Comparative and demographic analysis of orang-utan genomes

Devin P. Locke, Ladeana W. Hillier, Wesley C. Warren, Kim C. Worley, Lynne V. Nazareth, Donna M. Muzny, Shiaw Pyng Yang, Zhengyuan Wang, Asif T. Chinwalla, Pat Minx, Makedonka Mitreva, Lisa Cook, Kim D. Delehaunty, Catrina Fronick, Heather Schmidt, Lucinda A. Fulton, Robert S. Fulton, Joanne O. Nelson, Vincent Magrini, Craig PohlTina A. Graves, Chris Markovic, Andy Cree, Huyen H. Dinh, Jennifer Hume, Christie L. Kovar, Gerald R. Fowler, Gerton Lunter, Stephen Meader, Andreas Heger, Chris P. Ponting, Tomas Marques-Bonet, Can Alkan, Lin Chen, Ze Cheng, Jeffrey M. Kidd, Evan E. Eichler, Simon White, Stephen Searle, Albert J. Vilella, Yuan Chen, Paul Flicek, Jian Ma, Brian Raney, Bernard Suh, Richard Burhans, Javier Herrero, David Haussler, Rui Faria, Olga Fernando, Fleur Darré, Doménec Farré, Elodie Gazave, Meritxell Oliva, Arcadi Navarro, Roberta Roberto, Oronzo Capozzi, Nicoletta Archidiacono, Giuliano Della Valle, Stefania Purgato, Mariano Rocchi, Miriam K. Konkel, Jerilyn A. Walker, Brygg Ullmer, Mark A. Batzer, Arian F A Smit, Robert Hubley, Claudio Casola, Daniel R. Schrider, Matthew W. Hahn, Victor Quesada, Xose S. Puente, Gonzalo R. Ordõez, Carlos Ĺpez-Otín, Tomas Vinar, Brona Brejova, Aakrosh Ratan, Robert S. Harris, Webb Miller, Carolin Kosiol, Heather A. Lawson, Vikas Taliwal, André L. Martins, Adam Siepel, Arindam Roychoudhury, Xin Ma, Jeremiah Degenhardt, Carlos D. Bustamante, Ryan N Gutenkunst, Thomas Mailund, Julien Y. Dutheil, Asger Hobolth, Mikkel H. Schierup, Oliver A. Ryder, Yuko Yoshinaga, Pieter J. De Jong, George M. Weinstock, Jeffrey Rogers, Elaine R. Mardis, Richard A. Gibbs, Richard K. Wilson

Research output: Contribution to journalArticle

301 Citations (Scopus)

Abstract

Orang-utan- is derived from a Malay term meaning man of the forest- and aptly describes the southeast Asian great apes native to Sumatra and Borneo. The orang-utan species, Pongo abelii (Sumatran) and Pongo pygmaeus (Bornean), are the most phylogenetically distant great apes from humans, thereby providing an informative perspective on hominid evolution. Here we present a Sumatran orang-utan draft genome assembly and short read sequence data from five Sumatran and five Bornean orang-utan genomes. Our analyses reveal that, compared to other primates, the orang-utan genome has many unique features. Structural evolution of the orang-utan genome has proceeded much more slowly than other great apes, evidenced by fewer rearrangements, less segmental duplication, a lower rate of gene family turnover and surprisingly quiescent Alu repeats, which have played a major role in restructuring other primate genomes. We also describe a primate polymorphic neocentromere, found in both Pongo species, emphasizing the gradual evolution of orang-utan genome structure. Orang-utans have extremely low energy usage for a eutherian mammal, far lower than their hominid relatives. Adding their genome to the repertoire of sequenced primates illuminates new signals of positive selection in several pathways including glycolipid metabolism. From the population perspective, both Pongo species are deeply diverse; however, Sumatran individuals possess greater diversity than their Bornean counterparts, and more species-specific variation. Our estimate of Bornean/Sumatran speciation time, 400,000years ago, is more recent than most previous studies and underscores the complexity of the orang-utan speciation process. Despite a smaller modern census population size, the Sumatran effective population size (N e) expanded exponentially relative to the ancestral N e after the split, while Bornean N e declined over the same period. Overall, the resources and analyses presented here offer new opportunities in evolutionary genomics, insights into hominid biology, and an extensive database of variation for conservation efforts.

