A genomic history of Aboriginal Australia

Anna-Sapfo Malaspinas; Michael C. Westaway; Craig Muller; Vitor C. Sousa; Oscar Lao; Isabel Alves; Anders Bergström; Georgios Athanasiadis; Jade Y. Cheng; Jacob E. Crawford; Tim H. Heupink; Enrico Macholdt; Stephan Peischl; Simon Rasmussen; Stephan Schiffels; Sankar Subramanian; Joanne L. Wright; Anders Albrechtsen; Chiara Barbieri; Isabelle Dupanloup; Anders Eriksson; Ashot Margaryan; Ida Moltke; Irina Pugach; Thorfinn S. Korneliussen; Ivan P. Levkivskyi; J. Víctor Moreno-Mayar; Shengyu Ni; Fernando Racimo; Martin Sikora; Yali Xue; Farhang A. Aghakhanian; Nicolas Brucato; Søren Brunak; Paula F. Campos; Warren Clark; Sturla Ellingvåg; Gudjugudju Fourmile; Pascale Gerbault; Darren Injie; George Koki; Matthew Leavesley; Betty Logan; Aubrey Lynch; Elizabeth A. Matisoo-Smith; Peter J. McAllister; Alexander J. Mentzer; Mait Metspalu; Andrea B. Migliano; Les Murgha; Maude E. Phipps; William Pomat; Doc Reynolds; Francois-Xavier Ricaut; Peter Siba; Mark G. Thomas; Thomas Wales; Colleen Ma’run Wall; Stephen J. Oppenheimer; Chris Tyler-Smith; Richard Durbin; Joe Dortch; Andrea Manica; Mikkel H. Schierup; Robert A. Foley; Marta Mirazón Lahr; Claire Bowern; Jeffrey D. Wall; Thomas Mailund; Mark Stoneking; Rasmus Nielsen; Manjinder S. Sandhu; Laurent Excoffier; David M. Lambert; Eske Willerslev

doi:10.1038/nature18299

A genomic history of Aboriginal Australia

Anna-Sapfo Malaspinas, Michael C. Westaway, Craig Muller, Vitor C. Sousa, Oscar Lao, Isabel Alves, Anders Bergström, Georgios Athanasiadis, Jade Y. Cheng, Jacob E. Crawford, Tim H. Heupink, Enrico Macholdt, Stephan Peischl, Simon Rasmussen, Stephan Schiffels, Sankar Subramanian, Joanne L. Wright, Anders Albrechtsen, Chiara Barbieri, Isabelle DupanloupAnders Eriksson, Ashot Margaryan, Ida Moltke, Irina Pugach, Thorfinn S. Korneliussen, Ivan P. Levkivskyi, J. Víctor Moreno-Mayar, Shengyu Ni, Fernando Racimo, Martin Sikora, Yali Xue, Farhang A. Aghakhanian, Nicolas Brucato, Søren Brunak, Paula F. Campos, Warren Clark, Sturla Ellingvåg, Gudjugudju Fourmile, Pascale Gerbault, Darren Injie, George Koki, Matthew Leavesley, Betty Logan, Aubrey Lynch, Elizabeth A. Matisoo-Smith, Peter J. McAllister, Alexander J. Mentzer, Mait Metspalu, Andrea B. Migliano, Les Murgha, Maude E. Phipps, William Pomat, Doc Reynolds, Francois-Xavier Ricaut, Peter Siba, Mark G. Thomas, Thomas Wales, Colleen Ma’run Wall, Stephen J. Oppenheimer, Chris Tyler-Smith, Richard Durbin, Joe Dortch, Andrea Manica, Mikkel H. Schierup, Robert A. Foley, Marta Mirazón Lahr, Claire Bowern, Jeffrey D. Wall, Thomas Mailund, Mark Stoneking, Rasmus Nielsen, Manjinder S. Sandhu, Laurent Excoffier, David M. Lambert, Eske Willerslev

