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The genomic basis of adaptive evolution in threespine sticklebacks

Author

Listed:
  • Felicity C. Jones

    (Beckman Center B300, Stanford University School of Medicine)

  • Manfred G. Grabherr

    (Broad Institute of MIT and Harvard, 7 Cambridge Center
    Science for Life Laboratory Uppsala, Uppsala University, Uppsala 751 23, Sweden)

  • Yingguang Frank Chan

    (Beckman Center B300, Stanford University School of Medicine
    Present addresses: Max Planck Institute for Evolutionary Biology, August-Thienemann-Str. 2, Plön 24306, Germany (Y.F.C.); Children's Hospital Boston, Genetic Diagnostic Lab, 300 Longwood Avenue, Boston, Massachusetts 02115, USA (E.M.); Bioinformatics Core, Zuckerman Research Center, New York, New York 10065, USA (M.P.); Department of Molecular & Cell Biology, 142 LSA 3200, University of California, Berkeley, California 94720, USA (C.T.M.).)

  • Pamela Russell

    (Broad Institute of MIT and Harvard, 7 Cambridge Center)

  • Evan Mauceli

    (Broad Institute of MIT and Harvard, 7 Cambridge Center
    Present addresses: Max Planck Institute for Evolutionary Biology, August-Thienemann-Str. 2, Plön 24306, Germany (Y.F.C.); Children's Hospital Boston, Genetic Diagnostic Lab, 300 Longwood Avenue, Boston, Massachusetts 02115, USA (E.M.); Bioinformatics Core, Zuckerman Research Center, New York, New York 10065, USA (M.P.); Department of Molecular & Cell Biology, 142 LSA 3200, University of California, Berkeley, California 94720, USA (C.T.M.).)

  • Jeremy Johnson

    (Broad Institute of MIT and Harvard, 7 Cambridge Center)

  • Ross Swofford

    (Broad Institute of MIT and Harvard, 7 Cambridge Center)

  • Mono Pirun

    (Broad Institute of MIT and Harvard, 7 Cambridge Center
    Present addresses: Max Planck Institute for Evolutionary Biology, August-Thienemann-Str. 2, Plön 24306, Germany (Y.F.C.); Children's Hospital Boston, Genetic Diagnostic Lab, 300 Longwood Avenue, Boston, Massachusetts 02115, USA (E.M.); Bioinformatics Core, Zuckerman Research Center, New York, New York 10065, USA (M.P.); Department of Molecular & Cell Biology, 142 LSA 3200, University of California, Berkeley, California 94720, USA (C.T.M.).)

  • Michael C. Zody

    (Broad Institute of MIT and Harvard, 7 Cambridge Center)

  • Simon White

    (Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK)

  • Ewan Birney

    (European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK)

  • Stephen Searle

    (Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK)

  • Jeremy Schmutz

    (HudsonAlpha Institute for Biotechnology, 601 Genome Way, Huntsville, Alabama 35806, USA)

  • Jane Grimwood

    (HudsonAlpha Institute for Biotechnology, 601 Genome Way, Huntsville, Alabama 35806, USA)

  • Mark C. Dickson

    (HudsonAlpha Institute for Biotechnology, 601 Genome Way, Huntsville, Alabama 35806, USA)

  • Richard M. Myers

    (HudsonAlpha Institute for Biotechnology, 601 Genome Way, Huntsville, Alabama 35806, USA)

  • Craig T. Miller

    (Beckman Center B300, Stanford University School of Medicine
    Present addresses: Max Planck Institute for Evolutionary Biology, August-Thienemann-Str. 2, Plön 24306, Germany (Y.F.C.); Children's Hospital Boston, Genetic Diagnostic Lab, 300 Longwood Avenue, Boston, Massachusetts 02115, USA (E.M.); Bioinformatics Core, Zuckerman Research Center, New York, New York 10065, USA (M.P.); Department of Molecular & Cell Biology, 142 LSA 3200, University of California, Berkeley, California 94720, USA (C.T.M.).)

