selection. John Wiley and Sons Inc. 2021-10-30 /pmc/articles/PMC8591331/ /pubmed/34815748 http://dx.doi.org/10.1111/eva.13307 Text en © 2021 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
Folio, Dorinda Marie
Gil, Jordi
Caudron, Arnaud
Labonne, Jacques
Genotype‐by‐environment interactions drive the maintenance of genetic variation in a Salmo trutta L. hybrid zone
title Genotype‐by‐environment interactions drive the maintenance of genetic variation in a Salmo trutta L. hybrid zone
title_full Genotype‐by‐environment interactions drive the maintenance of genetic variation in a Salmo trutta L. hybrid zone
title_fullStr Genotype‐by‐environment interactions drive the maintenance of genetic variation in a Salmo trutta L. hybrid zone
title_full_unstemmed Genotype‐by‐environment interactions drive the maintenance of genetic variation in a Salmo trutta L. hybrid zone
title_short Genotype‐by‐environment interactions drive the maintenance of genetic variation in a Salmo trutta L. hybrid zone
title_sort genotype‐by‐environment interactions drive the maintenance of genetic variation in a salmo trutta l. hybrid zone
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8591331/
https://www.ncbi.nlm.nih.gov/pubmed/34815748
http://dx.doi.org/10.1111/eva.13307
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