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Gibbon genome and the fast karyotype evolution of small apes

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  • Lucia Carbone

    (Oregon Health & Science University, 3181 SW Sam Jackson Park Road Portland, Oregon 97239, USA.
    Oregon National Primate Research Center, 505 NW 185th Avenue, Beaverton, Oregon 97006, USA.
    Oregon Health & Science University, 3181 SW Sam Jackson Park Road, Portland, Oregon 97239, USA.
    Oregon Health & Science University, 3181 SW Sam Jackson Park Road, Portland, Oregon 97239, USA.)

  • R. Alan Harris

    (Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA.)

  • Sante Gnerre

    (Nabsys, 60 Clifford Street, Providence, Rhode Island 02903, USA.)

  • Krishna R. Veeramah

    (University of Arizona
    Stony Brook University, Stony Brook, New York 11790, USA.)

  • Belen Lorente-Galdos

    (IBE, Institut de Biologia Evolutiva (UPF-CSIC), Universitat Pompeu Fabra, PRBB, Doctor Aiguader, 88, 08003 Barcelona, Spain.)

  • John Huddleston

    (University of Washington School of Medicine
    Howard Hughes Medical Institute, 1705 NE Pacific Street, Seattle, Washington 98195, USA.)

  • Thomas J. Meyer

    (Oregon Health & Science University, 3181 SW Sam Jackson Park Road Portland, Oregon 97239, USA.)

  • Javier Herrero

    (European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.
    The Genome Analysis Centre, Norwich Research Park, Norwich NR4 7UH, UK.
    Present addresses: Bill Lyons Informatics Center, UCL Cancer Institute, University College London, London WC1E 6DD, UK (J.He); Seven Bridges Genomics, Cambridge, Massachusetts 02138, USA (D.P.L.); Department of Genetics, Stanford University School of Medicine, Stanford, California 94305, USA (F.L.M.); BioNano Genomics, San Diego, California 92121, USA (B.t.H.); University of Chicago, Department of Human Genetics, Chicago, Illinois 60637, USA (M.C.W.); Stanley Center for Psychiatric Research, Broad Institute, Cambridge, Massachusetts 02138, USA (C.W.W.); The CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China (B.Z.).)

  • Christian Roos

    (Leibniz Institute for Primate Research, Gene Bank of Primates, German Primate Center, Göttingen 37077, Germany.)

  • Bronwen Aken

    (European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.
    European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.)

  • Fabio Anaclerio

    (University of Bari, Via Orabona 4, 70125, Bari, Italy.)

  • Nicoletta Archidiacono

    (University of Bari, Via Orabona 4, 70125, Bari, Italy.)

  • Carl Baker

    (University of Washington School of Medicine)

  • Daniel Barrell

    (European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.
    European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.)

  • Mark A. Batzer

    (Louisiana State University)

  • Kathryn Beal

    (European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.)

  • Antoine Blancher

    (University of Paul Sabatier, Toulouse 31062, France.)

  • Craig L. Bohrson

    (The Johns Hopkins University School of Medicine)

  • Markus Brameier

    (Leibniz Institute for Primate Research, Gene Bank of Primates, German Primate Center, Göttingen 37077, Germany.)

  • Michael S. Campbell

    (University of Utah, Salt Lake City, Utah 84112, USA.)

  • Oronzo Capozzi

    (University of Bari, Via Orabona 4, 70125, Bari, Italy.)

  • Claudio Casola

    (Texas A&M University)

  • Giorgia Chiatante

    (University of Bari, Via Orabona 4, 70125, Bari, Italy.)

  • Andrew Cree

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA.)

  • Annette Damert

    (Babes-Bolyai-University, Institute for Interdisciplinary Research in Bio-Nano-Sciences, Molecular Biology Center, Cluj-Napoca 400084, Romania.)

  • Pieter J. de Jong

    (Children’s Hospital Oakland Research Institute, BACPAC Resources)

  • Laura Dumas

    (University of Colorado School of Medicine)

  • Marcos Fernandez-Callejo

    (IBE, Institut de Biologia Evolutiva (UPF-CSIC), Universitat Pompeu Fabra, PRBB, Doctor Aiguader, 88, 08003 Barcelona, Spain.)

  • Paul Flicek

    (European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.)

  • Nina V. Fuchs

    (Max Delbrück Center for Molecular Medicine, Berlin 13125, Germany.)

  • Ivo Gut

    (Centro Nacional de Análisis Genómico (CNAG), Parc Científic de Barcelona, Barcelona 08028, Spain.)