  • Brian R. Summers

    (Beckman Center B300, Stanford University School of Medicine)

  • Anne K. Knecht

    (Beckman Center B300, Stanford University School of Medicine)

  • Shannon D. Brady

    (Beckman Center B300, Stanford University School of Medicine)

  • Haili Zhang

    (Beckman Center B300, Stanford University School of Medicine)

  • Alex A. Pollen

    (Beckman Center B300, Stanford University School of Medicine)

  • Timothy Howes

    (Beckman Center B300, Stanford University School of Medicine)

  • Chris Amemiya

    (Benaroya Research Institute at Virginia Mason, 1201 Ninth Avenue, Seattle Washington 98101, USA)

  • Eric S. Lander

    (Broad Institute of MIT and Harvard, 7 Cambridge Center)

  • Federica Di Palma

    (Broad Institute of MIT and Harvard, 7 Cambridge Center)

  • Kerstin Lindblad-Toh

    (Broad Institute of MIT and Harvard, 7 Cambridge Center
    Science for Life Laboratory Uppsala, Uppsala University, Uppsala 751 23, Sweden)

  • David M. Kingsley

    (Beckman Center B300, Stanford University School of Medicine
    Howard Hughes Medical Institute, Stanford University)

Abstract

Marine stickleback fish have colonized and adapted to thousands of 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 twenty 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 indicate that reuse of globally shared standing genetic variation, including chromosomal inversions, has 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, but regulatory changes appear to predominate in this well known example of repeated adaptive evolution in nature.

Suggested Citation

  • Felicity C. Jones & Manfred G. Grabherr & Yingguang Frank Chan & Pamela Russell & Evan Mauceli & Jeremy Johnson & Ross Swofford & Mono Pirun & Michael C. Zody & Simon White & Ewan Birney & Stephen Sea, 2012. "The genomic basis of adaptive evolution in threespine sticklebacks," Nature, Nature, vol. 484(7392), pages 55-61, April.
    • Handle: RePEc:nat:nature:v:484:y:2012:i:7392:d:10.1038_nature10944
    DOI: 10.1038/nature10944
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    Cited by:

    1. David B. Stern & Nathan W. Anderson & Juanita A. Diaz & Carol Eunmi Lee, 2022. "Genome-wide signatures of synergistic epistasis during parallel adaptation in a Baltic Sea copepod," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Georgios A. Gkafas & Joanne Sarantopoulou & Chrysoula Apostologamvrou & Chryssanthi Antoniadou & Athanasios Exadactylos & Georgios Fleris & Dimitris Vafidis, 2023. "Admixture of Holothurian Species in the Hellenic Seas (Eastern Mediterranean) as Revealed by RADseq," Sustainability, MDPI, vol. 15(15), pages 1-12, July.
    3. Julio Diaz Caballero & Rachel M. Wheatley & Natalia Kapel & Carla López-Causapé & Thomas Van der Schalk & Angus Quinn & Liam P. Shaw & Lois Ogunlana & Claudia Recanatini & Basil Britto Xavier & Leen T, 2023. "Mixed strain pathogen populations accelerate the evolution of antibiotic resistance in patients," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    4. Rishi De-Kayne & Oliver M. Selz & David A. Marques & David Frei & Ole Seehausen & Philine G. D. Feulner, 2022. "Genomic architecture of adaptive radiation and hybridization in Alpine whitefish," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    5. Gabriela Montejo-Kovacevich & Joana I. Meier & Caroline N. Bacquet & Ian A. Warren & Yingguang Frank Chan & Marek Kucka & Camilo Salazar & Nicol Rueda-M & Stephen H. Montgomery & W. Owen McMillan & Kr, 2022. "Repeated genetic adaptation to altitude in two tropical butterflies," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    6. Julian Petersen & Lukas Englmaier & Artem V. Artemov & Irina Poverennaya & Ruba Mahmoud & Thibault Bouderlique & Marketa Tesarova & Ruslan Deviatiiarov & Anett Szilvásy-Szabó & Evgeny E. Akkuratov & D, 2023. "A previously uncharacterized Factor Associated with Metabolism and Energy (FAME/C14orf105/CCDC198/1700011H14Rik) is related to evolutionary adaptation, energy balance, and kidney physiology," Nature Communications, Nature, vol. 14(1), pages 1-22, December.

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