Insights into hominid evolution from the gorilla genome sequence

Aylwyn Scally; Julien Y. Dutheil; Ladeana W. Hillier; Gregory E. Jordan; Ian Goodhead; Javier Herrero; Asger Hobolth; Tuuli Lappalainen; Thomas Mailund; Tomas Marques-Bonet; Shane McCarthy; Stephen H. Montgomery; Petra C. Schwalie; Y. Amy Tang; Michelle C. Ward; Yali Xue; Bryndis Yngvadottir; Can Alkan; Lars N. Andersen; Qasim Ayub; Edward V. Ball; Kathryn Beal; Brenda J. Bradley; Yuan Chen; Chris M. Clee; Stephen Fitzgerald; Tina A. Graves; Yong Gu; Paul Heath; Andreas Heger; Emre Karakoc; Anja Kolb-Kokocinski; Gavin K. Laird; Gerton Lunter; Stephen Meader; Matthew Mort; James C. Mullikin; Kasper Munch; Timothy D. O'Connor; Andrew D. Phillips; Javier Prado-Martinez; Anthony S. Rogers; Saba Sajjadian; Dominic Schmidt; Katy Shaw; Jared T. Simpson; Peter D. Stenson; Daniel J. Turner; Linda Vigilant; Albert J. Vilella; Weldon Whitener; Baoli Zhu; David N. Cooper; Pieter De Jong; Emmanouil T. Dermitzakis; Evan E. Eichler; Paul Flicek; Nick Goldman; Nicholas I. Mundy; Zemin Ning; Duncan T. Odom; Chris P. Ponting; Michael A. Quail; Oliver A. Ryder; Stephen M. Searle; Wesley C. Warren; Richard K. Wilson; Mikkel H. Schierup; Jane Rogers; Chris Tyler-Smith; Richard Durbin

doi:10.1038/nature10842

Insights into hominid evolution from the gorilla genome sequence

Aylwyn Scally, Julien Y. Dutheil, Ladeana W. Hillier, Gregory E. Jordan, Ian Goodhead, Javier Herrero, Asger Hobolth, Tuuli Lappalainen, Thomas Mailund, Tomas Marques-Bonet, Shane McCarthy, Stephen H. Montgomery, Petra C. Schwalie, Y. Amy Tang, Michelle C. Ward, Yali Xue, Bryndis Yngvadottir, Can Alkan, Lars N. Andersen, Qasim AyubEdward V. Ball, Kathryn Beal, Brenda J. Bradley, Yuan Chen, Chris M. Clee, Stephen Fitzgerald, Tina A. Graves, Yong Gu, Paul Heath, Andreas Heger, Emre Karakoc, Anja Kolb-Kokocinski, Gavin K. Laird, Gerton Lunter, Stephen Meader, Matthew Mort, James C. Mullikin, Kasper Munch, Timothy D. O'Connor, Andrew D. Phillips, Javier Prado-Martinez, Anthony S. Rogers, Saba Sajjadian, Dominic Schmidt, Katy Shaw, Jared T. Simpson, Peter D. Stenson, Daniel J. Turner, Linda Vigilant, Albert J. Vilella, Weldon Whitener, Baoli Zhu, David N. Cooper, Pieter De Jong, Emmanouil T. Dermitzakis, Evan E. Eichler, Paul Flicek, Nick Goldman, Nicholas I. Mundy, Zemin Ning, Duncan T. Odom, Chris P. Ponting, Michael A. Quail, Oliver A. Ryder, Stephen M. Searle, Wesley C. Warren, Richard K. Wilson, Mikkel H. Schierup, Jane Rogers, Chris Tyler-Smith, Richard Durbin

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Abstract

Gorillas are humans' closest living relatives after chimpanzees, and are of comparable importance for the study of human origins and evolution. Here we present the assembly and analysis of a genome sequence for the western lowland gorilla, and compare the whole genomes of all extant great ape genera. We propose a synthesis of genetic and fossil evidence consistent with placing the human-chimpanzee and human-chimpanzee-gorilla speciation events at approximately 6 and 10 million years ago. In 30% of the genome, gorilla is closer to human or chimpanzee than the latter are to each other; this is rarer around coding genes, indicating pervasive selection throughout great ape evolution, and has functional consequences in gene expression. A comparison of protein coding genes reveals approximately 500 genes showing accelerated evolution on each of the gorilla, human and chimpanzee lineages, and evidence for parallel acceleration, particularly of genes involved in hearing. We also compare the western and eastern gorilla species, estimating an average sequence divergence time 1.75 million years ago, but with evidence for more recent genetic exchange and a population bottleneck in the eastern species. The use of the genome sequence in these and future analyses will promote a deeper understanding of great ape biology and evolution.