Original languageEnglish (US)
Pages (from-to)529-533
Number of pages5
JournalNature
Volume469
Issue number7331
DOIs
StatePublished - Jan 27 2011

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Hominidae
Demography
Genome
Primates
Pongo
Population Density
Pongo abelii
Pongo pygmaeus
Borneo
Genomic Segmental Duplications
Indonesia
Glycolipids
Censuses
Genomics
Mammals
Databases
Population
Genes

ASJC Scopus subject areas

  • General

Cite this

Locke, D. P., Hillier, L. W., Warren, W. C., Worley, K. C., Nazareth, L. V., Muzny, D. M., ... Wilson, R. K. (2011). Comparative and demographic analysis of orang-utan genomes. Nature, 469(7331), 529-533. https://doi.org/10.1038/nature09687

Comparative and demographic analysis of orang-utan genomes. / Locke, Devin P.; Hillier, Ladeana W.; Warren, Wesley C.; Worley, Kim C.; Nazareth, Lynne V.; Muzny, Donna M.; Yang, Shiaw Pyng; Wang, Zhengyuan; Chinwalla, Asif T.; Minx, Pat; Mitreva, Makedonka; Cook, Lisa; Delehaunty, Kim D.; Fronick, Catrina; Schmidt, Heather; Fulton, Lucinda A.; Fulton, Robert S.; Nelson, Joanne O.; Magrini, Vincent; Pohl, Craig; Graves, Tina A.; Markovic, Chris; Cree, Andy; Dinh, Huyen H.; Hume, Jennifer; Kovar, Christie L.; Fowler, Gerald R.; Lunter, Gerton; Meader, Stephen; Heger, Andreas; Ponting, Chris P.; Marques-Bonet, Tomas; Alkan, Can; Chen, Lin; Cheng, Ze; Kidd, Jeffrey M.; Eichler, Evan E.; White, Simon; Searle, Stephen; Vilella, Albert J.; Chen, Yuan; Flicek, Paul; Ma, Jian; Raney, Brian; Suh, Bernard; Burhans, Richard; Herrero, Javier; Haussler, David; Faria, Rui; Fernando, Olga; Darré, Fleur; Farré, Doménec; Gazave, Elodie; Oliva, Meritxell; Navarro, Arcadi; Roberto, Roberta; Capozzi, Oronzo; Archidiacono, Nicoletta; Valle, Giuliano Della; Purgato, Stefania; Rocchi, Mariano; Konkel, Miriam K.; Walker, Jerilyn A.; Ullmer, Brygg; Batzer, Mark A.; Smit, Arian F A; Hubley, Robert; Casola, Claudio; Schrider, Daniel R.; Hahn, Matthew W.; Quesada, Victor; Puente, Xose S.; Ordõez, Gonzalo R.; Ĺpez-Otín, Carlos; Vinar, Tomas; Brejova, Brona; Ratan, Aakrosh; Harris, Robert S.; Miller, Webb; Kosiol, Carolin; Lawson, Heather A.; Taliwal, Vikas; Martins, André L.; Siepel, Adam; Roychoudhury, Arindam; Ma, Xin; Degenhardt, Jeremiah; Bustamante, Carlos D.; Gutenkunst, Ryan N; Mailund, Thomas; Dutheil, Julien Y.; Hobolth, Asger; Schierup, Mikkel H.; Ryder, Oliver A.; Yoshinaga, Yuko; De Jong, Pieter J.; Weinstock, George M.; Rogers, Jeffrey; Mardis, Elaine R.; Gibbs, Richard A.; Wilson, Richard K.

In: Nature, Vol. 469, No. 7331, 27.01.2011, p. 529-533.

