Gibbon genome and the fast karyotype evolution of small apes

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; Nicoletta Archidiacono; Carl Baker; Daniel Barrell; Mark A Batzer; Kathryn Beal; Antoine Blancher; Craig L Bohrson; Markus Brameier; Michael S Campbell; Oronzo Capozzi; Claudio Casola; Giorgia Chiatante; Andrew Cree; Annette Damert; Pieter J de Jong; Laura Dumas; Marcos Fernandez-Callejo; Paul Flicek; Nina V Fuchs; Ivo Gut; Marta Gut; Matthew W Hahn; Jessica Hernandez-Rodriguez; LaDeana W Hillier; Robert Hubley; Bianca Ianc; Zsuzsanna Izsvák; Nina G Jablonski; Laurel M Johnstone; Anis Karimpour-Fard; Miriam K Konkel; Dennis Kostka; Nathan H Lazar; Sandra L Lee; Lora R Lewis; Yue Liu; Devin P Locke; Swapan Mallick; Fernando L Mendez; Matthieu Muffato; Lynne V Nazareth; Kimberly A Nevonen; Majesta O'Bleness; Cornelia Ochis; Duncan T Odom; Katherine S Pollard; Javier Quilez; David Reich; Mariano Rocchi; Gerald G Schumann; Stephen Searle; James M Sikela; Gabriella Skollar; Arian Smit; Kemal Sonmez; Boudewijn ten Hallers; Elizabeth Terhune; Gregg W C Thomas; Brygg Ullmer; Mario Ventura; Jerilyn A Walker; Jeffrey D Wall; Lutz Walter; Michelle C Ward; Sarah J Wheelan; Christopher W Whelan; Simon White; Larry J Wilhelm; August E Woerner; Mark Yandell; Baoli Zhu; Michael F Hammer; Tomas Marques-Bonet; Evan E Eichler; Lucinda Fulton; Catrina Fronick; Donna M Muzny; Wesley C Warren; Kim C Worley; Jeffrey Rogers; Richard K Wilson; Richard A Gibbs

doi:10.1038/nature13679

Gibbon genome and the fast karyotype evolution of small apes

Nature. 2014 Sep 11;513(7517):195-201. doi: 10.1038/nature13679.

Authors

Lucia Carbone¹, R Alan Harris², Sante Gnerre³, Krishna R Veeramah⁴, Belen Lorente-Galdos⁵, John Huddleston⁶, Thomas J Meyer⁷, Javier Herrero⁸, Christian Roos⁹, Bronwen Aken¹⁰, Fabio Anaclerio¹¹, Nicoletta Archidiacono¹¹, Carl Baker¹², Daniel Barrell¹⁰, Mark A Batzer¹³, Kathryn Beal¹⁴, Antoine Blancher¹⁵, Craig L Bohrson¹⁶, Markus Brameier⁹, Michael S Campbell¹⁷, Oronzo Capozzi¹¹, Claudio Casola¹⁸, Giorgia Chiatante¹¹, Andrew Cree¹⁹, Annette Damert²⁰, Pieter J de Jong²¹, Laura Dumas²², Marcos Fernandez-Callejo⁵, Paul Flicek¹⁴, Nina V Fuchs²³, Ivo Gut²⁴, Marta Gut²⁴, Matthew W Hahn²⁵, Jessica Hernandez-Rodriguez⁵, LaDeana W Hillier²⁶, Robert Hubley²⁷, Bianca Ianc²⁰, Zsuzsanna Izsvák²³, Nina G Jablonski²⁸, Laurel M Johnstone²⁹, Anis Karimpour-Fard²², Miriam K Konkel¹³, Dennis Kostka³⁰, Nathan H Lazar³¹, Sandra L Lee¹⁹, Lora R Lewis¹⁹, Yue Liu¹⁹, Devin P Locke³², Swapan Mallick³³, Fernando L Mendez³⁴, Matthieu Muffato¹⁴, Lynne V Nazareth¹⁹, Kimberly A Nevonen³⁵, Majesta O'Bleness²², Cornelia Ochis²⁰, Duncan T Odom³⁶, Katherine S Pollard³⁷, Javier Quilez⁵, David Reich³³, Mariano Rocchi¹¹, Gerald G Schumann³⁸, Stephen Searle³⁹, James M Sikela²², Gabriella Skollar⁴⁰, Arian Smit²⁶, Kemal Sonmez⁴¹, Boudewijn ten Hallers⁴², Elizabeth Terhune³⁵, Gregg W C Thomas²⁵, Brygg Ullmer⁴³, Mario Ventura¹¹, Jerilyn A Walker¹³, Jeffrey D Wall⁴⁴, Lutz Walter⁹, Michelle C Ward⁴⁵, Sarah J Wheelan¹⁶, Christopher W Whelan⁴⁶, Simon White³⁹, Larry J Wilhelm³⁵, August E Woerner²⁹, Mark Yandell¹⁷, Baoli Zhu⁴², Michael F Hammer²⁹, Tomas Marques-Bonet⁴⁷, Evan E Eichler⁶, Lucinda Fulton²⁶, Catrina Fronick²⁶, Donna M Muzny¹⁹, Wesley C Warren²⁶, Kim C Worley¹⁹, Jeffrey Rogers¹⁹, Richard K Wilson²⁶, Richard A Gibbs¹⁹