Biological, Environmental Sciences and Engineering

Research output: Contribution to journal › Article › peer-review

371 Scopus citations

Abstract

The population history of Aboriginal Australians remains largely uncharacterized. Here we generate high-coverage genomes for 83 Aboriginal Australians (speakers of Pama-Nyungan languages) and 25 Papuans from the New Guinea Highlands. We find that Papuan and Aboriginal Australian ancestors diversified 25-40 thousand years ago (kya), suggesting pre-Holocene population structure in the ancient continent of Sahul (Australia, New Guinea and Tasmania). However, all of the studied Aboriginal Australians descend from a single founding population that differentiated ∼10-32 kya. We infer a population expansion in northeast Australia during the Holocene epoch (past 10,000 years) associated with limited gene flow from this region to the rest of Australia, consistent with the spread of the Pama-Nyungan languages. We estimate that Aboriginal Australians and Papuans diverged from Eurasians 51-72 kya, following a single out-of-Africa dispersal, and subsequently admixed with archaic populations. Finally, we report evidence of selection in Aboriginal Australians potentially associated with living in the desert. © 2016 Macmillan Publishers Limited, part of Springer Nature. All rights reserved

Original language	English (US)
Pages (from-to)	207-214
Number of pages	8
Journal	Nature
Volume	538
Issue number	7624
DOIs	https://doi.org/10.1038/nature18299
State	Published - Sep 21 2016

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Malaspinas, A.-S., Westaway, M. C., Muller, C., Sousa, V. C., Lao, O., Alves, I., Bergström, A., Athanasiadis, G., Cheng, J. Y., Crawford, J. E., Heupink, T. H., Macholdt, E., Peischl, S., Rasmussen, S., Schiffels, S., Subramanian, S., Wright, J. L., Albrechtsen, A., Barbieri, C., ... Willerslev, E. (2016). A genomic history of Aboriginal Australia. Nature, 538(7624), 207-214. https://doi.org/10.1038/nature18299

@article{258e1d94f6a746b48816e23c3000a61c,

title = "A genomic history of Aboriginal Australia",

abstract = "The population history of Aboriginal Australians remains largely uncharacterized. Here we generate high-coverage genomes for 83 Aboriginal Australians (speakers of Pama-Nyungan languages) and 25 Papuans from the New Guinea Highlands. We find that Papuan and Aboriginal Australian ancestors diversified 25-40 thousand years ago (kya), suggesting pre-Holocene population structure in the ancient continent of Sahul (Australia, New Guinea and Tasmania). However, all of the studied Aboriginal Australians descend from a single founding population that differentiated ∼10-32 kya. We infer a population expansion in northeast Australia during the Holocene epoch (past 10,000 years) associated with limited gene flow from this region to the rest of Australia, consistent with the spread of the Pama-Nyungan languages. We estimate that Aboriginal Australians and Papuans diverged from Eurasians 51-72 kya, following a single out-of-Africa dispersal, and subsequently admixed with archaic populations. Finally, we report evidence of selection in Aboriginal Australians potentially associated with living in the desert. {\textcopyright} 2016 Macmillan Publishers Limited, part of Springer Nature. All rights reserved",