Research output: Contribution to journalArticle

Locke, DP, Hillier, LW, Warren, WC, Worley, KC, Nazareth, LV, Muzny, DM, Yang, SP, Wang, Z, Chinwalla, AT, Minx, P, Mitreva, M, Cook, L, Delehaunty, KD, Fronick, C, Schmidt, H, Fulton, LA, Fulton, RS, Nelson, JO, Magrini, V, Pohl, C, Graves, TA, Markovic, C, Cree, A, Dinh, HH, Hume, J, Kovar, CL, Fowler, GR, Lunter, G, Meader, S, Heger, A, Ponting, CP, Marques-Bonet, T, Alkan, C, Chen, L, Cheng, Z, Kidd, JM, Eichler, EE, White, S, Searle, S, Vilella, AJ, Chen, Y, Flicek, P, Ma, J, Raney, B, Suh, B, Burhans, R, Herrero, J, Haussler, D, Faria, R, Fernando, O, Darré, F, Farré, D, Gazave, E, Oliva, M, Navarro, A, Roberto, R, Capozzi, O, Archidiacono, N, Valle, GD, Purgato, S, Rocchi, M, Konkel, MK, Walker, JA, Ullmer, B, Batzer, MA, Smit, AFA, Hubley, R, Casola, C, Schrider, DR, Hahn, MW, Quesada, V, Puente, XS, Ordõez, GR, Ĺpez-Otín, C, Vinar, T, Brejova, B, Ratan, A, Harris, RS, Miller, W, Kosiol, C, Lawson, HA, Taliwal, V, Martins, AL, Siepel, A, Roychoudhury, A, Ma, X, Degenhardt, J, Bustamante, CD, Gutenkunst, RN, Mailund, T, Dutheil, JY, Hobolth, A, Schierup, MH, Ryder, OA, Yoshinaga, Y, De Jong, PJ, Weinstock, GM, Rogers, J, Mardis, ER, Gibbs, RA & Wilson, RK 2011, 'Comparative and demographic analysis of orang-utan genomes', Nature, vol. 469, no. 7331, pp. 529-533. https://doi.org/10.1038/nature09687
Locke DP, Hillier LW, Warren WC, Worley KC, Nazareth LV, Muzny DM et al. Comparative and demographic analysis of orang-utan genomes. Nature. 2011 Jan 27;469(7331):529-533. https://doi.org/10.1038/nature09687
Locke, Devin P. ; Hillier, Ladeana W. ; Warren, Wesley C. ; Worley, Kim C. ; Nazareth, Lynne V. ; Muzny, Donna M. ; Yang, Shiaw Pyng ; Wang, Zhengyuan ; Chinwalla, Asif T. ; Minx, Pat ; Mitreva, Makedonka ; Cook, Lisa ; Delehaunty, Kim D. ; Fronick, Catrina ; Schmidt, Heather ; Fulton, Lucinda A. ; Fulton, Robert S. ; Nelson, Joanne O. ; Magrini, Vincent ; Pohl, Craig ; Graves, Tina A. ; Markovic, Chris ; Cree, Andy ; Dinh, Huyen H. ; Hume, Jennifer ; Kovar, Christie L. ; Fowler, Gerald R. ; Lunter, Gerton ; Meader, Stephen ; Heger, Andreas ; Ponting, Chris P. ; Marques-Bonet, Tomas ; Alkan, Can ; Chen, Lin ; Cheng, Ze ; Kidd, Jeffrey M. ; Eichler, Evan E. ; White, Simon ; Searle, Stephen ; Vilella, Albert J. ; Chen, Yuan ; Flicek, Paul ; Ma, Jian ; Raney, Brian ; Suh, Bernard ; Burhans, Richard ; Herrero, Javier ; Haussler, David ; Faria, Rui ; Fernando, Olga ; Darré, Fleur ; Farré, Doménec ; Gazave, Elodie ; Oliva, Meritxell ; Navarro, Arcadi ; Roberto, Roberta ; Capozzi, Oronzo ; Archidiacono, Nicoletta ; Valle, Giuliano Della ; Purgato, Stefania ; Rocchi, Mariano ; Konkel, Miriam K. ; Walker, Jerilyn A. ; Ullmer, Brygg ; Batzer, Mark A. ; Smit, Arian F A ; Hubley, Robert ; Casola, Claudio ; Schrider, Daniel R. ; Hahn, Matthew W. ; Quesada, Victor ; Puente, Xose S. ; Ordõez, Gonzalo R. ; Ĺpez-Otín, Carlos ; Vinar, Tomas ; Brejova, Brona ; Ratan, Aakrosh ; Harris, Robert S. ; Miller, Webb ; Kosiol, Carolin ; Lawson, Heather A. ; Taliwal, Vikas ; Martins, André L. ; Siepel, Adam ; Roychoudhury, Arindam ; Ma, Xin ; Degenhardt, Jeremiah ; Bustamante, Carlos D. ; Gutenkunst, Ryan N ; Mailund, Thomas ; Dutheil, Julien Y. ; Hobolth, Asger ; Schierup, Mikkel H. ; Ryder, Oliver A. ; Yoshinaga, Yuko ; De Jong, Pieter J. ; Weinstock, George M. ; Rogers, Jeffrey ; Mardis, Elaine R. ; Gibbs, Richard A. ; Wilson, Richard K. / Comparative and demographic analysis of orang-utan genomes. In: Nature. 2011 ; Vol. 469, No. 7331. pp. 529-533.
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abstract = "Orang-utan- is derived from a Malay term meaning man of the forest- and aptly describes the southeast Asian great apes native to Sumatra and Borneo. The orang-utan species, Pongo abelii (Sumatran) and Pongo pygmaeus (Bornean), are the most phylogenetically distant great apes from humans, thereby providing an informative perspective on hominid evolution. Here we present a Sumatran orang-utan draft genome assembly and short read sequence data from five Sumatran and five Bornean orang-utan genomes. Our analyses reveal that, compared to other primates, the orang-utan genome has many unique features. Structural evolution of the orang-utan genome has proceeded much more slowly than other great apes, evidenced by fewer rearrangements, less segmental duplication, a lower rate of gene family turnover and surprisingly quiescent Alu repeats, which have played a major role in restructuring other primate genomes. We also describe a primate polymorphic neocentromere, found in both Pongo species, emphasizing the gradual evolution of orang-utan genome structure. Orang-utans have extremely low energy usage for a eutherian mammal, far lower than their hominid relatives. Adding their genome to the repertoire of sequenced primates illuminates new signals of positive selection in several pathways including glycolipid metabolism. From the population perspective, both Pongo species are deeply diverse; however, Sumatran individuals possess greater diversity than their Bornean counterparts, and more species-specific variation. Our estimate of Bornean/Sumatran speciation time, 400,000years ago, is more recent than most previous studies and underscores the complexity of the orang-utan speciation process. Despite a smaller modern census population size, the Sumatran effective population size (N e) expanded exponentially relative to the ancestral N e after the split, while Bornean N e declined over the same period. Overall, the resources and analyses presented here offer new opportunities in evolutionary genomics, insights into hominid biology, and an extensive database of variation for conservation efforts.",
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T1 - Comparative and demographic analysis of orang-utan genomes

