The genomic impact of historical hybridization with massive mitochondrial DNA introgression

International audience Background: The extent to which selection determines interspecific patterns of genetic exchange enlightens the role of adaptation in evolution and speciation. Often reported extensive interspecific introgression could be selection-driven, but also result from demographic proce...

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Published in:Genome Biology
Main Authors: Seixas, Fernando, Boursot, Pierre, Melo-Ferreira, José
Other Authors: Institut des Sciences de l'Evolution de Montpellier (UMR ISEM), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École Pratique des Hautes Études (EPHE), Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Université de Montpellier (UM)-Institut de recherche pour le développement IRD : UR226-Centre National de la Recherche Scientifique (CNRS), Centro de Investigação em Biodiversidade e Recursos Genéticos (CIBIO-UP), Universidade do Porto = University of Porto-CESPU, ANR-12-ISV7-0002,HybridAdapt,Hybridation, adaptation et histoire des peuplements: une approche génomique.(2012)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2018
Subjects:
Online Access:https://hal.umontpellier.fr/hal-02346728
https://hal.umontpellier.fr/hal-02346728/document
https://hal.umontpellier.fr/hal-02346728/file/s13059-018-1471-8.pdf
https://doi.org/10.1186/s13059-018-1471-8
id ftunimontpellier:oai:HAL:hal-02346728v1
record_format openpolar
spelling ftunimontpellier:oai:HAL:hal-02346728v1 2024-05-19T07:36:41+00:00 The genomic impact of historical hybridization with massive mitochondrial DNA introgression Seixas, Fernando Boursot, Pierre Melo-Ferreira, José Institut des Sciences de l'Evolution de Montpellier (UMR ISEM) Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École Pratique des Hautes Études (EPHE) Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Université de Montpellier (UM)-Institut de recherche pour le développement IRD : UR226-Centre National de la Recherche Scientifique (CNRS) Centro de Investigação em Biodiversidade e Recursos Genéticos (CIBIO-UP) Universidade do Porto = University of Porto-CESPU ANR-12-ISV7-0002,HybridAdapt,Hybridation, adaptation et histoire des peuplements: une approche génomique.(2012) 2018-12 https://hal.umontpellier.fr/hal-02346728 https://hal.umontpellier.fr/hal-02346728/document https://hal.umontpellier.fr/hal-02346728/file/s13059-018-1471-8.pdf https://doi.org/10.1186/s13059-018-1471-8 en eng HAL CCSD BioMed Central info:eu-repo/semantics/altIdentifier/doi/10.1186/s13059-018-1471-8 hal-02346728 https://hal.umontpellier.fr/hal-02346728 https://hal.umontpellier.fr/hal-02346728/document https://hal.umontpellier.fr/hal-02346728/file/s13059-018-1471-8.pdf doi:10.1186/s13059-018-1471-8 http://creativecommons.org/licenses/by/ info:eu-repo/semantics/OpenAccess ISSN: 1465-6906 EISSN: 1474-760X Genome Biology https://hal.umontpellier.fr/hal-02346728 Genome Biology, 2018, 19 (1), ⟨10.1186/s13059-018-1471-8⟩ Introgressive hybridization Iberian hares Whole genome sequencing Range invasion Adaptation [SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE] [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE] info:eu-repo/semantics/article Journal articles 2018 ftunimontpellier https://doi.org/10.1186/s13059-018-1471-8 2024-05-01T00:32:10Z International audience Background: The extent to which selection determines interspecific patterns of genetic exchange enlightens the role of adaptation in evolution and speciation. Often reported extensive interspecific introgression could be selection-driven, but also result from demographic processes, especially in cases of invasive species replacements, which can promote introgression at their invasion front. Because invasion and selective sweeps similarly mold variation, population genetics evidence for selection can only be gathered in an explicit demographic framework. The Iberian hare, Lepus granatensis, displays in its northern range extensive mitochondrial DNA introgression from L. timidus, an arctic/boreal species that it replaced locally after the last glacial maximum. We use whole-genome sequencing to infer geographic and genomic patterns of nuclear introgression and fit a neutral model of species replacement with hybridization, allowing us to evaluate how selection influenced introgression genome-wide, including for mtDNA. Results: Although the average nuclear and mtDNA introgression patterns contrast strongly, they fit a single demographic model of post-glacial invasive replacement of timidus by granatensis. Outliers of elevated introgression include several genes related to immunity, spermatogenesis, and mitochondrial metabolism. Introgression is reduced on the X chromosome and in low recombining regions. Conclusions: General nuclear and mtDNA patterns of introgression can be explained by purely demographic processes. Hybrid incompatibilities and interplay between selection and recombination locally modulate levels of nuclear introgression. Selection promoted introgression of some genes involved in conflicts, either interspecific (parasites) or possibly cytonuclear. In the latter case, nuclear introgression could mitigate the potential negative effects of alien mtDNA on mitochondrial metabolism and male-specific traits. Article in Journal/Newspaper Arctic Université de Montpellier: HAL Genome Biology 19 1