Affiliations

¹ 1] Oregon Health &Science University, Department of Behavioral Neuroscience, 3181 SW Sam Jackson Park Road Portland, Oregon 97239, USA. [2] Oregon National Primate Research Center, Division of Neuroscience, 505 NW 185th Avenue, Beaverton, Oregon 97006, USA. [3] Oregon Health &Science University, Department of Molecular &Medical Genetics, 3181 SW Sam Jackson Park Road, Portland, Oregon 97239, USA. [4] Oregon Health &Science University, Bioinformatics and Computational Biology Division, Department of Medical Informatics &Clinical Epidemiology, 3181 SW Sam Jackson Park Road, Portland, Oregon 97239, USA.
² Baylor College of Medicine, Department of Molecular and Human Genetics, One Baylor Plaza, Houston, Texas 77030, USA.
³ Nabsys, 60 Clifford Street, Providence, Rhode Island 02903, USA.
⁴ 1] University of Arizona, ARL Division of Biotechnology, Tucson, Arizona 85721, USA. [2] Stony Brook University, Department of Ecology and Evolution, Stony Brook, New York 11790, USA.
⁵ IBE, Institut de Biologia Evolutiva (UPF-CSIC), Universitat Pompeu Fabra, PRBB, Doctor Aiguader, 88, 08003 Barcelona, Spain.
⁶ 1] Department of Genome Sciences, University of Washington School of Medicine, Seattle, Washington 98195, USA. [2] Howard Hughes Medical Institute, 1705 NE Pacific Street, Seattle, Washington 98195, USA.
⁷ Oregon Health &Science University, Department of Behavioral Neuroscience, 3181 SW Sam Jackson Park Road Portland, Oregon 97239, USA.
⁸ 1] European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK. [2] The Genome Analysis Centre, Norwich Research Park, Norwich NR4 7UH, UK. [3] 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.).
⁹ Leibniz Institute for Primate Research, Gene Bank of Primates, German Primate Center, Göttingen 37077, Germany.
¹⁰ 1] European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK. [2] European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.
¹¹ University of Bari, Department of Biology, Via Orabona 4, 70125, Bari, Italy.
¹² Department of Genome Sciences, University of Washington School of Medicine, Seattle, Washington 98195, USA.
¹³ Louisiana State University, Department of Biological Sciences, Baton Rouge, Louisiana 70803, USA.
¹⁴ European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.
¹⁵ University of Paul Sabatier, Toulouse 31062, France.
¹⁶ The Johns Hopkins University School of Medicine, Department of Oncology, Division of Biostatistics and Bioinformatics, Baltimore, Maryland 21205, USA.
¹⁷ University of Utah, Salt Lake City, Utah 84112, USA.
¹⁸ Texas A&M University, Department of Ecosystem Science and Management, College Station, Texas 77843, USA.
¹⁹ Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA.
²⁰ Babes-Bolyai-University, Institute for Interdisciplinary Research in Bio-Nano-Sciences, Molecular Biology Center, Cluj-Napoca 400084, Romania.
²¹ Children's Hospital Oakland Research Institute, BACPAC Resources, Oakland, California 94609, USA.
²² University of Colorado School of Medicine, Department of Biochemistry and Molecular Genetics, Aurora, Colorado 80045, USA.
²³ Max Delbrück Center for Molecular Medicine, Berlin 13125, Germany.
²⁴ Centro Nacional de Análisis Genómico (CNAG), Parc Científic de Barcelona, Barcelona 08028, Spain.
²⁵ Indiana University, School of Informatics and Computing, Bloomington, Indiana 47408, USA.
²⁶ The Genome Center at Washington University, Washington University School of Medicine, 4444 Forest Park Avenue, Saint Louis, Missouri 63108, USA.
²⁷ Institute for Systems Biology, Seattle, Washington 98109-5234, USA.
²⁸ The Pennsylvania State University, Department of Anthropology, University Park, Pennsylvania 16802, USA.