  • Marta Gut

    (Centro Nacional de Análisis Genómico (CNAG), Parc Científic de Barcelona, Barcelona 08028, Spain.)

  • Matthew W. Hahn

    (Indiana University, School of Informatics and Computing)

  • Jessica Hernandez-Rodriguez

    (IBE, Institut de Biologia Evolutiva (UPF-CSIC), Universitat Pompeu Fabra, PRBB, Doctor Aiguader, 88, 08003 Barcelona, Spain.)

  • LaDeana W. Hillier

    (The Genome Center at Washington University, Washington University School of Medicine, 4444 Forest Park Avenue, Saint Louis, Missouri 63108, USA.)

  • Robert Hubley

    (Institute for Systems Biology)

  • Bianca Ianc

    (Babes-Bolyai-University, Institute for Interdisciplinary Research in Bio-Nano-Sciences, Molecular Biology Center, Cluj-Napoca 400084, Romania.)

  • Zsuzsanna Izsvák

    (Max Delbrück Center for Molecular Medicine, Berlin 13125, Germany.)

  • Nina G. Jablonski

    (The Pennsylvania State University, University Park)

  • Laurel M. Johnstone

    (University of Arizona)

  • Anis Karimpour-Fard

    (University of Colorado School of Medicine)

  • Miriam K. Konkel

    (Louisiana State University)

  • Dennis Kostka

    (University of Pittsburgh School of Medicine)

  • Nathan H. Lazar

    (Oregon Health & Science University, 3181 SW Sam Jackson Park Road, Portland, Oregon 97239, USA.)

  • Sandra L. Lee

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA.)

  • Lora R. Lewis

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA.)

  • Yue Liu

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA.)

  • Devin P. Locke

    (The Genome Center at Washington University, Washington University School of Medicine, 4444 Forest Park Avenue, Saint Louis, Missouri 63108, USA.
    Present addresses: Bill Lyons Informatics Center, UCL Cancer Institute, University College London, London WC1E 6DD, UK (J.He); Seven Bridges Genomics, Cambridge, Massachusetts 02138, USA (D.P.L.); Department of Genetics, Stanford University School of Medicine, Stanford, California 94305, USA (F.L.M.); BioNano Genomics, San Diego, California 92121, USA (B.t.H.); University of Chicago, Department of Human Genetics, Chicago, Illinois 60637, USA (M.C.W.); Stanley Center for Psychiatric Research, Broad Institute, Cambridge, Massachusetts 02138, USA (C.W.W.); The CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China (B.Z.).)

  • Swapan Mallick

    (Harvard Medical School)

  • Fernando L. Mendez

    (University of Arizona
    Present addresses: Bill Lyons Informatics Center, UCL Cancer Institute, University College London, London WC1E 6DD, UK (J.He); Seven Bridges Genomics, Cambridge, Massachusetts 02138, USA (D.P.L.); Department of Genetics, Stanford University School of Medicine, Stanford, California 94305, USA (F.L.M.); BioNano Genomics, San Diego, California 92121, USA (B.t.H.); University of Chicago, Department of Human Genetics, Chicago, Illinois 60637, USA (M.C.W.); Stanley Center for Psychiatric Research, Broad Institute, Cambridge, Massachusetts 02138, USA (C.W.W.); The CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China (B.Z.).)

  • Matthieu Muffato

    (European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.)

  • Lynne V. Nazareth

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA.)

  • Kimberly A. Nevonen

    (Oregon National Primate Research Center, 505 NW 185th Avenue, Beaverton, Oregon 97006, USA.)

  • Majesta O’Bleness

    (University of Colorado School of Medicine)

  • Cornelia Ochis

    (Babes-Bolyai-University, Institute for Interdisciplinary Research in Bio-Nano-Sciences, Molecular Biology Center, Cluj-Napoca 400084, Romania.)

  • Duncan T. Odom

    (European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.
    University of Cambridge, Cancer Research UK-Cambridge Institute, Cambridge CB2 0RE, UK.)

  • Katherine S. Pollard

    (University of California, Gladstone Institutes
    Institute for Human Genetics, University of California
    University of California)

  • Javier Quilez

    (IBE, Institut de Biologia Evolutiva (UPF-CSIC), Universitat Pompeu Fabra, PRBB, Doctor Aiguader, 88, 08003 Barcelona, Spain.)

  • David Reich

    (Harvard Medical School)

  • Mariano Rocchi

    (University of Bari, Via Orabona 4, 70125, Bari, Italy.)