author = "Anna-Sapfo Malaspinas and Westaway, {Michael C.} and Craig Muller and Sousa, {Vitor C.} and Oscar Lao and Isabel Alves and Anders Bergstr{\"o}m and Georgios Athanasiadis and Cheng, {Jade Y.} and Crawford, {Jacob E.} and Heupink, {Tim H.} and Enrico Macholdt and Stephan Peischl and Simon Rasmussen and Stephan Schiffels and Sankar Subramanian and Wright, {Joanne L.} and Anders Albrechtsen and Chiara Barbieri and Isabelle Dupanloup and Anders Eriksson and Ashot Margaryan and Ida Moltke and Irina Pugach and Korneliussen, {Thorfinn S.} and Levkivskyi, {Ivan P.} and Moreno-Mayar, {J. V{\'i}ctor} and Shengyu Ni and Fernando Racimo and Martin Sikora and Yali Xue and Aghakhanian, {Farhang A.} and Nicolas Brucato and S{\o}ren Brunak and Campos, {Paula F.} and Warren Clark and Sturla Ellingv{\aa}g and Gudjugudju Fourmile and Pascale Gerbault and Darren Injie and George Koki and Matthew Leavesley and Betty Logan and Aubrey Lynch and Matisoo-Smith, {Elizabeth A.} and McAllister, {Peter J.} and Mentzer, {Alexander J.} and Mait Metspalu and Migliano, {Andrea B.} and Les Murgha and Phipps, {Maude E.} and William Pomat and Doc Reynolds and Francois-Xavier Ricaut and Peter Siba and Thomas, {Mark G.} and Thomas Wales and Wall, {Colleen Ma{\textquoteright}run} and Oppenheimer, {Stephen J.} and Chris Tyler-Smith and Richard Durbin and Joe Dortch and Andrea Manica and Schierup, {Mikkel H.} and Foley, {Robert A.} and Lahr, {Marta Miraz{\'o}n} and Claire Bowern and Wall, {Jeffrey D.} and Thomas Mailund and Mark Stoneking and Rasmus Nielsen and Sandhu, {Manjinder S.} and Laurent Excoffier and Lambert, {David M.} and Eske Willerslev",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank all sample donors for contributing to this study. We thank Macrogen (http://www.macrogen.com/) for sequencing of the Aboriginal Australian genomes, M. Rasmussen, C. Der Sarkissian, M. Allentoft, D. Cooper, R. Gray, S. Greenhill, A. Seguin-Orlando, T. Carstensen, M. Przeworski, J. D. Jensen and L. Orlando for helpful discussions. We thank E. Thorsby for sample collection and contributing the DNA extract for the P2077 genome, I. Lissimore for support with data storage and distribution. We thank T. Parks, K. Auckland, K. Robson, A. V. Hill, J. B. Clegg, D. Higgs, D. J. Weatherall and M. Alpers for assistance in sample collection and discussion. L.E., V.C.S., I.A., I.D. and S.P. are grateful to the High Performance Computation platform of the University of Bern for providing access to the UBELIX cluster. This work was supported by the Danish National Research Foundation, the Lundbeck Foundation, the KU2016 grant and the Australian Research Council. A.-S.M. was supported by an ambizione grant with reference PZ00P3_154717 from the Swiss National Science Foundation (SNSF). M.C.W. was supported by the Australian Research Council (ARC) Discovery grants DP110102635 and DP140101405 and by a Linkage grant LP140100387. V.C.S., I.D. and S.P. were supported by SNSF grants to L.E. with references 31003A-143393 and CRSII3_141940. O.L. was supported by a Ram{\'o}n y Cajal grant from the Spanish Ministerio de Economia y Competitividad (MINECO) with reference RYC-2013-14797 and by a BFU2015-68759-P (MINECO/FEDER) grant. I.A. was supported by a grant with reference SFRH/BD/73150/2010 from the Portuguese Foundation for Science and Technology (FCT). A.B., S.Sc., Y.X., C.T.-S. and R.D. were supported by a Wellcome Trust grant with reference WT098051. E.M., C.Ba., I.P., S.N. and M.St. acknowledge the Max Planck Society. S.Su. was supported by an ARC Discovery grant with reference DP140101405. J.L.W. was supported by a PhD scholarship from Griffith University. A.A. acknowledges the Villum foundation. I.M. was supported by a grant from the Danish Council for Independent Research with reference DFF–4090-00244. J.V.M.-M. acknowledges the Consejo Nacional de Ciencia y Tecnolog{\'i}a (Mexico) for funding. N.B. and F.-X.R. were supported by the French Ministry of Foreign and European Affairs and French ANR with the grant ANR14-CE31-0013-01. S.B. was supported by a Novo Nordisk Foundation grant with reference NNF14CC0001. P.G. and A.B.M. were supported by a Leverhulme Programme grant number RP2011-R-045 to A.B.M. at UCL Department of Anthropology and M.G.T. at UCL Department of Genetics, Evolution and Environment. A.J.M. was supported by a Wellcome Trust grant with reference 106289/Z/14/Z. M.M. acknowledges the EU European Regional Development Fund through the Centre of Excellence in Genomics to Estonian Biocentre; Estonian Institutional Research grant IUT24-1. M.G.T. was supported by a Wellcome Trust Senior Investigator Award with grant number 100719/Z/12/Z. S.J.O. was supported by a Wellcome Trust Core Award Grant Number 090532/Z/09/Z. A.Man. was supported by an ERC Consolidator Grant 647787 {\textquoteleft}LocalAdaptation{\textquoteright}. M.E.P. would like to acknowledge the cardio-metabolic research cluster at Jeffrey Cheah School of Medicine & Health Sciences, Monash University Malaysia and Ministry of Science, Technology & Innovation, Malaysia for research grant 100-RM1/BIOTEK 16/6/2B. M.H.S. was supported by a grant from the Danish Independence Research Council with reference FNU 12-125062. R.A.F. was supported by the Leverhulme Trust. M.M.L. is supported by an ERC Advanced Grant 295907 {\textquoteleft}In-Africa{\textquoteright}. C.Bo. was supported by USA National Science Foundation (NSF) grants BCS-0844550 and BCS-1423711, awarded to C.Bo. and Yale University. T.M. was supported by a grant from the Danish Independence Research Council with reference FNU 1323-00749. M.S.S. was supported by a Wellcome Trust grant with reference WT098051. L.E. was supported by Swiss NSF grant number 31003A-143393, D.M.L. was supported by ARC Discovery Grants DP110102635 and DP140101405 and Linkage grants LP140100387, LP120200144 and LP150100583. E.W. is grateful to St John{\textquoteright}s College in Cambridge for help and support.",

