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

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. CampbellOronzo 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

Research output: Contribution to journal › Article

142 Scopus citations

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 language	English (US)
Pages (from-to)	195-201
Number of pages	7
Journal	Nature
Volume	513
Issue number	7517
DOIs	https://doi.org/10.1038/nature13679
State	Published - Sep 11 2014

ASJC Scopus subject areas

General

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Carbone, L., Alan Harris, R., Gnerre, S., Veeramah, K. R., Lorente-Galdos, B., Huddleston, J., Meyer, T. J., Herrero, J., Roos, C., Aken, B., Anaclerio, F., Archidiacono, N., Baker, C., Barrell, D., Batzer, M. A., Beal, K., Blancher, A., Bohrson, C. L., Brameier, M., ... 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, 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 journal › Article

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, K, 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, 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, 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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title = "Gibbon genome and the fast karyotype evolution of small apes",

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.",

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

year = "2014",

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day = "11",

doi = "10.1038/nature13679",

language = "English (US)",

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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, 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

Y1 - 2014/9/11

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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