Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels

Abstract Human‐mediated transport creates secondary contacts between genetically differentiated lineages, bringing new opportunities for gene exchange. When similar introductions occur in different places, they provide informally replicated experiments for studying hybridisation. We here examined 4,...

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Main Authors: Alexis Simon, Christine Arbiol, Einar Eg Nielsen, Jérôme Couteau, Rossana Sussarellu, Thierry Burgeot, Ismaël Bernard, Joop W. P. Coolen, Jean‐Baptiste Lamy, Stéphane Robert, Maria Skazina, Petr Strelkov, Henrique Queiroga, Ibon Cancio, John J. Welch, Frédérique Viard, Nicolas Bierne
Format: Article
Language:English
Published: Wiley 2020-03-01
Series:Evolutionary Applications
Subjects:
Online Access:https://doi.org/10.1111/eva.12879
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spelling doaj-272a61f0d5ec450fba33eaedebeb28662020-11-25T03:42:14ZengWileyEvolutionary Applications1752-45712020-03-0113357559910.1111/eva.12879Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine musselsAlexis Simon0Christine Arbiol1Einar Eg Nielsen2Jérôme Couteau3Rossana Sussarellu4Thierry Burgeot5Ismaël Bernard6Joop W. P. Coolen7Jean‐Baptiste Lamy8Stéphane Robert9Maria Skazina10Petr Strelkov11Henrique Queiroga12Ibon Cancio13John J. Welch14Frédérique Viard15Nicolas Bierne16ISEM Univ Montpellier CNRS EPHE IRD Montpellier FranceISEM Univ Montpellier CNRS EPHE IRD Montpellier FranceSection for Marine Living Resources National Institute of Aquatic Resources Technical University of Denmark Silkeborg DenmarkSARL TOXEM Le Havre FranceIfremer Unité Biogéochimie et Écotoxicologie Centre Atlantique Nantes FranceIfremer Unité Biogéochimie et Écotoxicologie Centre Atlantique Nantes FranceSAS Eurêka Mer Lézardrieux FranceWageningen Marine Research Den Helder The NetherlandsSG2M‐LGPMM Laboratoire de Génétique et Pathologie des Mollusques Marins Ifremer La Tremblade FranceSG2M‐LGPMM Laboratoire de Génétique et Pathologie des Mollusques Marins Ifremer La Tremblade FranceSt. Petersburg State University St. Petersburg RussiaSt. Petersburg State University St. Petersburg RussiaDepartment of Biology & CESAM University of Aveiro Aveiro PortugalCBET Research Group Department of Zoology and Animal Cell Biology Faculty Science and Technology and Research Centre for Experimental Marine Biology and Biotechnology (PiE‐UPV/EHU) University of the Basque Country (UPV/EHU) Bilbao SpainDepartment of Genetics University of Cambridge Cambridge UKDepartment AD2M UPMC Univ Paris 06 CNRS UMR 7144 Station Biologique Sorbonne Universités Roscoff FranceISEM Univ Montpellier CNRS EPHE IRD Montpellier FranceAbstract Human‐mediated transport creates secondary contacts between genetically differentiated lineages, bringing new opportunities for gene exchange. When similar introductions occur in different places, they provide informally replicated experiments for studying hybridisation. We here examined 4,279 Mytilus mussels, sampled in Europe and genotyped with 77 ancestry‐informative markers. We identified a type of introduced mussels, called “dock mussels,” associated with port habitats and displaying a particular genetic signal of admixture between M. edulis and the Mediterranean lineage of M. galloprovincialis. These mussels exhibit similarities in their ancestry compositions, regardless of the local native genetic backgrounds and the distance separating colonised ports. We observed fine‐scale genetic shifts at the port entrance, at scales below natural dispersal distance. Such sharp clines do not fit with migration‐selection tension zone models, and instead suggest habitat choice and early‐stage adaptation to the port environment, possibly coupled with connectivity barriers. Variations in the spread and admixture patterns of dock mussels seem to be influenced by the local native genetic backgrounds encountered. We next examined departures from the average admixture rate at different loci, and compared human‐mediated admixture events, to naturally admixed populations and experimental crosses. When the same M. galloprovincialis background was involved, positive correlations in the departures of loci across locations were found; but when different backgrounds were involved, no or negative correlations were observed. While some observed positive correlations might be best explained by a shared history and saltatory colonisation, others are likely produced by parallel selective events. Altogether, genome‐wide effect of admixture seems repeatable and more dependent on genetic background than environmental context. Our results pave the way towards further genomic analyses of admixture, and monitoring of the spread of dock mussels both at large and at fine spacial scales.https://doi.org/10.1111/eva.12879admixturebentho‐pelagic speciesbiological introductionsclinesportssecondary contact