Original language	English
Pages (from-to)	169-175
Number of pages	7
Journal	Nature
Volume	483
Issue number	7388
DOIs	https://doi.org/10.1038/nature10842
Publication status	Published - 8 Mar 2012
Externally published	Yes

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10.1038/nature10842Licence: CC BY-NC-SA

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Scally, A., Dutheil, J. Y., Hillier, L. W., Jordan, G. E., Goodhead, I., Herrero, J., Hobolth, A., Lappalainen, T., Mailund, T., Marques-Bonet, T., McCarthy, S., Montgomery, S. H., Schwalie, P. C., Tang, Y. A., Ward, M. C., Xue, Y., Yngvadottir, B., Alkan, C., Andersen, L. N., ... Durbin, R. (2012). Insights into hominid evolution from the gorilla genome sequence. Nature, 483(7388), 169-175. https://doi.org/10.1038/nature10842

@article{f8f65c99a9724f56b880ea0fb9a7366b,

title = "Insights into hominid evolution from the gorilla genome sequence",

abstract = "Gorillas are humans' closest living relatives after chimpanzees, and are of comparable importance for the study of human origins and evolution. Here we present the assembly and analysis of a genome sequence for the western lowland gorilla, and compare the whole genomes of all extant great ape genera. We propose a synthesis of genetic and fossil evidence consistent with placing the human-chimpanzee and human-chimpanzee-gorilla speciation events at approximately 6 and 10 million years ago. In 30% of the genome, gorilla is closer to human or chimpanzee than the latter are to each other; this is rarer around coding genes, indicating pervasive selection throughout great ape evolution, and has functional consequences in gene expression. A comparison of protein coding genes reveals approximately 500 genes showing accelerated evolution on each of the gorilla, human and chimpanzee lineages, and evidence for parallel acceleration, particularly of genes involved in hearing. We also compare the western and eastern gorilla species, estimating an average sequence divergence time 1.75 million years ago, but with evidence for more recent genetic exchange and a population bottleneck in the eastern species. The use of the genome sequence in these and future analyses will promote a deeper understanding of great ape biology and evolution.",

author = "Aylwyn Scally and Dutheil, {Julien Y.} and Hillier, {Ladeana W.} and Jordan, {Gregory E.} and Ian Goodhead and Javier Herrero and Asger Hobolth and Tuuli Lappalainen and Thomas Mailund and Tomas Marques-Bonet and Shane McCarthy and Montgomery, {Stephen H.} and Schwalie, {Petra C.} and Tang, {Y. Amy} and Ward, {Michelle C.} and Yali Xue and Bryndis Yngvadottir and Can Alkan and Andersen, {Lars N.} and Qasim Ayub and Ball, {Edward V.} and Kathryn Beal and Bradley, {Brenda J.} and Yuan Chen and Clee, {Chris M.} and Stephen Fitzgerald and Graves, {Tina A.} and Yong Gu and Paul Heath and Andreas Heger and Emre Karakoc and Anja Kolb-Kokocinski and Laird, {Gavin K.} and Gerton Lunter and Stephen Meader and Matthew Mort and Mullikin, {James C.} and Kasper Munch and O'Connor, {Timothy D.} and Phillips, {Andrew D.} and Javier Prado-Martinez and Rogers, {Anthony S.} and Saba Sajjadian and Dominic Schmidt and Katy Shaw and Simpson, {Jared T.} and Stenson, {Peter D.} and Turner, {Daniel J.} and Linda Vigilant and Vilella, {Albert J.} and Weldon Whitener and Baoli Zhu and Cooper, {David N.} and {De Jong}, Pieter and Dermitzakis, {Emmanouil T.} and Eichler, {Evan E.} and Paul Flicek and Nick Goldman and Mundy, {Nicholas I.} and Zemin Ning and Odom, {Duncan T.} and Ponting, {Chris P.} and Quail, {Michael A.} and Ryder, {Oliver A.} and Searle, {Stephen M.} and Warren, {Wesley C.} and Wilson, {Richard K.} and Schierup, {Mikkel H.} and Jane Rogers and Chris Tyler-Smith and Richard Durbin",

