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 & 73 others 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, Mustafa (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

Research output: Contribution to journalArticle

119 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)195-201
Number of pages7
JournalNature
Volume513
Issue number7517
DOIs
StatePublished - Sep 11 2014

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Hylobates
Hominidae
Karyotype
Genome
Ecosystem
Cercopithecidae
Retroelements
Chromosome Segregation
Southeastern Asia
Forelimb
Phylogeny
Connective Tissue
Primates
Genes

ASJC Scopus subject areas

  • General

Cite this

Carbone, L., Alan Harris, R., Gnerre, S., Veeramah, K. R., Lorente-Galdos, B., Huddleston, J., ... Gibbs, R. A. (2014). Gibbon genome and the fast karyotype evolution of small apes. Nature, 513(7517), 195-201. https://doi.org/10.1038/nature13679

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

In: Nature, Vol. 513, No. 7517, 11.09.2014, p. 195-201.

Research output: Contribution to journalArticle

Carbone, L, Alan Harris, R, Gnerre, S, Veeramah, KR, Lorente-Galdos, B, Huddleston, J, Meyer, TJ, Herrero, J, Roos, C, Aken, B, Anaclerio, F, Archidiacono, N, Baker, C, Barrell, D, Batzer, MA, Beal, K, Blancher, A, Bohrson, CL, Brameier, M, Campbell, MS, Capozzi, O, Casola, C, Chiatante, G, Cree, A, Damert, A, De Jong, PJ, Dumas, L, Fernandez-Callejo, M, Flicek, P, Fuchs, NV, Gut, I, Gut, M, Hahn, MW, Hernandez-Rodriguez, J, Hillier, LW, Hubley, R, Ianc, B, Izsvák, Z, Jablonski, NG, Johnstone, LM, Karimpour-Fard, A, Konkel, MK, Kostka, D, Lazar, NH, Lee, SL, Lewis, LR, Liu, Y, Locke, DP, Mallick, S, Mendez, FL, Muffato, M, Nazareth, LV, Nevonen, KA, O'Bleness, M, Ochis, C, Odom, DT, Pollard, KS, Quilez, J, Reich, D, Rocchi, M, Schumann, GG, Searle, S, Sikela, JM, Skollar, G, Smit, A, Sonmez, MK, Ten Hallers, B, Terhune, E, Thomas, GWC, Ullmer, B, Ventura, M, Walker, JA, Wall, JD, Walter, L, Ward, MC, Wheelan, SJ, Whelan, CW, White, S, Wilhelm, LJ, Woerner, AE, Yandell, M, Zhu, B, Hammer, MF, Marques-Bonet, T, Eichler, EE, Fulton, L, Fronick, C, Muzny, DM, Warren, WC, Worley, KC, Rogers, J, Wilson, RK & Gibbs, RA 2014, 'Gibbon genome and the fast karyotype evolution of small apes', Nature, vol. 513, no. 7517, pp. 195-201. https://doi.org/10.1038/nature13679
Carbone L, Alan Harris R, Gnerre S, Veeramah KR, Lorente-Galdos B, Huddleston J et al. Gibbon genome and the fast karyotype evolution of small apes. Nature. 2014 Sep 11;513(7517):195-201. https://doi.org/10.1038/nature13679
Carbone, Lucia ; Alan Harris, R. ; Gnerre, Sante ; Veeramah, Krishna R. ; Lorente-Galdos, Belen ; Huddleston, John ; Meyer, Thomas J. ; Herrero, Javier ; Roos, Christian ; Aken, Bronwen ; Anaclerio, Fabio ; Archidiacono, Nicoletta ; Baker, Carl ; Barrell, Daniel ; Batzer, Mark A. ; Beal, Kathryn ; Blancher, Antoine ; Bohrson, Craig L. ; Brameier, Markus ; Campbell, Michael S. ; Capozzi, Oronzo ; Casola, Claudio ; Chiatante, Giorgia ; Cree, Andrew ; Damert, Annette ; De Jong, Pieter J. ; Dumas, Laura ; Fernandez-Callejo, Marcos ; Flicek, Paul ; Fuchs, Nina V. ; Gut, Ivo ; Gut, Marta ; Hahn, Matthew W. ; Hernandez-Rodriguez, Jessica ; Hillier, Ladeana W. ; Hubley, Robert ; Ianc, Bianca ; Izsvák, Zsuzsanna ; Jablonski, Nina G. ; Johnstone, Laurel M. ; Karimpour-Fard, Anis ; Konkel, Miriam K. ; Kostka, Dennis ; Lazar, Nathan H. ; Lee, Sandra L. ; Lewis, Lora R. ; Liu, Yue ; Locke, Devin P. ; Mallick, Swapan ; Mendez, Fernando L. ; Muffato, Matthieu ; Nazareth, Lynne V. ; Nevonen, Kimberly A. ; O'Bleness, Majesta ; Ochis, Cornelia ; Odom, Duncan T. ; Pollard, Katherine S. ; Quilez, Javier ; Reich, David ; Rocchi, Mariano ; Schumann, Gerald G. ; Searle, Stephen ; Sikela, James M. ; Skollar, Gabriella ; Smit, Arian ; Sonmez, Mustafa (Kemal) ; Ten Hallers, Boudewijn ; Terhune, Elizabeth ; Thomas, Gregg W C ; Ullmer, Brygg ; Ventura, Mario ; Walker, Jerilyn A. ; Wall, Jeffrey D. ; Walter, Lutz ; Ward, Michelle C. ; Wheelan, Sarah J. ; Whelan, Christopher W. ; White, Simon ; Wilhelm, Larry J. ; Woerner, August E. ; Yandell, Mark ; Zhu, Baoli ; Hammer, Michael F. ; Marques-Bonet, Tomas ; Eichler, Evan E. ; Fulton, Lucinda ; Fronick, Catrina ; Muzny, Donna M. ; Warren, Wesley C. ; Worley, Kim C. ; Rogers, Jeffrey ; Wilson, Richard K. ; Gibbs, Richard A. / Gibbon genome and the fast karyotype evolution of small apes. In: Nature. 2014 ; Vol. 513, No. 7517. pp. 195-201.
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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.",
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T1 - Gibbon genome and the fast karyotype evolution of small apes