  • Gerald G. Schumann

    (Paul Ehrlich Institute, 63225 Langen, Germany.)

  • Stephen Searle

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

  • James M. Sikela

    (University of Colorado School of Medicine)

  • Gabriella Skollar

    (Gibbon Conservation Center, 19100 Esguerra Rd, Santa Clarita, California 91350, USA.)

  • Arian Smit

    (The Genome Center at Washington University, Washington University School of Medicine, 4444 Forest Park Avenue, Saint Louis, Missouri 63108, USA.)

  • Kemal Sonmez

    (Oregon Health & Science University, 3181 SW Sam Jackson Park Road, Portland, Oregon 97239, USA.
    Oregon Health & Science University, Center for Spoken Language Understanding, Institute on Development and Disability)

  • Boudewijn ten Hallers

    (Children’s Hospital Oakland Research Institute, BACPAC Resources
    Present addresses: Bill Lyons Informatics Center, UCL Cancer Institute, University College London, London WC1E 6DD, UK (J.He); Seven Bridges Genomics, Cambridge, Massachusetts 02138, USA (D.P.L.); Department of Genetics, Stanford University School of Medicine, Stanford, California 94305, USA (F.L.M.); BioNano Genomics, San Diego, California 92121, USA (B.t.H.); University of Chicago, Department of Human Genetics, Chicago, Illinois 60637, USA (M.C.W.); Stanley Center for Psychiatric Research, Broad Institute, Cambridge, Massachusetts 02138, USA (C.W.W.); The CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China (B.Z.).)

  • Elizabeth Terhune

    (Oregon National Primate Research Center, 505 NW 185th Avenue, Beaverton, Oregon 97006, USA.)

  • Gregg W. C. Thomas

    (Indiana University, School of Informatics and Computing)

  • Brygg Ullmer

    (Louisiana State University, School of Electrical Engineering and Computer Science)

  • Mario Ventura

    (University of Bari, Via Orabona 4, 70125, Bari, Italy.)

  • Jerilyn A. Walker

    (Louisiana State University)

  • Jeffrey D. Wall

    (Institute for Human Genetics, University of California
    University of California)

  • Lutz Walter

    (Leibniz Institute for Primate Research, Gene Bank of Primates, German Primate Center, Göttingen 37077, Germany.)

  • Michelle C. Ward

    (University of Cambridge, Cancer Research UK-Cambridge Institute, Cambridge CB2 0RE, UK.
    Present addresses: Bill Lyons Informatics Center, UCL Cancer Institute, University College London, London WC1E 6DD, UK (J.He); Seven Bridges Genomics, Cambridge, Massachusetts 02138, USA (D.P.L.); Department of Genetics, Stanford University School of Medicine, Stanford, California 94305, USA (F.L.M.); BioNano Genomics, San Diego, California 92121, USA (B.t.H.); University of Chicago, Department of Human Genetics, Chicago, Illinois 60637, USA (M.C.W.); Stanley Center for Psychiatric Research, Broad Institute, Cambridge, Massachusetts 02138, USA (C.W.W.); The CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China (B.Z.).)

  • Sarah J. Wheelan

    (The Johns Hopkins University School of Medicine)

  • Christopher W. Whelan

    (Oregon Health & Science University, Center for Spoken Language Understanding, Institute on Development and Disability
    Present addresses: Bill Lyons Informatics Center, UCL Cancer Institute, University College London, London WC1E 6DD, UK (J.He); Seven Bridges Genomics, Cambridge, Massachusetts 02138, USA (D.P.L.); Department of Genetics, Stanford University School of Medicine, Stanford, California 94305, USA (F.L.M.); BioNano Genomics, San Diego, California 92121, USA (B.t.H.); University of Chicago, Department of Human Genetics, Chicago, Illinois 60637, USA (M.C.W.); Stanley Center for Psychiatric Research, Broad Institute, Cambridge, Massachusetts 02138, USA (C.W.W.); The CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China (B.Z.).)

  • Simon White

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

  • Larry J. Wilhelm

    (Oregon National Primate Research Center, 505 NW 185th Avenue, Beaverton, Oregon 97006, USA.)

  • August E. Woerner

    (University of Arizona)

  • Mark Yandell

    (University of Utah, Salt Lake City, Utah 84112, USA.)