note = "Funding Information: Acknowledgements We thank H. Li and E. Birney for discussions, D. Zerbino, J. Stalker, L. Wilming, D. Rajan and H. Clawson for technical assistance, J. Ahringer for comments on the manuscript, K. Leus of the Center for Research and Conservation of the Royal Zoological Society of Antwerp for sample material from Mukisi, and the Marmoset Genome Analysis Consortium for permission to use the unpublished assembly of the marmoset genome. This research was supported in part by Wellcome Trust grants WT062023 (to J.H., K.B., S.F., A.J.V., P.F.), WT089066 (to R.D.), WT077192 (to R.D., S.M., A.K.-K., J.T.S., W.W.), WT077009 (to Y.X., B.Y., Q.A., Y.C., C.T.-S.), WT077198 (to G.K.L.) and 075491/Z/04 (to G.L.); EMBL grants (to P.C.S., P.F.); scholarships from the Gates Cambridge Trust (to G.E.J. and T.D.O{\textquoteright}C.); an MRC Special Fellowship in Biomedical Informatics (to A.S.); funding from the Lundbeck Foundation (to A.H.); the Academy of Finlandand the EmilAaltonen Foundation(to T.L.); aMarieCurie fellowship (to T.M.-B.); the European Community{\textquoteright}s Seventh Framework Programme (FP7/2007-2013)/ ERC Starting Grant (StG_20091118) (to T.M.-B.); an FPI grant from the Spanish Ministry of Education (BES-2010-032251) (to J.P.-M.); a BBSRC Doctoral Training Grant (to S.H.M.); grants from the UK Medical Research Council (to A.H., S.M., C.P.P.); the Intramural Research Program of the National Human Genome Research Institute, National Institutes of Health (to J.C.M.); the Danish Council for Independent Research, Natural Sciences, grantno. 09-062535 (to K.M.,M.H.S.); a CommonwealthScholarship (to M.C.W.); the Swiss National Science Foundation, Louis Jeantet Foundation (to E.T.D.); an ERC Starting Grant and an EMBO Young Investigator Award, Hutchinson Whampoa (to D.T.O.); NHGRI support (to W.C.W.); support from BIOBASE GmbH (to E.V.B., P.D.S., M.M., A.D.P., K.S., D.N.C.); US National Science Foundation grant DGE-0739133 (to W.W.); NHGRI U54 HG003079 (to R.K.W.); NIH grant HG002385 (to E.E.E). E.E.E. is an investigator of the Howard Hughes Medical Institute.",

year = "2012",

month = mar,

day = "8",

doi = "10.1038/nature10842",

language = "English",

volume = "483",

pages = "169--175",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Publishing Group",

number = "7388",

}

Scally, A, Dutheil, JY, Hillier, LW, Jordan, GE, Goodhead, I, Herrero, J, Hobolth, A, Lappalainen, T, Mailund, T, Marques-Bonet, T, McCarthy, S, Montgomery, SH, Schwalie, PC, Tang, YA, Ward, MC, Xue, Y, Yngvadottir, B, Alkan, C, Andersen, LN, Ayub, Q, Ball, EV, Beal, K, Bradley, BJ, Chen, Y, Clee, CM, Fitzgerald, S, Graves, TA, Gu, Y, Heath, P, Heger, A, Karakoc, E, Kolb-Kokocinski, A, Laird, GK, Lunter, G, Meader, S, Mort, M, Mullikin, JC, Munch, K, O'Connor, TD, Phillips, AD, Prado-Martinez, J, Rogers, AS, Sajjadian, S, Schmidt, D, Shaw, K, Simpson, JT, Stenson, PD, Turner, DJ, Vigilant, L, Vilella, AJ, Whitener, W, Zhu, B, Cooper, DN, De Jong, P, Dermitzakis, ET, Eichler, EE, Flicek, P, Goldman, N, Mundy, NI, Ning, Z, Odom, DT, Ponting, CP, Quail, MA, Ryder, OA, Searle, SM, Warren, WC, Wilson, RK, Schierup, MH, Rogers, J, Tyler-Smith, C & Durbin, R 2012, 'Insights into hominid evolution from the gorilla genome sequence', Nature, vol. 483, no. 7388, pp. 169-175. https://doi.org/10.1038/nature10842