AU - Carbone, Lucia

AU - Alan Harris, R.

AU - Gnerre, Sante

AU - Veeramah, Krishna R.

AU - Lorente-Galdos, Belen

AU - Huddleston, John

AU - Meyer, Thomas J.

AU - Herrero, Javier

AU - Roos, Christian

AU - Aken, Bronwen

AU - Anaclerio, Fabio

AU - Archidiacono, Nicoletta

AU - Baker, Carl

AU - Barrell, Daniel

AU - Batzer, Mark A.

AU - Beal, Kathryn

AU - Blancher, Antoine

AU - Bohrson, Craig L.

AU - Brameier, Markus

AU - Campbell, Michael S.

AU - Capozzi, Oronzo

AU - Casola, Claudio

AU - Chiatante, Giorgia

AU - Cree, Andrew

AU - Damert, Annette

AU - De Jong, Pieter J.

AU - Dumas, Laura

AU - Fernandez-Callejo, Marcos

AU - Flicek, Paul

AU - Fuchs, Nina V.

AU - Gut, Ivo

AU - Gut, Marta

AU - Hahn, Matthew W.

AU - Hernandez-Rodriguez, Jessica

AU - Hillier, Ladeana W.

AU - Hubley, Robert

AU - Ianc, Bianca

AU - Izsvák, Zsuzsanna

AU - Jablonski, Nina G.

AU - Johnstone, Laurel M.

AU - Karimpour-Fard, Anis

AU - Konkel, Miriam K.

AU - Kostka, Dennis

AU - Lazar, Nathan H.

AU - Lee, Sandra L.

AU - Lewis, Lora R.

AU - Liu, Yue

AU - Locke, Devin P.

AU - Mallick, Swapan

AU - Mendez, Fernando L.

AU - Muffato, Matthieu

AU - Nazareth, Lynne V.

AU - Nevonen, Kimberly A.

AU - O'Bleness, Majesta

AU - Ochis, Cornelia

AU - Odom, Duncan T.

AU - Pollard, Katherine S.

AU - Quilez, Javier

AU - Reich, David

AU - Rocchi, Mariano

AU - Schumann, Gerald G.

AU - Searle, Stephen

AU - Sikela, James M.

AU - Skollar, Gabriella

AU - Smit, Arian

AU - Sonmez, Mustafa (Kemal)

AU - Ten Hallers, Boudewijn

AU - Terhune, Elizabeth

AU - Thomas, Gregg W C

AU - Ullmer, Brygg

AU - Ventura, Mario

AU - Walker, Jerilyn A.

AU - Wall, Jeffrey D.

AU - Walter, Lutz

AU - Ward, Michelle C.

AU - Wheelan, Sarah J.

AU - Whelan, Christopher W.

AU - White, Simon

AU - Wilhelm, Larry J.

AU - Woerner, August E.

AU - Yandell, Mark

AU - Zhu, Baoli

AU - Hammer, Michael F.

AU - Marques-Bonet, Tomas

AU - Eichler, Evan E.

AU - Fulton, Lucinda

AU - Fronick, Catrina

AU - Muzny, Donna M.

AU - Warren, Wesley C.

AU - Worley, Kim C.

AU - Rogers, Jeffrey

AU - Wilson, Richard K.

AU - Gibbs, Richard A.

PY - 2014/9/11

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N2 - 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.

AB - 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.

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