  • Baoli Zhu

    (Children’s Hospital Oakland Research Institute, BACPAC Resources
    Present addresses: Bill Lyons Informatics Center, UCL Cancer Institute, University College London, London WC1E 6DD, UK (J.He); Seven Bridges Genomics, Cambridge, Massachusetts 02138, USA (D.P.L.); Department of Genetics, Stanford University School of Medicine, Stanford, California 94305, USA (F.L.M.); BioNano Genomics, San Diego, California 92121, USA (B.t.H.); University of Chicago, Department of Human Genetics, Chicago, Illinois 60637, USA (M.C.W.); Stanley Center for Psychiatric Research, Broad Institute, Cambridge, Massachusetts 02138, USA (C.W.W.); The CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China (B.Z.).)

  • Michael F. Hammer

    (University of Arizona)

  • Tomas Marques-Bonet

    (IBE, Institut de Biologia Evolutiva (UPF-CSIC), Universitat Pompeu Fabra, PRBB, Doctor Aiguader, 88, 08003 Barcelona, Spain.
    Centro Nacional de Análisis Genómico (CNAG), Parc Científic de Barcelona, Barcelona 08028, Spain.)

  • Evan E. Eichler

    (University of Washington School of Medicine
    Howard Hughes Medical Institute, 1705 NE Pacific Street, Seattle, Washington 98195, USA.)

  • Lucinda Fulton

    (The Genome Center at Washington University, Washington University School of Medicine, 4444 Forest Park Avenue, Saint Louis, Missouri 63108, USA.)

  • Catrina Fronick

    (The Genome Center at Washington University, Washington University School of Medicine, 4444 Forest Park Avenue, Saint Louis, Missouri 63108, USA.)

  • Donna M. Muzny

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA.)

  • Wesley C. Warren

    (The Genome Center at Washington University, Washington University School of Medicine, 4444 Forest Park Avenue, Saint Louis, Missouri 63108, USA.)

  • Kim C. Worley

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA.)

  • Jeffrey Rogers

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA.)

  • Richard K. Wilson

    (The Genome Center at Washington University, Washington University School of Medicine, 4444 Forest Park Avenue, Saint Louis, Missouri 63108, USA.)

  • Richard A. Gibbs

    (Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA.)

Abstract

Gibbons are small arboreal apes that display an accelerated rate of evolutionary chromosomal rearrangement and occupy a key node in the primate phylogeny between Old World monkeys and great apes. Here we present the assembly and analysis of a northern white-cheeked gibbon (Nomascus leucogenys) genome. We describe the propensity for a gibbon-specific retrotransposon (LAVA) to insert into chromosome segregation genes and alter transcription by providing a premature termination site, suggesting a possible molecular mechanism for the genome plasticity of the gibbon lineage. We further show that the gibbon genera (Nomascus, Hylobates, Hoolock and Symphalangus) experienced a near-instantaneous radiation ∼5 million years ago, coincident with major geographical changes in southeast Asia that caused cycles of habitat compression and expansion. Finally, we identify signatures of positive selection in genes important for forelimb development (TBX5) and connective tissues (COL1A1) that may have been involved in the adaptation of gibbons to their arboreal habitat.

Suggested Citation

  • Lucia Carbone & R. Alan Harris & Sante Gnerre & Krishna R. Veeramah & Belen Lorente-Galdos & John Huddleston & Thomas J. Meyer & Javier Herrero & Christian Roos & Bronwen Aken & Fabio Anaclerio & Nico, 2014. "Gibbon genome and the fast karyotype evolution of small apes," Nature, Nature, vol. 513(7517), pages 195-201, September.
    • Handle: RePEc:nat:nature:v:513:y:2014:i:7517:d:10.1038_nature13679
    DOI: 10.1038/nature13679
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    Cited by:

    1. Yuan Yin & Huizhong Fan & Botong Zhou & Yibo Hu & Guangyi Fan & Jinhuan Wang & Fan Zhou & Wenhui Nie & Chenzhou Zhang & Lin Liu & Zhenyu Zhong & Wenbo Zhu & Guichun Liu & Zeshan Lin & Chang Liu & Jion, 2021. "Molecular mechanisms and topological consequences of drastic chromosomal rearrangements of muntjac deer," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    2. Mariam Okhovat & Jake VanCampen & Kimberly A. Nevonen & Lana Harshman & Weiyu Li & Cora E. Layman & Samantha Ward & Jarod Herrera & Jackson Wells & Rory R. Sheng & Yafei Mao & Blaise Ndjamen & Ana C. , 2023. "TAD evolutionary and functional characterization reveals diversity in mammalian TAD boundary properties and function," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

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