TY - JOUR

T1 - Insights into hominid evolution from the gorilla genome sequence

AU - Scally, Aylwyn

AU - Dutheil, Julien Y.

AU - Hillier, Ladeana W.

AU - Jordan, Gregory E.

AU - Goodhead, Ian

AU - Herrero, Javier

AU - Hobolth, Asger

AU - Lappalainen, Tuuli

AU - Mailund, Thomas

AU - Marques-Bonet, Tomas

AU - McCarthy, Shane

AU - Montgomery, Stephen H.

AU - Schwalie, Petra C.

AU - Tang, Y. Amy

AU - Ward, Michelle C.

AU - Xue, Yali

AU - Yngvadottir, Bryndis

AU - Alkan, Can

AU - Andersen, Lars N.

AU - Ayub, Qasim

AU - Ball, Edward V.

AU - Beal, Kathryn

AU - Bradley, Brenda J.

AU - Chen, Yuan

AU - Clee, Chris M.

AU - Fitzgerald, Stephen

AU - Graves, Tina A.

AU - Gu, Yong

AU - Heath, Paul

AU - Heger, Andreas

AU - Karakoc, Emre

AU - Kolb-Kokocinski, Anja

AU - Laird, Gavin K.

AU - Lunter, Gerton

AU - Meader, Stephen

AU - Mort, Matthew

AU - Mullikin, James C.

AU - Munch, Kasper

AU - O'Connor, Timothy D.

AU - Phillips, Andrew D.

AU - Prado-Martinez, Javier

AU - Rogers, Anthony S.

AU - Sajjadian, Saba

AU - Schmidt, Dominic

AU - Shaw, Katy

AU - Simpson, Jared T.

AU - Stenson, Peter D.

AU - Turner, Daniel J.

AU - Vigilant, Linda

AU - Vilella, Albert J.

AU - Whitener, Weldon

AU - Zhu, Baoli

AU - Cooper, David N.

AU - De Jong, Pieter

AU - Dermitzakis, Emmanouil T.

AU - Eichler, Evan E.

AU - Flicek, Paul

AU - Goldman, Nick

AU - Mundy, Nicholas I.

AU - Ning, Zemin

AU - Odom, Duncan T.

AU - Ponting, Chris P.

AU - Quail, Michael A.

AU - Ryder, Oliver A.

AU - Searle, Stephen M.

AU - Warren, Wesley C.

AU - Wilson, Richard K.

AU - Schierup, Mikkel H.

