Cytonuclear discordance among Southeast Asian black rats (Rattus rattus complex)

International audience Black rats are major invasive vertebrate pests with severe ecological, economic and health impacts. Remarkably, their evolutionary history has received little attention, and there is no firm agreement on how many species should be recognized within the black rat complex. This...

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Published in:Molecular Ecology
Main Authors: Pages, Marie, Bazin, Eric, Galan, Maxime, Chaval, Yannick, Claude, Julien, Herbreteau, Vincent, Michaux, Johan, Piry, Sylvain, Morand, Serge, Cosson, Jean-Francois
Other Authors: Centre de Biologie pour la Gestion des Populations (UMR CBGP), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut National de la Recherche Agronomique (INRA)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Université de Montpellier (UM)-Institut de Recherche pour le Développement (IRD France-Sud )-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Laboratoire d'Ecologie Alpine (LECA), Université Joseph Fourier - Grenoble 1 (UJF)-Université Savoie Mont Blanc (USMB Université de Savoie Université de Chambéry )-Centre National de la Recherche Scientifique (CNRS), 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), UMR 228 Espace-Dev, Espace pour le développement, Institut de Recherche pour le Développement (IRD)-Université de Perpignan Via Domitia (UPVD)-Avignon Université (AU)-Université de La Réunion (UR)-Université de Montpellier (UM)-Université de Guyane (UG)-Université des Antilles (UA), Animal et gestion intégrée des risques (UPR AGIRs), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2013
Subjects:
Online Access:https://hal.univ-reunion.fr/hal-01239633
https://doi.org/10.1111/mec.12149
id ftunivavignon:oai:HAL:hal-01239633v1
record_format openpolar
institution Open Polar
collection Université d'Avignon et des Pays de Vaucluse: HAL
op_collection_id ftunivavignon
language English
topic incomplete lineage sorting
introgression
paraphyly
Rattus
recent speciation
species complex
[SHS.GEO]Humanities and Social Sciences/Geography
spellingShingle incomplete lineage sorting
introgression
paraphyly
Rattus
recent speciation
species complex
[SHS.GEO]Humanities and Social Sciences/Geography
Pages, Marie
Bazin, Eric
Galan, Maxime
Chaval, Yannick
Claude, Julien
Herbreteau, Vincent
Michaux, Johan
Piry, Sylvain
Morand, Serge
Cosson, Jean-Francois
Cytonuclear discordance among Southeast Asian black rats (Rattus rattus complex)
topic_facet incomplete lineage sorting
introgression
paraphyly
Rattus
recent speciation
species complex
[SHS.GEO]Humanities and Social Sciences/Geography
description International audience Black rats are major invasive vertebrate pests with severe ecological, economic and health impacts. Remarkably, their evolutionary history has received little attention, and there is no firm agreement on how many species should be recognized within the black rat complex. This species complex is native to India and Southeast Asia. According to current taxonomic classification, there are three taxa living in sympatry in several parts of Thailand, Cambodia and Lao People's Democratic Republic, where this study was conducted: two accepted species (Rattus tanezumi, Rattus sakeratensis) and an additional mitochondrial lineage of unclear taxonomic status referred to here as ‘Rattus R3’. We used extensive sampling, morphological data and diverse genetic markers differing in rates of evolution and parental inheritance (two mitochondrial DNA genes, one nuclear gene and eight microsatellite loci) to assess the reproductive isolation of these three taxa. Two close Asian relatives, Rattus argentiventer and Rattus exulans, were also included in the genetic analyses. Genetic analyses revealed discordance between the mitochondrial and nuclear data. Mitochondrial phylogeny studies identified three reciprocally monophyletic clades in the black rat complex. However, studies of the phylogeny of the nuclear exon interphotoreceptor retinoid-binding protein gene and clustering and assignation analyses with eight microsatellites failed to separate R. tanezumi and R3. Morphometric analyses were consistent with nuclear data. The incongruence between mitochondrial and nuclear (and morphological) data rendered R. tanezumi/R3 paraphyletic for mitochondrial lineages with respect to R. sakeratensis. Various evolutionary processes, such as shared ancestral polymorphism and incomplete lineage sorting or hybridization with massive mitochondrial introgression between species, may account for this unusual genetic pattern in mammals.