²⁹ University of Arizona, ARL Division of Biotechnology, Tucson, Arizona 85721, USA.
³⁰ University of Pittsburgh School of Medicine, Department of Developmental Biology, Department of Computational and Systems Biology, Pittsburg, Pennsylvania 15261, USA.
³¹ Oregon Health &Science University, Bioinformatics and Computational Biology Division, Department of Medical Informatics &Clinical Epidemiology, 3181 SW Sam Jackson Park Road, Portland, Oregon 97239, USA.
³² 1] The Genome Center at Washington University, Washington University School of Medicine, 4444 Forest Park Avenue, Saint Louis, Missouri 63108, USA. [2] 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.).
³³ Harvard Medical School, Department of Genetics, Boston, Massachusetts 02115, USA.
³⁴ 1] University of Arizona, ARL Division of Biotechnology, Tucson, Arizona 85721, USA. [2] 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.).
³⁵ Oregon National Primate Research Center, Division of Neuroscience, 505 NW 185th Avenue, Beaverton, Oregon 97006, USA.
³⁶ 1] European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK. [2] University of Cambridge, Cancer Research UK-Cambridge Institute, Cambridge CB2 0RE, UK.
³⁷ 1] University of California, Gladstone Institutes, San Francisco, California 94158-226, USA. [2] Institute for Human Genetics, University of California, San Francisco, California 94143-0794, USA. [3] Division of Biostatistics, University of California, San Francisco, California 94143-0794, USA.
³⁸ Paul Ehrlich Institute, Division of Medical Biotechnology, 63225 Langen, Germany.
³⁹ European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SD, UK.
⁴⁰ Gibbon Conservation Center, 19100 Esguerra Rd, Santa Clarita, California 91350, USA.
⁴¹ 1] Oregon Health &Science University, Bioinformatics and Computational Biology Division, Department of Medical Informatics &Clinical Epidemiology, 3181 SW Sam Jackson Park Road, Portland, Oregon 97239, USA. [2] Oregon Health &Science University, Center for Spoken Language Understanding, Institute on Development and Disability, Portland, Oregon 97239, USA.
⁴² 1] Children's Hospital Oakland Research Institute, BACPAC Resources, Oakland, California 94609, USA. [2] 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.).
⁴³ Louisiana State University, School of Electrical Engineering and Computer Science, Baton Rouge, Louisiana 70803, USA.
⁴⁴ 1] Institute for Human Genetics, University of California, San Francisco, California 94143-0794, USA. [2] Division of Biostatistics, University of California, San Francisco, California 94143-0794, USA.
⁴⁵ 1] University of Cambridge, Cancer Research UK-Cambridge Institute, Cambridge CB2 0RE, UK. [2] 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.).
⁴⁶ 1] Oregon Health &Science University, Center for Spoken Language Understanding, Institute on Development and Disability, Portland, Oregon 97239, USA. [2] 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.).
⁴⁷ 1] IBE, Institut de Biologia Evolutiva (UPF-CSIC), Universitat Pompeu Fabra, PRBB, Doctor Aiguader, 88, 08003 Barcelona, Spain. [2] Centro Nacional de Análisis Genómico (CNAG), Parc Científic de Barcelona, Barcelona 08028, Spain.

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.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Evolution, Molecular
Genome / genetics*
Hominidae / classification
Hominidae / genetics
Humans
Hylobates / classification*
Hylobates / genetics*
Karyotype*
Molecular Sequence Data
Phylogeny*
Retroelements / genetics
Selection, Genetic
Transcription Termination, Genetic

Gibbon genome and the fast karyotype evolution of small apes

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