AU - Rogers, Jane

AU - Tyler-Smith, Chris

AU - Durbin, Richard

N1 - Funding Information: Acknowledgements We thank H. Li and E. Birney for discussions, D. Zerbino, J. Stalker, L. Wilming, D. Rajan and H. Clawson for technical assistance, J. Ahringer for comments on the manuscript, K. Leus of the Center for Research and Conservation of the Royal Zoological Society of Antwerp for sample material from Mukisi, and the Marmoset Genome Analysis Consortium for permission to use the unpublished assembly of the marmoset genome. This research was supported in part by Wellcome Trust grants WT062023 (to J.H., K.B., S.F., A.J.V., P.F.), WT089066 (to R.D.), WT077192 (to R.D., S.M., A.K.-K., J.T.S., W.W.), WT077009 (to Y.X., B.Y., Q.A., Y.C., C.T.-S.), WT077198 (to G.K.L.) and 075491/Z/04 (to G.L.); EMBL grants (to P.C.S., P.F.); scholarships from the Gates Cambridge Trust (to G.E.J. and T.D.O’C.); an MRC Special Fellowship in Biomedical Informatics (to A.S.); funding from the Lundbeck Foundation (to A.H.); the Academy of Finlandand the EmilAaltonen Foundation(to T.L.); aMarieCurie fellowship (to T.M.-B.); the European Community’s Seventh Framework Programme (FP7/2007-2013)/ ERC Starting Grant (StG_20091118) (to T.M.-B.); an FPI grant from the Spanish Ministry of Education (BES-2010-032251) (to J.P.-M.); a BBSRC Doctoral Training Grant (to S.H.M.); grants from the UK Medical Research Council (to A.H., S.M., C.P.P.); the Intramural Research Program of the National Human Genome Research Institute, National Institutes of Health (to J.C.M.); the Danish Council for Independent Research, Natural Sciences, grantno. 09-062535 (to K.M.,M.H.S.); a CommonwealthScholarship (to M.C.W.); the Swiss National Science Foundation, Louis Jeantet Foundation (to E.T.D.); an ERC Starting Grant and an EMBO Young Investigator Award, Hutchinson Whampoa (to D.T.O.); NHGRI support (to W.C.W.); support from BIOBASE GmbH (to E.V.B., P.D.S., M.M., A.D.P., K.S., D.N.C.); US National Science Foundation grant DGE-0739133 (to W.W.); NHGRI U54 HG003079 (to R.K.W.); NIH grant HG002385 (to E.E.E). E.E.E. is an investigator of the Howard Hughes Medical Institute.

PY - 2012/3/8

Y1 - 2012/3/8

N2 - Gorillas are humans' closest living relatives after chimpanzees, and are of comparable importance for the study of human origins and evolution. Here we present the assembly and analysis of a genome sequence for the western lowland gorilla, and compare the whole genomes of all extant great ape genera. We propose a synthesis of genetic and fossil evidence consistent with placing the human-chimpanzee and human-chimpanzee-gorilla speciation events at approximately 6 and 10 million years ago. In 30% of the genome, gorilla is closer to human or chimpanzee than the latter are to each other; this is rarer around coding genes, indicating pervasive selection throughout great ape evolution, and has functional consequences in gene expression. A comparison of protein coding genes reveals approximately 500 genes showing accelerated evolution on each of the gorilla, human and chimpanzee lineages, and evidence for parallel acceleration, particularly of genes involved in hearing. We also compare the western and eastern gorilla species, estimating an average sequence divergence time 1.75 million years ago, but with evidence for more recent genetic exchange and a population bottleneck in the eastern species. The use of the genome sequence in these and future analyses will promote a deeper understanding of great ape biology and evolution.

AB - Gorillas are humans' closest living relatives after chimpanzees, and are of comparable importance for the study of human origins and evolution. Here we present the assembly and analysis of a genome sequence for the western lowland gorilla, and compare the whole genomes of all extant great ape genera. We propose a synthesis of genetic and fossil evidence consistent with placing the human-chimpanzee and human-chimpanzee-gorilla speciation events at approximately 6 and 10 million years ago. In 30% of the genome, gorilla is closer to human or chimpanzee than the latter are to each other; this is rarer around coding genes, indicating pervasive selection throughout great ape evolution, and has functional consequences in gene expression. A comparison of protein coding genes reveals approximately 500 genes showing accelerated evolution on each of the gorilla, human and chimpanzee lineages, and evidence for parallel acceleration, particularly of genes involved in hearing. We also compare the western and eastern gorilla species, estimating an average sequence divergence time 1.75 million years ago, but with evidence for more recent genetic exchange and a population bottleneck in the eastern species. The use of the genome sequence in these and future analyses will promote a deeper understanding of great ape biology and evolution.

UR - http://www.scopus.com/inward/record.url?scp=84863230553&partnerID=8YFLogxK

U2 - 10.1038/nature10842

DO - 10.1038/nature10842

M3 - Article

C2 - 22398555

AN - SCOPUS:84863230553

SN - 0028-0836

VL - 483

SP - 169

EP - 175

JO - Nature

JF - Nature

IS - 7388

ER -

Insights into hominid evolution from the gorilla genome sequence

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