author2 Centre de Biologie pour la Gestion des Populations (UMR CBGP)
Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut National de la Recherche Agronomique (INRA)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Université de Montpellier (UM)-Institut de Recherche pour le Développement (IRD France-Sud )-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro)
Laboratoire d'Ecologie Alpine (LECA)
Université Joseph Fourier - Grenoble 1 (UJF)-Université Savoie Mont Blanc (USMB Université de Savoie Université de Chambéry )-Centre National de la Recherche Scientifique (CNRS)
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)
UMR 228 Espace-Dev, Espace pour le développement
Institut de Recherche pour le Développement (IRD)-Université de Perpignan Via Domitia (UPVD)-Avignon Université (AU)-Université de La Réunion (UR)-Université de Montpellier (UM)-Université de Guyane (UG)-Université des Antilles (UA)
Animal et gestion intégrée des risques (UPR AGIRs)
Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)
format Article in Journal/Newspaper
author Pages, Marie
Bazin, Eric
Galan, Maxime
Chaval, Yannick
Claude, Julien
Herbreteau, Vincent
Michaux, Johan
Piry, Sylvain
Morand, Serge
Cosson, Jean-Francois
author_facet Pages, Marie
Bazin, Eric
Galan, Maxime
Chaval, Yannick
Claude, Julien
Herbreteau, Vincent
Michaux, Johan
Piry, Sylvain
Morand, Serge
Cosson, Jean-Francois
author_sort Pages, Marie
title Cytonuclear discordance among Southeast Asian black rats (Rattus rattus complex)
title_short Cytonuclear discordance among Southeast Asian black rats (Rattus rattus complex)
title_full Cytonuclear discordance among Southeast Asian black rats (Rattus rattus complex)
title_fullStr Cytonuclear discordance among Southeast Asian black rats (Rattus rattus complex)
title_full_unstemmed Cytonuclear discordance among Southeast Asian black rats (Rattus rattus complex)
title_sort cytonuclear discordance among southeast asian black rats (rattus rattus complex)
publisher HAL CCSD
publishDate 2013
url https://hal.univ-reunion.fr/hal-01239633
https://doi.org/10.1111/mec.12149
genre Rattus rattus
genre_facet Rattus rattus
op_source ISSN: 0962-1083
EISSN: 1365-294X
Molecular Ecology
https://hal.univ-reunion.fr/hal-01239633
Molecular Ecology, 2013, 22 (4), pp.1019--1034. ⟨10.1111/mec.12149⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1111/mec.12149
hal-01239633
https://hal.univ-reunion.fr/hal-01239633
doi:10.1111/mec.12149
PRODINRA: 195426
WOS: 000314220900010
op_doi https://doi.org/10.1111/mec.12149
container_title Molecular Ecology
container_volume 22
container_issue 4
container_start_page 1019
op_container_end_page 1034
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spelling ftunivavignon:oai:HAL:hal-01239633v1 2024-05-19T07:47:45+00:00 Cytonuclear discordance among Southeast Asian black rats (Rattus rattus complex) Pages, Marie Bazin, Eric Galan, Maxime Chaval, Yannick Claude, Julien Herbreteau, Vincent Michaux, Johan Piry, Sylvain Morand, Serge Cosson, Jean-Francois Centre de Biologie pour la Gestion des Populations (UMR CBGP) Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut National de la Recherche Agronomique (INRA)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Université de Montpellier (UM)-Institut de Recherche pour le Développement (IRD France-Sud )-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro) Laboratoire d'Ecologie Alpine (LECA) Université Joseph Fourier - Grenoble 1 (UJF)-Université Savoie Mont Blanc (USMB Université de Savoie Université de Chambéry )-Centre National de la Recherche Scientifique (CNRS) 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) UMR 228 Espace-Dev, Espace pour le développement Institut de Recherche pour le Développement (IRD)-Université de Perpignan Via Domitia (UPVD)-Avignon Université (AU)-Université de La Réunion (UR)-Université de Montpellier (UM)-Université de Guyane (UG)-Université des Antilles (UA) Animal et gestion intégrée des risques (UPR AGIRs) Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad) 2013 https://hal.univ-reunion.fr/hal-01239633 https://doi.org/10.1111/mec.12149 en eng HAL CCSD Wiley info:eu-repo/semantics/altIdentifier/doi/10.1111/mec.12149 hal-01239633 https://hal.univ-reunion.fr/hal-01239633 doi:10.1111/mec.12149 PRODINRA: 195426 WOS: 000314220900010 ISSN: 0962-1083 EISSN: 1365-294X Molecular Ecology https://hal.univ-reunion.fr/hal-01239633 Molecular Ecology, 2013, 22 (4), pp.1019--1034. ⟨10.1111/mec.12149⟩ incomplete lineage sorting introgression paraphyly Rattus recent speciation species complex [SHS.GEO]Humanities and Social Sciences/Geography info:eu-repo/semantics/article Journal articles 2013 ftunivavignon https://doi.org/10.1111/mec.12149 2024-05-01T23:49:31Z International audience Black rats are major invasive vertebrate pests with severe ecological, economic and health impacts. Remarkably, their evolutionary history has received little attention, and there is no firm agreement on how many species should be recognized within the black rat complex. This species complex is native to India and Southeast Asia. According to current taxonomic classification, there are three taxa living in sympatry in several parts of Thailand, Cambodia and Lao People's Democratic Republic, where this study was conducted: two accepted species (Rattus tanezumi, Rattus sakeratensis) and an additional mitochondrial lineage of unclear taxonomic status referred to here as ‘Rattus R3’. We used extensive sampling, morphological data and diverse genetic markers differing in rates of evolution and parental inheritance (two mitochondrial DNA genes, one nuclear gene and eight microsatellite loci) to assess the reproductive isolation of these three taxa. Two close Asian relatives, Rattus argentiventer and Rattus exulans, were also included in the genetic analyses. Genetic analyses revealed discordance between the mitochondrial and nuclear data. Mitochondrial phylogeny studies identified three reciprocally monophyletic clades in the black rat complex. However, studies of the phylogeny of the nuclear exon interphotoreceptor retinoid-binding protein gene and clustering and assignation analyses with eight microsatellites failed to separate R. tanezumi and R3. Morphometric analyses were consistent with nuclear data. The incongruence between mitochondrial and nuclear (and morphological) data rendered R. tanezumi/R3 paraphyletic for mitochondrial lineages with respect to R. sakeratensis. Various evolutionary processes, such as shared ancestral polymorphism and incomplete lineage sorting or hybridization with massive mitochondrial introgression between species, may account for this unusual genetic pattern in mammals. Article in Journal/Newspaper Rattus rattus Université d'Avignon et des Pays de Vaucluse: HAL Molecular Ecology 22 4 1019 1034