Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs

Subdivided Pleistocene glacial refugia, best known as “refugia within refugia”, provided opportunities for diverging populations to evolve into incipient species and/or to hybridize and merge following range shifts tracking the climatic fluctuations, potentially promoting extensive cytonuclear disco...

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Autores: Dufresnes, Christophe, Nicieza, Alfredo G., Litvinchuk, Spartak N., Rodrigues, Nicolas, Jeffries, Daniel L., Vences, Miguel, Perrin, Nicolas, Martínez-Solano, Íñigo
Tipo de recurso: artículo
Estado:Versión aceptada para publicación
Fecha de publicación:2020
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/236781
Acceso en línea:http://hdl.handle.net/10261/236781
Access Level:acceso abierto
Palabra clave:Ghost linage
Glacial refugium
Hybrid zone
RAD-sequencing
Rana parvipalmata
Rana temporaria
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spelling Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogsDufresnes, ChristopheNicieza, Alfredo G.Litvinchuk, Spartak N.Rodrigues, NicolasJeffries, Daniel L.Vences, MiguelPerrin, NicolasMartínez-Solano, ÍñigoGhost linageGlacial refugiumHybrid zoneRAD-sequencingRana parvipalmataRana temporariaSubdivided Pleistocene glacial refugia, best known as “refugia within refugia”, provided opportunities for diverging populations to evolve into incipient species and/or to hybridize and merge following range shifts tracking the climatic fluctuations, potentially promoting extensive cytonuclear discordances and “ghost” mtDNA lineages. Here, we tested which of these opposing evolutionary outcomes prevails in northern Iberian areas hosting multiple historical refugia of common frogs (Rana cf. temporaria), based on a genomic phylogeography approach (mtDNA barcoding and RAD-sequencing). We found evidence for both incipient speciation events and massive cytonuclear discordances. On the one hand, populations from northwestern Spain (Galicia and Asturias, assigned to the regional endemic R. parvipalmata), are deeply-diverged at mitochondrial and nuclear genomes (~4 My of independent evolution), and barely admix with northeastern populations (assigned to R. temporaria sensu stricto) across a narrow hybrid zone (~25 km) located in the Cantabrian Mountains, suggesting that they represent distinct species. On the other hand, the most divergent mtDNA clade, widespread in Cantabria and the Basque country, shares its nuclear genome with other R. temporaria s. s. lineages. Patterns of population expansions and isolation-by-distance among these populations are consistent with past mitochondrial capture and/or drift in generating and maintaining this ghost mitochondrial lineage. This remarkable case study emphasizes the complex evolutionary history that shaped the present genetic diversity of refugial populations, and stresses the need to revisit their phylogeography by genomic approaches, in order to make informed taxonomic inferences.We thank C. Cabido, I. Garin, A. Gosá, F. Martínez, J. Rubines, X. Rubio, and G. Sánchez‐Montes for help in sample collection. This study was funded by the Swiss National Science Foundation (fellowship P2LAP3_171818 to CD, and grant 31003A_166323 to NP). MV was supported by the Deutsche Forschungsgemeinschaft (grant VE247/16‐1–HO 3492/6‐1) in the framework of the ‘TaxonOmics' priority program, SNL by the RFBR (grant 20‐04‐00918), and AGN by the Ministerio de Ciencia, Innovación y Universidades, Gobierno de España (MICINN grants CGL2012‐40246 and CGL2017‐86924‐P).John Wiley & SonsSwiss National Science FoundationGerman Research FoundationMinisterio de Ciencia e Innovación (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2021202120202021info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Postprintinfo:eu-repo/semantics/acceptedVersionhttp://hdl.handle.net/10261/236781reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/CGL2017‐86924‐Phttp://dx.doi.org/10.1111/mec.15368Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2367812026-05-22T06:33:51Z
dc.title.none.fl_str_mv Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs
title Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs
spellingShingle Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs
Dufresnes, Christophe
Ghost linage
Glacial refugium
Hybrid zone
RAD-sequencing
Rana parvipalmata
Rana temporaria
title_short Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs
title_full Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs
title_fullStr Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs
title_full_unstemmed Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs
title_sort Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs
dc.creator.none.fl_str_mv Dufresnes, Christophe
Nicieza, Alfredo G.
Litvinchuk, Spartak N.
Rodrigues, Nicolas
Jeffries, Daniel L.
Vences, Miguel
Perrin, Nicolas
Martínez-Solano, Íñigo
author Dufresnes, Christophe
author_facet Dufresnes, Christophe
Nicieza, Alfredo G.
Litvinchuk, Spartak N.
Rodrigues, Nicolas
Jeffries, Daniel L.
Vences, Miguel
Perrin, Nicolas
Martínez-Solano, Íñigo
author_role author
author2 Nicieza, Alfredo G.
Litvinchuk, Spartak N.
Rodrigues, Nicolas
Jeffries, Daniel L.
Vences, Miguel
Perrin, Nicolas
Martínez-Solano, Íñigo
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Swiss National Science Foundation
German Research Foundation
Ministerio de Ciencia e Innovación (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Ghost linage
Glacial refugium
Hybrid zone
RAD-sequencing
Rana parvipalmata
Rana temporaria
topic Ghost linage
Glacial refugium
Hybrid zone
RAD-sequencing
Rana parvipalmata
Rana temporaria
description Subdivided Pleistocene glacial refugia, best known as “refugia within refugia”, provided opportunities for diverging populations to evolve into incipient species and/or to hybridize and merge following range shifts tracking the climatic fluctuations, potentially promoting extensive cytonuclear discordances and “ghost” mtDNA lineages. Here, we tested which of these opposing evolutionary outcomes prevails in northern Iberian areas hosting multiple historical refugia of common frogs (Rana cf. temporaria), based on a genomic phylogeography approach (mtDNA barcoding and RAD-sequencing). We found evidence for both incipient speciation events and massive cytonuclear discordances. On the one hand, populations from northwestern Spain (Galicia and Asturias, assigned to the regional endemic R. parvipalmata), are deeply-diverged at mitochondrial and nuclear genomes (~4 My of independent evolution), and barely admix with northeastern populations (assigned to R. temporaria sensu stricto) across a narrow hybrid zone (~25 km) located in the Cantabrian Mountains, suggesting that they represent distinct species. On the other hand, the most divergent mtDNA clade, widespread in Cantabria and the Basque country, shares its nuclear genome with other R. temporaria s. s. lineages. Patterns of population expansions and isolation-by-distance among these populations are consistent with past mitochondrial capture and/or drift in generating and maintaining this ghost mitochondrial lineage. This remarkable case study emphasizes the complex evolutionary history that shaped the present genetic diversity of refugial populations, and stresses the need to revisit their phylogeography by genomic approaches, in order to make informed taxonomic inferences.
publishDate 2020
dc.date.none.fl_str_mv 2020
2021
2021
2021
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Postprint
info:eu-repo/semantics/acceptedVersion
format article
status_str acceptedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/236781
url http://hdl.handle.net/10261/236781
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/CGL2017‐86924‐P
http://dx.doi.org/10.1111/mec.15368
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv John Wiley & Sons
publisher.none.fl_str_mv John Wiley & Sons
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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