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      Genomics and the origin of species.

      1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 , 9 , 10 , 11 , 12 , 8 , 13 , 14 , 15 , 16 , 17 , 18 , 19 , 4 , 20 , 21 , 17 , 22 , 21 , 23 , 24 , 25 , 26 , 27 , 28 , 29 , 14
      Nature reviews. Genetics
      Springer Nature

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          Abstract

          Speciation is a fundamental evolutionary process, the knowledge of which is crucial for understanding the origins of biodiversity. Genomic approaches are an increasingly important aspect of this research field. We review current understanding of genome-wide effects of accumulating reproductive isolation and of genomic properties that influence the process of speciation. Building on this work, we identify emergent trends and gaps in our understanding, propose new approaches to more fully integrate genomics into speciation research, translate speciation theory into hypotheses that are testable using genomic tools and provide an integrative definition of the field of speciation genomics.

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          Most cited references136

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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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              Chromosome inversions, local adaptation and speciation.

              We study the evolution of inversions that capture locally adapted alleles when two populations are exchanging migrants or hybridizing. By suppressing recombination between the loci, a new inversion can spread. Neither drift nor coadaptation between the alleles (epistasis) is needed, so this local adaptation mechanism may apply to a broader range of genetic and demographic situations than alternative hypotheses that have been widely discussed. The mechanism can explain many features observed in inversion systems. It will drive an inversion to high frequency if there is no countervailing force, which could explain fixed differences observed between populations and species. An inversion can be stabilized at an intermediate frequency if it also happens to capture one or more deleterious recessive mutations, which could explain polymorphisms that are common in some species. This polymorphism can cycle in frequency with the changing selective advantage of the locally favored alleles. The mechanism can establish underdominant inversions that decrease heterokaryotype fitness by several percent if the cause of fitness loss is structural, while if the cause is genic there is no limit to the strength of underdominance that can result. The mechanism is expected to cause loci responsible for adaptive species-specific differences to map to inversions, as seen in recent QTL studies. We discuss data that support the hypothesis, review other mechanisms for inversion evolution, and suggest possible tests.
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                Author and article information

                Journal
                Nat. Rev. Genet.
                Nature reviews. Genetics
                Springer Nature
                1471-0064
                1471-0056
                Mar 2014
                : 15
                : 3
                Affiliations
                [1 ] Department of Fish Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Switzerland; and Division of Aquatic Ecology and Evolution, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland.
                [2 ] Department of Animal and Plant Sciences, the University of Sheffield, Sheffield S10 2TN, UK; and the Sven Lovén Centre - Tjärnö, University of Gothenburg, S-452 96 Strömstad, Sweden.
                [3 ] Department of Fish Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Switzerland; the Division of Aquatic Ecology and Evolution, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland; and the Institute of Integrative Biology, ETH Zürich, ETH Zentrum CHN, 8092 Zürich, Switzerland.
                [4 ] Department of Fish Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Switzerland; and the Division of Aquatic Ecology and Evolution, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland.
                [5 ] Department of Fish Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Switzerland; and the Department of Zoology; Ecology, Evolutionary Biology and Behavior Program; BEACON Center, Michigan State University, 203 Natural Sciences, East Lansing, Michigan 48824, USA.
                [6 ] Department of Biological Sciences, Institute of Bioinformatics and Evolutionary Studies, University of Idaho, Moscow, Idaho 83844-3051, USA.
                [7 ] Division of Human Biology, Fred Hutchinson Cancer Research Center, Seattle, Washington 98109, USA.
                [8 ] Department of Biosciences, Centre for Ecological and Evolutionary Synthesis, University of Oslo, PO BOX 1066, Blindern, N-0316 Oslo, Norway.
                [9 ] School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland.
                [10 ] Integrated Science Laboratory and the Department of Mathematics and Mathematical Statistics, Umeå University, 90187 Umeå, Sweden.
                [11 ] Department of Ecology and Evolution, University of Lausanne, CH-1015 Lausanne, Switzerland.
                [12 ] Liverpool School of Tropical Medicine, Liverpool L3 5QA, UK.
                [13 ] Department of Biological Sciences, University of Notre Dame, Notre Dame, Indiana 46556-0369 USA.
                [14 ] Institute of Integrative Biology, ETH Zürich, ETH Zentrum CHN, 8092 Zürich, Switzerland.
                [15 ] Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, DK-1350 Copenhagen, Denmark. Present address: the Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, SE-752 36 Uppsala, Sweden.
                [16 ] Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, 78457 Konstanz, Germany.
                [17 ] Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK.
                [18 ] Friedrich Miescher Laboratory of the Max Planck Society, 72076 Tübingen, Germany.
                [19 ] Institute of Evolutionary Biology and Environmental Studies, University of Zurich, CH-8057 Zurich, Switzerland.
                [20 ] Behavioural Biology Group, Centre for Behaviour and Neurosciences, University of Groningen, PO BOX 11103, 9700 CC Groningen, The Netherlands.
                [21 ] Department of Fish Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Switzerland; the Division of Aquatic Ecology and Evolution, and the Computational and Molecular Population Genetics Laboratory, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland.
                [22 ] Department of Aquatic Ecology, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Switzerland.
                [23 ] Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK; and the Department of Aquatic Ecology, Eawag: Swiss Federal Institute of Aquatic Science and Technology, 8600 Dübendorf, Switzerland.
                [24 ] Museum of Vertebrate Zoology and Department of Integrative Biology, University of California, Berkeley, California 94720-3160, USA.
                [25 ] Integrated Science Laboratory and Department of Ecology and Environmental Science, Umeå University, 90187 Umeå, Sweden.
                [26 ] Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada.
                [27 ] Department of Fish Ecology and Evolution, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, 6047 Kastanienbaum, Switzerland; the Division of Aquatic Ecology and Evolution, Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland; and Zoologisches Forschungsmuseum Alexander Koenig, 53113 Bonn, Germany.
                [28 ] Department of Biology, The University of Texas at Arlington, 76010-0498 Texas, USA.
                [29 ] Department of Animal and Plant Sciences, the University of Sheffield, Sheffield S10 2TN, UK.
                Article
                nrg3644
                10.1038/nrg3644
                24535286
                698582cc-892a-406d-b73c-433971e15c00
                History

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