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 and Richard A. Gibbs
Additional contact information
Lucia Carbone: 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
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
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.
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.
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.
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.
Swapan Mallick: Harvard Medical School
Fernando L. Mendez: University of Arizona
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.
Katherine S. Pollard: University of California, Gladstone Institutes
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.
Boudewijn ten Hallers: Children’s Hospital Oakland Research Institute, BACPAC Resources
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
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.
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
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
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.
Evan E. Eichler: University of Washington School of Medicine
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.

Nature, 2014, vol. 513, issue 7517, 195-201

Abstract: 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.

Date: 2014
References: Add references at CitEc
Citations: View citations in EconPapers (2)

Downloads: (external link)
https://www.nature.com/articles/nature13679 Abstract (text/html)
Access to the full text of the articles in this series is restricted.

Related works:
This item may be available elsewhere in EconPapers: Search for items with the same title.

Export reference: BibTeX RIS (EndNote, ProCite, RefMan) HTML/Text

Persistent link: https://EconPapers.repec.org/RePEc:nat:nature:v:513:y:2014:i:7517:d:10.1038_nature13679

Ordering information: This journal article can be ordered from
https://www.nature.com/

DOI: 10.1038/nature13679

Access Statistics for this article

Nature is currently edited by Magdalena Skipper

More articles in Nature from Nature
Bibliographic data for series maintained by Sonal Shukla () and Springer Nature Abstracting and Indexing ().