Gibbon genome and the fast karyotype evolution of small apes

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 gibbon genome project was funded by the National Human Genome Research Institute (NHGRI) including grants U54 HG003273 (R.A.G.) and U54 HG003079 (R.K.W.) with further support from National Institutes of Health NIH/NIAAA P30 AA019355 and NIH/NCRR P51 RR000163 (L.C.), R01_HG005226 (J.D.W., M.F.H.), NIH P30CA006973 (S.J.W.), a fellowship from the National Library of Medicine Biomedical Informatics Research Training Program (N.H.L.), R01 GM59290 (M.A.B.) and U41 HG007497-01 (M.A.B, M.K.K.), R01 MH081203 (J.M.S.), HG002385 (E.E.E.), National Science Foundation (NSF) CNS-1126739 (B.U., M.A.B., M.K.K.) and DBI-0845494 (M.W.H.), PRIN 2012 (M.R.), Futuro in ricerca 2010 RBFR103CE3 (M.V.), ERC Starting Grant (260372) and MICINN (Spain) BFU2011-28549 (T.M.-B.), grant of the Ministry of National Education, CNCS – UEFISCDI, project number PN-II-ID-PCE-2012-4-0090 (A.D.), grant of the Deutsche Forschungsgemeinschaft SCHU1014/8-1 (G.G.S.), ERC Starting and Advanced Grant and EMBO Young Investigator Award (Z.I., N.V.F.), ERC Starting Grant and EMBO Young Investigator Award (D.T.O.), Commonwealth Scholarship Commission (M.C.W.). E.E.E. is an investigator of the Howard Hughes Medical Institute. We acknowledge the contributions of the staff of the HGSC, including the operations team: H. Dinh, S. Jhangiani V. Korchina, C. Kovar; the library team: K. Blankenburg, L. Pu, S. Vattathil; the assembly team: D. Rio-Deiros, H. Jiang; the submissions team: M. Batterton, D. Kalra, K. Wilczek-Boney, W. Hale, G. Fowler, J. Zhang; the quality control team: P. Aqrawi, S. Gross, V. Joshi, J. Santibanez; and the sequence production team: U. Anosike, C. Babu, D. Bandaranaike, B. Beltran, D. Berhane-Mersha, C. Bickham, T. Bolden, M. Dao, M. Davila, L. Davy-Carroll, S. Denson, P. Fernando, C. Francis, R. Garcia III, B. Hollins, B. Johnson, J. Jones, J. Kalu, N. Khan, B. Leal, F. Legall III, Y. Liu, J. Lopez, R. Mata, M. Obregon, C. Onwere, A. Parra, Y. Perez, A. Perez, C. Pham, J. Quiroz, S. Ruiz, M. Scheel, D. Simmons, I. Sisson, J. Tisius, G. Toledanes, R. Varghese, V. Vee, D. Walker, C. White, A. Williams, R. Wright, T. Attaway, T. Garrett, C. Mercado, N. Ngyen, H. Paul and Z. Trejos. We thank Z. Ivics for providing some of the reagents. We additionally acknowledge the Production Sequencing Group at The Genome Institute. Wellcome Trust (grant numbers WT095908 and WT098051), NHGRI (U41HG007234) and European Molecular Biology Laboratory. For the production of next-generation sequences, we acknowledge the Massively Parallel Sequencing Shared Resources (MPSSR) at OHSU, the National Center of Genomic Analyses (CNAG) (Barcelona, Spain), the University of Arizona Genetics Core (UAGC), and the UCSF sequencing core. We also acknowledge the Louisiana Optical Network Institute (LONI). We thank the Gibbon Conservation Center and the Fort Wayne Children’s Zoo for providing the gibbon samples. The MAKER annotation pipeline is supported by NSF IOS-1126998.We thank T. Brown for proofreading and editing the manuscript