Gibbon genome and the fast karyotype evolution of small apes

Lucia Carbone(Oregon Health & Science University), R. Alan Harris(Baylor College of Medicine), Sante Gnerre(Providence College), Krishna R. Veeramah(University of Arizona), Belén Lorente-Galdós(Universitat Pompeu Fabra), John Huddleston(Howard Hughes Medical Institute), Thomas J. Meyer(Oregon Health & Science University), Javier Herrero(European Bioinformatics Institute), Christian Roos(German Primate Center), Bronwen Aken(European Bioinformatics Institute), Fabio Anaclerio(University of Bari Aldo Moro), Nicoletta Archidiacono(University of Bari Aldo Moro), Carl Baker(University of Washington), Daniel Barrell(European Bioinformatics Institute), Mark A. Batzer(Louisiana State University), Kathryn Beal(European Bioinformatics Institute), Antoine Blancher(Université Toulouse III - Paul Sabatier), Craig L. Bohrson(Johns Hopkins University), Markus Brameier(German Primate Center), Michael S. Campbell(University of Utah), Oronzo Capozzi(University of Bari Aldo Moro), Claudio Casola(Texas A&M University), Giorgia Chiatante(University of Bari Aldo Moro), Andrew Cree(Baylor College of Medicine), Annette Damert(Babeș-Bolyai University), Pieter J. de Jong(Children’s Institute), Laura Dumas(University of Colorado Denver), Marcos Fernández-Callejo(Universitat Pompeu Fabra), Paul Flicek(European Bioinformatics Institute), Nina V. Fuchs(Max Delbrück Center), Marta Gut(Centro Nacional de Análisis Genómico), Marta Gut(Centro Nacional de Análisis Genómico), Matthew W. Hahn(Indiana University Bloomington), Jessica Hernández-Rodríguez(Universitat Pompeu Fabra), LaDeana W. Hillier(Washington University in St. Louis), Robert Hubley(Institute for Systems Biology), Bianca Ianc(Babeș-Bolyai University), Zsuzsanna Izsvák(Max Delbrück Center), Nina G. Jablonski(Pennsylvania State University), Laurel Johnstone(University of Arizona), Anis Karimpour‐Fard(University of Colorado Denver), Miriam K. Konkel(Louisiana State University), Dennis Kostka(University of Pittsburgh), Nathan H. Lazar(Oregon Health & Science University), Sandra L. Lee(Baylor College of Medicine), Lora Lewis(Baylor College of Medicine), Yue Liu(Baylor College of Medicine), Devin P. Locke(Washington University in St. Louis), Swapan Mallick(Harvard University), Fernando L. Méndez(University of Arizona), Matthieu Muffato(European Bioinformatics Institute), Lynne V. Nazareth(Baylor College of Medicine), Kimberly A. Nevonen(Oregon National Primate Research Center), Majesta O’Bleness(University of Colorado Denver), Cornelia Ochis(Babeș-Bolyai University), Duncan T. Odom(European Bioinformatics Institute), Katherine S. Pollard(Gladstone Institutes), Javier Quilez(Universitat Pompeu Fabra), David Reich(Harvard University), Mariano Rocchi(University of Bari Aldo Moro), Gerald G. Schumann(Paul Ehrlich Institut), Stephen M. J. Searle(European Bioinformatics Institute), James M. Sikela(University of Colorado Denver), Gabriella Skollár(College of the Canyons), Arian F. A. Smit(Washington University in St. Louis), Kemal Sönmez(Oregon Health & Science University), Boudewijn ten Hallers(Genomics England), Elizabeth Terhune(Oregon National Primate Research Center), Gregg W.C. Thomas(Indiana University Bloomington), Brygg Ullmer(Louisiana State University), Mario Ventura(University of Bari Aldo Moro), Jerilyn A. Walker(Louisiana State University), Jeffrey D. Wall(University of California, San Francisco), Lutz Walter(German Primate Center), Michelle C. Ward(University of Cambridge), Sarah J. Wheelan(Johns Hopkins University), Christopher W. Whelan(Oregon Health & Science University), Simon White(European Bioinformatics Institute), Larry Wilhelm(Oregon National Primate Research Center), August E. Woerner(University of Arizona), Mark Yandell(University of Utah), Baoli Zhu(Genomics England), Michael F. Hammer(University of Arizona), Tomàs Marquès‐Bonet(Institut de Biologia Evolutiva), Evan E. Eichler(Howard Hughes Medical Institute), Lucinda A. Fulton(Washington University in St. Louis), Catrina C. Fronick(Washington University in St. Louis), Donna M. Muzny(Baylor College of Medicine), Wesley C. Warren(Washington University in St. Louis), Kim C. Worley(Baylor College of Medicine), Jeffrey Rogers(Baylor College of Medicine), Richard K. Wilson(Washington University in St. Louis), Richard A. Gibbs(Baylor College of Medicine)
Nature
September 9, 2014
Cited by 393Open Access
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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. The genome of the gibbon, a tree-dwelling ape from Asia positioned between Old World monkeys and the great apes, is presented, providing insights into the evolutionary history of gibbon species and their accelerated karyotypes, as well as evidence for selection of genes such as those for forelimb development and connective tissue that may be important for locomotion through trees. The many species of gibbons are small, tree-living apes from Southeast Asia, most of them listed as 'endangered' or 'critically endangered' on the IUCN list. In their presentation of the genome of the northern white-cheeked gibbon (Nomascus leucogenys) , Lucia Carbone and colleagues provide intriguing insights into the biology and evolutionary history of a group that straddles the divide between Old World monkeys and the great apes. The authors investigate how a novel gibbon-specific retrotransposon might be the source of gibbons' genome plasticity. Rapid karyotype evolution combined with multiple episodes of climate and environmental change might explain the almost instantaneous divergence of the four gibbon genera. Positive selection on genes involved in forelimb development and connective tissue might have been related to gibbons' unique mode of locomotion in the tropical canopy.


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