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      The origin and remolding of genomic islands of differentiation in the European sea bass

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          Abstract

          Speciation is a complex process that leads to the progressive establishment of reproductive isolation barriers between diverging populations. Genome-wide comparisons between closely related species have revealed the existence of heterogeneous divergence patterns, dominated by genomic islands of increased divergence supposed to contain reproductive isolation loci. However, this divergence landscape only provides a static picture of the dynamic process of speciation, during which confounding mechanisms unrelated to speciation can interfere. Here we use haplotype-resolved whole-genome sequences to identify the mechanisms responsible for the formation of genomic islands between Atlantic and Mediterranean sea bass lineages. Local ancestry patterns show that genomic islands first emerged in allopatry through linked selection acting on a heterogeneous recombination landscape. Then, upon secondary contact, preexisting islands were strongly remolded by differential introgression, revealing variable fitness effects among regions involved in reproductive isolation. Interestingly, we find that divergent regions containing ancient polymorphisms conferred the strongest resistance to introgression.

          Abstract

          The speciation process tends to generate ‘genomic islands’ of increased divergence. Here, the authors use haplotype–resolved whole-genome sequences of European sea bass lineages to infer divergence history and show that linked selection generated genomic islands that resist introgression at secondary contact.

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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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            The genomic basis of adaptive evolution in threespine sticklebacks

            Summary Marine stickleback fish have colonized and adapted to innumerable streams and lakes formed since the last ice age, providing an exceptional opportunity to characterize genomic mechanisms underlying repeated ecological adaptation in nature. Here we develop a high quality reference genome assembly for threespine sticklebacks. By sequencing the genomes of 20 additional individuals from a global set of marine and freshwater populations, we identify a genome-wide set of loci that are consistently associated with marine-freshwater divergence. Our results suggest that reuse of globally-shared standing genetic variation, including chromosomal inversions, plays an important role in repeated evolution of distinct marine and freshwater sticklebacks, and in the maintenance of divergent ecotypes during early stages of reproductive isolation. Both coding and regulatory changes occur in the set of loci underlying marine-freshwater evolution, with regulatory changes likely predominating in this classic example of repeated adaptive evolution in nature.
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              The hitch-hiking effect of a favourable gene

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                Author and article information

                Contributors
                maud.duranton@umontpellier.fr
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                28 June 2018
                28 June 2018
                2018
                : 9
                : 2518
                Affiliations
                [1 ]ISNI 0000 0001 2188 7059, GRID grid.462058.d, Institut des Sciences de l’Evolution de Montpellier - UMR5554 UM-CNRS-IRD-EPHE, ; Place Eugène Bataillon, 34095 Montpellier, France
                [2 ]ISNI 0000 0001 2097 0141, GRID grid.121334.6, Université de Montpellier, ; Place Eugène Bataillon, 34095 Montpellier, France
                [3 ]ISNI 0000 0001 2097 0141, GRID grid.121334.6, MARBEC, , Université de Montpellier, Ifremer-CNRS-IRD-UM, ; 34250 Palavas-les-Flots, France
                Author information
                http://orcid.org/0000-0003-3943-8061
                http://orcid.org/0000-0002-8232-904X
                Article
                4963
                10.1038/s41467-018-04963-6
                6023918
                29955054
                fdfff3ad-ddbc-4e65-8367-a305ed2b2a72
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 4 December 2017
                : 23 May 2018
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100001665, Agence Nationale de la Recherche (French National Research Agency);
                Award ID: 11-PDOC-009-01
                Award ID: ANR-17-CE02-0006-01
                Award Recipient :
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