AU - Locke, Devin P.

AU - Hillier, Ladeana W.

AU - Warren, Wesley C.

AU - Worley, Kim C.

AU - Nazareth, Lynne V.

AU - Muzny, Donna M.

AU - Yang, Shiaw Pyng

AU - Wang, Zhengyuan

AU - Chinwalla, Asif T.

AU - Minx, Pat

AU - Mitreva, Makedonka

AU - Cook, Lisa

AU - Delehaunty, Kim D.

AU - Fronick, Catrina

AU - Schmidt, Heather

AU - Fulton, Lucinda A.

AU - Fulton, Robert S.

AU - Nelson, Joanne O.

AU - Magrini, Vincent

AU - Pohl, Craig

AU - Graves, Tina A.

AU - Markovic, Chris

AU - Cree, Andy

AU - Dinh, Huyen H.

AU - Hume, Jennifer

AU - Kovar, Christie L.

AU - Fowler, Gerald R.

AU - Lunter, Gerton

AU - Meader, Stephen

AU - Heger, Andreas

AU - Ponting, Chris P.

AU - Marques-Bonet, Tomas

AU - Alkan, Can

AU - Chen, Lin

AU - Cheng, Ze

AU - Kidd, Jeffrey M.

AU - Eichler, Evan E.

AU - White, Simon

AU - Searle, Stephen

AU - Vilella, Albert J.

AU - Chen, Yuan

AU - Flicek, Paul

AU - Ma, Jian

AU - Raney, Brian

AU - Suh, Bernard

AU - Burhans, Richard

AU - Herrero, Javier

AU - Haussler, David

AU - Faria, Rui

AU - Fernando, Olga

AU - Darré, Fleur

AU - Farré, Doménec

AU - Gazave, Elodie

AU - Oliva, Meritxell

AU - Navarro, Arcadi

AU - Roberto, Roberta

AU - Capozzi, Oronzo

AU - Archidiacono, Nicoletta

AU - Valle, Giuliano Della

AU - Purgato, Stefania

AU - Rocchi, Mariano

AU - Konkel, Miriam K.

AU - Walker, Jerilyn A.

AU - Ullmer, Brygg

AU - Batzer, Mark A.

AU - Smit, Arian F A

AU - Hubley, Robert

AU - Casola, Claudio

AU - Schrider, Daniel R.

AU - Hahn, Matthew W.

AU - Quesada, Victor

AU - Puente, Xose S.

AU - Ordõez, Gonzalo R.