institution Open Polar
collection Université de Montpellier: HAL
op_collection_id ftunimontpellier
language English
topic Introgressive hybridization
Iberian hares
Whole genome sequencing
Range invasion
Adaptation
[SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE]
[SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]
spellingShingle Introgressive hybridization
Iberian hares
Whole genome sequencing
Range invasion
Adaptation
[SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE]
[SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]
Seixas, Fernando
Boursot, Pierre
Melo-Ferreira, José
The genomic impact of historical hybridization with massive mitochondrial DNA introgression
topic_facet Introgressive hybridization
Iberian hares
Whole genome sequencing
Range invasion
Adaptation
[SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE]
[SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]
description International audience Background: The extent to which selection determines interspecific patterns of genetic exchange enlightens the role of adaptation in evolution and speciation. Often reported extensive interspecific introgression could be selection-driven, but also result from demographic processes, especially in cases of invasive species replacements, which can promote introgression at their invasion front. Because invasion and selective sweeps similarly mold variation, population genetics evidence for selection can only be gathered in an explicit demographic framework. The Iberian hare, Lepus granatensis, displays in its northern range extensive mitochondrial DNA introgression from L. timidus, an arctic/boreal species that it replaced locally after the last glacial maximum. We use whole-genome sequencing to infer geographic and genomic patterns of nuclear introgression and fit a neutral model of species replacement with hybridization, allowing us to evaluate how selection influenced introgression genome-wide, including for mtDNA. Results: Although the average nuclear and mtDNA introgression patterns contrast strongly, they fit a single demographic model of post-glacial invasive replacement of timidus by granatensis. Outliers of elevated introgression include several genes related to immunity, spermatogenesis, and mitochondrial metabolism. Introgression is reduced on the X chromosome and in low recombining regions. Conclusions: General nuclear and mtDNA patterns of introgression can be explained by purely demographic processes. Hybrid incompatibilities and interplay between selection and recombination locally modulate levels of nuclear introgression. Selection promoted introgression of some genes involved in conflicts, either interspecific (parasites) or possibly cytonuclear. In the latter case, nuclear introgression could mitigate the potential negative effects of alien mtDNA on mitochondrial metabolism and male-specific traits.
author2 Institut des Sciences de l'Evolution de Montpellier (UMR ISEM)
Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École Pratique des Hautes Études (EPHE)
Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Université de Montpellier (UM)-Institut de recherche pour le développement IRD : UR226-Centre National de la Recherche Scientifique (CNRS)
Centro de Investigação em Biodiversidade e Recursos Genéticos (CIBIO-UP)
Universidade do Porto = University of Porto-CESPU
ANR-12-ISV7-0002,HybridAdapt,Hybridation, adaptation et histoire des peuplements: une approche génomique.(2012)
format Article in Journal/Newspaper
author Seixas, Fernando
Boursot, Pierre
Melo-Ferreira, José
author_facet Seixas, Fernando
Boursot, Pierre
Melo-Ferreira, José
author_sort Seixas, Fernando
title The genomic impact of historical hybridization with massive mitochondrial DNA introgression
title_short The genomic impact of historical hybridization with massive mitochondrial DNA introgression
title_full The genomic impact of historical hybridization with massive mitochondrial DNA introgression
title_fullStr The genomic impact of historical hybridization with massive mitochondrial DNA introgression
title_full_unstemmed The genomic impact of historical hybridization with massive mitochondrial DNA introgression
title_sort genomic impact of historical hybridization with massive mitochondrial dna introgression
publisher HAL CCSD
publishDate 2018
url https://hal.umontpellier.fr/hal-02346728
https://hal.umontpellier.fr/hal-02346728/document
https://hal.umontpellier.fr/hal-02346728/file/s13059-018-1471-8.pdf
https://doi.org/10.1186/s13059-018-1471-8
genre Arctic
genre_facet Arctic
op_source ISSN: 1465-6906
EISSN: 1474-760X
Genome Biology
https://hal.umontpellier.fr/hal-02346728
Genome Biology, 2018, 19 (1), ⟨10.1186/s13059-018-1471-8⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1186/s13059-018-1471-8
hal-02346728
https://hal.umontpellier.fr/hal-02346728
https://hal.umontpellier.fr/hal-02346728/document
https://hal.umontpellier.fr/hal-02346728/file/s13059-018-1471-8.pdf
doi:10.1186/s13059-018-1471-8
op_rights http://creativecommons.org/licenses/by/
info:eu-repo/semantics/OpenAccess
op_doi https://doi.org/10.1186/s13059-018-1471-8
container_title Genome Biology
container_volume 19
container_issue 1
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