collection DOAJ
language English
format Article
sources DOAJ
author Alexis Simon
Christine Arbiol
Einar Eg Nielsen
Jérôme Couteau
Rossana Sussarellu
Thierry Burgeot
Ismaël Bernard
Joop W. P. Coolen
Jean‐Baptiste Lamy
Stéphane Robert
Maria Skazina
Petr Strelkov
Henrique Queiroga
Ibon Cancio
John J. Welch
Frédérique Viard
Nicolas Bierne
spellingShingle Alexis Simon
Christine Arbiol
Einar Eg Nielsen
Jérôme Couteau
Rossana Sussarellu
Thierry Burgeot
Ismaël Bernard
Joop W. P. Coolen
Jean‐Baptiste Lamy
Stéphane Robert
Maria Skazina
Petr Strelkov
Henrique Queiroga
Ibon Cancio
John J. Welch
Frédérique Viard
Nicolas Bierne
Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels
Evolutionary Applications
admixture
bentho‐pelagic species
biological introductions
clines
ports
secondary contact
author_facet Alexis Simon
Christine Arbiol
Einar Eg Nielsen
Jérôme Couteau
Rossana Sussarellu
Thierry Burgeot
Ismaël Bernard
Joop W. P. Coolen
Jean‐Baptiste Lamy
Stéphane Robert
Maria Skazina
Petr Strelkov
Henrique Queiroga
Ibon Cancio
John J. Welch
Frédérique Viard
Nicolas Bierne
author_sort Alexis Simon
title Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels
title_short Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels
title_full Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels
title_fullStr Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels
title_full_unstemmed Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels
title_sort replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels
publisher Wiley
series Evolutionary Applications
issn 1752-4571
publishDate 2020-03-01
description Abstract Human‐mediated transport creates secondary contacts between genetically differentiated lineages, bringing new opportunities for gene exchange. When similar introductions occur in different places, they provide informally replicated experiments for studying hybridisation. We here examined 4,279 Mytilus mussels, sampled in Europe and genotyped with 77 ancestry‐informative markers. We identified a type of introduced mussels, called “dock mussels,” associated with port habitats and displaying a particular genetic signal of admixture between M. edulis and the Mediterranean lineage of M. galloprovincialis. These mussels exhibit similarities in their ancestry compositions, regardless of the local native genetic backgrounds and the distance separating colonised ports. We observed fine‐scale genetic shifts at the port entrance, at scales below natural dispersal distance. Such sharp clines do not fit with migration‐selection tension zone models, and instead suggest habitat choice and early‐stage adaptation to the port environment, possibly coupled with connectivity barriers. Variations in the spread and admixture patterns of dock mussels seem to be influenced by the local native genetic backgrounds encountered. We next examined departures from the average admixture rate at different loci, and compared human‐mediated admixture events, to naturally admixed populations and experimental crosses. When the same M. galloprovincialis background was involved, positive correlations in the departures of loci across locations were found; but when different backgrounds were involved, no or negative correlations were observed. While some observed positive correlations might be best explained by a shared history and saltatory colonisation, others are likely produced by parallel selective events. Altogether, genome‐wide effect of admixture seems repeatable and more dependent on genetic background than environmental context. Our results pave the way towards further genomic analyses of admixture, and monitoring of the spread of dock mussels both at large and at fine spacial scales.
topic admixture
bentho‐pelagic species
biological introductions
clines
ports
secondary contact
url https://doi.org/10.1111/eva.12879
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