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      PARALLEL EVOLUTION OF LOCAL ADAPTATION AND REPRODUCTIVE ISOLATION IN THE FACE OF GENE FLOW

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          Abstract

          Parallel evolution of similar phenotypes provides strong evidence for the operation of natural selection. Where these phenotypes contribute to reproductive isolation, they further support a role for divergent, habitat-associated selection in speciation. However, the observation of pairs of divergent ecotypes currently occupying contrasting habitats in distinct geographical regions is not sufficient to infer parallel origins. Here we show striking parallel phenotypic divergence between populations of the rocky-shore gastropod, Littorina saxatilis, occupying contrasting habitats exposed to either wave action or crab predation. This divergence is associated with barriers to gene exchange but, nevertheless, genetic variation is more strongly structured by geography than by ecotype. Using approximate Bayesian analysis of sequence data and amplified fragment length polymorphism markers, we show that the ecotypes are likely to have arisen in the face of continuous gene flow and that the demographic separation of ecotypes has occurred in parallel at both regional and local scales. Parameter estimates suggest a long delay between colonization of a locality and ecotype formation, perhaps because the postglacial spread of crab populations was slower than the spread of snails. Adaptive differentiation may not be fully genetically independent despite being demographically parallel. These results provide new insight into a major model of ecologically driven speciation.

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          Most cited references83

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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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              DnaSP, DNA polymorphism analyses by the coalescent and other methods.

              DnaSP is a software package for the analysis of DNA polymorphism data. Present version introduces several new modules and features which, among other options allow: (1) handling big data sets (approximately 5 Mb per sequence); (2) conducting a large number of coalescent-based tests by Monte Carlo computer simulations; (3) extensive analyses of the genetic differentiation and gene flow among populations; (4) analysing the evolutionary pattern of preferred and unpreferred codons; (5) generating graphical outputs for an easy visualization of results. The software package, including complete documentation and examples, is freely available to academic users from: http://www.ub.es/dnasp

                Author and article information

                Journal
                Evolution
                Evolution
                evo
                Evolution; International Journal of Organic Evolution
                BlackWell Publishing Ltd (Oxford, UK )
                0014-3820
                1558-5646
                April 2014
                23 December 2013
                : 68
                : 4
                : 935-949
                Affiliations
                [1 ]Animal and Plant Sciences, The University of Sheffield Sheffield S10 2TN, United Kingdom
                [2 ]Biological and Environmental Sciences-Tjärnö, University of Gothenburg SE-452 96, Strömstad, Sweden
                [3 ] E-mail: r.k.butlin@ 123456sheffield.ac.uk
                [4 ]Departamento de Bioquímica, Genética e Inmunología, Facultad de Biología, Universidade de Vigo 36310 Vigo, Spain
                [5 ]Departamento Mejora Genética INIA Crta. La Coruña Km 7.5, 28040 Madrid, Spain
                [6 ]Present address: LEMAR (UMR 6539), European Institute for Marine Studies, University of Western Brittany, Technopôle Brest-Iroise, rue Dumont d'Urville 29280 Plouzané, France
                [7 ]Department of Ecology and Evolution, University of Chicago Chicago, Illinosis, 60637
                [8 ]School of Biology, University of Leeds Leeds LS2 9JT, United Kingdom
                [9 ]Department of Biology, Lund University SE-223 62 Lund, Sweden
                [10 ]Faculty of Life Sciences, Manchester University Manchester M13 9PT, United Kingdom
                [11 ]Present address: Molecular Oncology Unit, Basic Research Department, CIEMAT Av. Complutense, 40, 28040 Madrid, Spain
                [12 ]Department of Ecology and Evolutionary Biology, University of California Irvine, 92697, California
                Author notes
                * These authors contributed equally.
                † These authors contributed equally.

                Associate Editor: J. Wares

                Article
                10.1111/evo.12329
                4261988
                24299519
                2064576a-96a4-4249-8599-1c70b62ff4d9
                © 2013 The Authors. Evolution published by Wiley Periodicals, Inc. on behalf of The Society for the Study of Evolution.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 09 August 2013
                : 06 November 2013
                Categories
                Original Articles

                Evolutionary Biology
                gene flow,local adaptation,parallel evolution,speciation
                Evolutionary Biology
                gene flow, local adaptation, parallel evolution, speciation

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