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      Replicated anthropogenic hybridisations reveal parallel patterns of admixture in marine mussels

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          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.

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          Hybridization and speciation.

          Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and recombination. It may accelerate speciation via adaptive introgression or cause near-instantaneous speciation by allopolyploidization. It may have multiple effects at different stages and in different spatial contexts within a single speciation event. We offer a perspective on the context and evolutionary significance of hybridization during speciation, highlighting issues of current interest and debate. In secondary contact zones, it is uncertain if barriers to gene flow will be strengthened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate speciation. Gene regulatory networks, epigenetic effects and the evolution of selfish genetic material in the genome suggest that the Dobzhansky-Muller model of hybrid incompatibilities requires a broader interpretation. Finally, although the incidence of reinforcement remains uncertain, this and other interactions in areas of sympatry may have knock-on effects on speciation both within and outside regions of hybridization. © 2013 The Authors. Journal of Evolutionary Biology © 2013 European Society For Evolutionary Biology.
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            R/qtl: QTL mapping in experimental crosses

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              The evolutionary impact of invasive species.

              Since the Age of Exploration began, there has been a drastic breaching of biogeographic barriers that previously had isolated the continental biotas for millions of years. We explore the nature of these recent biotic exchanges and their consequences on evolutionary processes. The direct evidence of evolutionary consequences of the biotic rearrangements is of variable quality, but the results of trajectories are becoming clear as the number of studies increases. There are examples of invasive species altering the evolutionary pathway of native species by competitive exclusion, niche displacement, hybridization, introgression, predation, and ultimately extinction. Invaders themselves evolve in response to their interactions with natives, as well as in response to the new abiotic environment. Flexibility in behavior, and mutualistic interactions, can aid in the success of invaders in their new environment.
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                Author and article information

                Contributors
                alexis.simon@normalesup.org
                Journal
                Evol Appl
                Evol Appl
                10.1111/(ISSN)1752-4571
                EVA
                Evolutionary Applications
                John Wiley and Sons Inc. (Hoboken )
                1752-4571
                22 November 2019
                March 2020
                : 13
                : 3 , An evolutionary perspective on marine bioinvasions: evolutionary history, adaptation, and species interactions ( doiID: 10.1111/eva.v13.3 )
                : 575-599
                Affiliations
                [ 1 ] ISEM Univ Montpellier CNRS EPHE IRD Montpellier France
                [ 2 ] Section for Marine Living Resources National Institute of Aquatic Resources Technical University of Denmark Silkeborg Denmark
                [ 3 ] SARL TOXEM Le Havre France
                [ 4 ] Ifremer Unité Biogéochimie et Écotoxicologie Centre Atlantique Nantes France
                [ 5 ] SAS Eurêka Mer Lézardrieux France
                [ 6 ] Wageningen Marine Research Den Helder The Netherlands
                [ 7 ] Aquatic Ecology and Water Quality Management Group Wageningen University Wageningen The Netherlands
                [ 8 ] SG2M‐LGPMM Laboratoire de Génétique et Pathologie des Mollusques Marins Ifremer La Tremblade France
                [ 9 ] St. Petersburg State University St. Petersburg Russia
                [ 10 ] Laboratory of Monitoring and Conservation of Natural Arctic Ecosystems Murmansk Arctic State University Murmansk Russia
                [ 11 ] Department of Biology & CESAM University of Aveiro Aveiro Portugal
                [ 12 ] CBET 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 Spain
                [ 13 ] Department of Genetics University of Cambridge Cambridge UK
                [ 14 ] Department AD2M UPMC Univ Paris 06 CNRS UMR 7144 Station Biologique Sorbonne Universités Roscoff France
                Author notes
                [*] [* ] Correspondence

                Alexis Simon, ISEM, CNRS, EPHE, IRD, Univ Montpellier, Montpellier, France.

                Email: alexis.simon@ 123456normalesup.org

                Author information
                https://orcid.org/0000-0002-6176-5045
                https://orcid.org/0000-0002-7009-9814
                https://orcid.org/0000-0002-3666-7419
                https://orcid.org/0000-0002-8127-6097
                https://orcid.org/0000-0002-6078-0905
                https://orcid.org/0000-0002-1663-4871
                https://orcid.org/0000-0002-6030-7034
                https://orcid.org/0000-0002-2338-0013
                https://orcid.org/0000-0003-4841-0079
                https://orcid.org/0000-0001-5603-9527
                https://orcid.org/0000-0003-1856-3197
                Article
                EVA12879
                10.1111/eva.12879
                7045717
                32431737
                6ffd1a96-02c7-4dd5-b73e-3ffec5b6da3c
                © 2019 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 11 March 2019
                : 27 September 2019
                : 02 October 2019
                Page count
                Figures: 5, Tables: 1, Pages: 25, Words: 20301
                Funding
                Funded by: Agence Nationale de la Recherche , open-funder-registry 10.13039/501100001665;
                Award ID: ANR‐10‐LABX‐04‐01
                Award ID: ANR‐12‐BSV7‐0011
                Funded by: Russian Science Foundation , open-funder-registry 10.13039/501100006769;
                Award ID: 19‐74‐20024
                Categories
                Original Article
                Special Issue Original Articles
                Custom metadata
                2.0
                March 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.6.1 mode:remove_FC converted:27.02.2020

                Evolutionary Biology
                admixture,bentho‐pelagic species,biological introductions,clines,ports,secondary contact

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