AU - Ĺpez-Otín, Carlos

AU - Vinar, Tomas

AU - Brejova, Brona

AU - Ratan, Aakrosh

AU - Harris, Robert S.

AU - Miller, Webb

AU - Kosiol, Carolin

AU - Lawson, Heather A.

AU - Taliwal, Vikas

AU - Martins, André L.

AU - Siepel, Adam

AU - Roychoudhury, Arindam

AU - Ma, Xin

AU - Degenhardt, Jeremiah

AU - Bustamante, Carlos D.

AU - Gutenkunst, Ryan N

AU - Mailund, Thomas

AU - Dutheil, Julien Y.

AU - Hobolth, Asger

AU - Schierup, Mikkel H.

AU - Ryder, Oliver A.

AU - Yoshinaga, Yuko

AU - De Jong, Pieter J.

AU - Weinstock, George M.

AU - Rogers, Jeffrey

AU - Mardis, Elaine R.

AU - Gibbs, Richard A.

AU - Wilson, Richard K.

PY - 2011/1/27

Y1 - 2011/1/27

N2 - Orang-utan- is derived from a Malay term meaning man of the forest- and aptly describes the southeast Asian great apes native to Sumatra and Borneo. The orang-utan species, Pongo abelii (Sumatran) and Pongo pygmaeus (Bornean), are the most phylogenetically distant great apes from humans, thereby providing an informative perspective on hominid evolution. Here we present a Sumatran orang-utan draft genome assembly and short read sequence data from five Sumatran and five Bornean orang-utan genomes. Our analyses reveal that, compared to other primates, the orang-utan genome has many unique features. Structural evolution of the orang-utan genome has proceeded much more slowly than other great apes, evidenced by fewer rearrangements, less segmental duplication, a lower rate of gene family turnover and surprisingly quiescent Alu repeats, which have played a major role in restructuring other primate genomes. We also describe a primate polymorphic neocentromere, found in both Pongo species, emphasizing the gradual evolution of orang-utan genome structure. Orang-utans have extremely low energy usage for a eutherian mammal, far lower than their hominid relatives. Adding their genome to the repertoire of sequenced primates illuminates new signals of positive selection in several pathways including glycolipid metabolism. From the population perspective, both Pongo species are deeply diverse; however, Sumatran individuals possess greater diversity than their Bornean counterparts, and more species-specific variation. Our estimate of Bornean/Sumatran speciation time, 400,000years ago, is more recent than most previous studies and underscores the complexity of the orang-utan speciation process. Despite a smaller modern census population size, the Sumatran effective population size (N e) expanded exponentially relative to the ancestral N e after the split, while Bornean N e declined over the same period. Overall, the resources and analyses presented here offer new opportunities in evolutionary genomics, insights into hominid biology, and an extensive database of variation for conservation efforts.

AB - Orang-utan- is derived from a Malay term meaning man of the forest- and aptly describes the southeast Asian great apes native to Sumatra and Borneo. The orang-utan species, Pongo abelii (Sumatran) and Pongo pygmaeus (Bornean), are the most phylogenetically distant great apes from humans, thereby providing an informative perspective on hominid evolution. Here we present a Sumatran orang-utan draft genome assembly and short read sequence data from five Sumatran and five Bornean orang-utan genomes. Our analyses reveal that, compared to other primates, the orang-utan genome has many unique features. Structural evolution of the orang-utan genome has proceeded much more slowly than other great apes, evidenced by fewer rearrangements, less segmental duplication, a lower rate of gene family turnover and surprisingly quiescent Alu repeats, which have played a major role in restructuring other primate genomes. We also describe a primate polymorphic neocentromere, found in both Pongo species, emphasizing the gradual evolution of orang-utan genome structure. Orang-utans have extremely low energy usage for a eutherian mammal, far lower than their hominid relatives. Adding their genome to the repertoire of sequenced primates illuminates new signals of positive selection in several pathways including glycolipid metabolism. From the population perspective, both Pongo species are deeply diverse; however, Sumatran individuals possess greater diversity than their Bornean counterparts, and more species-specific variation. Our estimate of Bornean/Sumatran speciation time, 400,000years ago, is more recent than most previous studies and underscores the complexity of the orang-utan speciation process. Despite a smaller modern census population size, the Sumatran effective population size (N e) expanded exponentially relative to the ancestral N e after the split, while Bornean N e declined over the same period. Overall, the resources and analyses presented here offer new opportunities in evolutionary genomics, insights into hominid biology, and an extensive database of variation for conservation efforts.

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