year = "2016",

month = sep,

day = "21",

doi = "10.1038/nature18299",

language = "English (US)",

volume = "538",

pages = "207--214",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Research",

number = "7624",

}

Malaspinas, A-S, Westaway, MC, Muller, C, Sousa, VC, Lao, O, Alves, I, Bergström, A, Athanasiadis, G, Cheng, JY, Crawford, JE, Heupink, TH, Macholdt, E, Peischl, S, Rasmussen, S, Schiffels, S, Subramanian, S, Wright, JL, Albrechtsen, A, Barbieri, C, Dupanloup, I, Eriksson, A, Margaryan, A, Moltke, I, Pugach, I, Korneliussen, TS, Levkivskyi, IP, Moreno-Mayar, JV, Ni, S, Racimo, F, Sikora, M, Xue, Y, Aghakhanian, FA, Brucato, N, Brunak, S, Campos, PF, Clark, W, Ellingvåg, S, Fourmile, G, Gerbault, P, Injie, D, Koki, G, Leavesley, M, Logan, B, Lynch, A, Matisoo-Smith, EA, McAllister, PJ, Mentzer, AJ, Metspalu, M, Migliano, AB, Murgha, L, Phipps, ME, Pomat, W, Reynolds, D, Ricaut, F-X, Siba, P, Thomas, MG, Wales, T, Wall, CM, Oppenheimer, SJ, Tyler-Smith, C, Durbin, R, Dortch, J, Manica, A, Schierup, MH, Foley, RA, Lahr, MM, Bowern, C, Wall, JD, Mailund, T, Stoneking, M, Nielsen, R, Sandhu, MS, Excoffier, L, Lambert, DM & Willerslev, E 2016, 'A genomic history of Aboriginal Australia', Nature, vol. 538, no. 7624, pp. 207-214. https://doi.org/10.1038/nature18299

TY - JOUR

T1 - A genomic history of Aboriginal Australia

AU - Malaspinas, Anna-Sapfo

AU - Westaway, Michael C.

AU - Muller, Craig

AU - Sousa, Vitor C.

AU - Lao, Oscar

AU - Alves, Isabel

AU - Bergström, Anders

AU - Athanasiadis, Georgios

AU - Cheng, Jade Y.

AU - Crawford, Jacob E.

AU - Heupink, Tim H.

AU - Macholdt, Enrico

AU - Peischl, Stephan

AU - Rasmussen, Simon

AU - Schiffels, Stephan

AU - Subramanian, Sankar

AU - Wright, Joanne L.

AU - Albrechtsen, Anders

AU - Barbieri, Chiara

AU - Dupanloup, Isabelle

AU - Eriksson, Anders

AU - Margaryan, Ashot

AU - Moltke, Ida

AU - Pugach, Irina

AU - Korneliussen, Thorfinn S.

AU - Levkivskyi, Ivan P.

AU - Moreno-Mayar, J. Víctor

AU - Ni, Shengyu

AU - Racimo, Fernando

AU - Sikora, Martin

AU - Xue, Yali

AU - Aghakhanian, Farhang A.

AU - Brucato, Nicolas

AU - Brunak, Søren

AU - Campos, Paula F.

AU - Clark, Warren

AU - Ellingvåg, Sturla

AU - Fourmile, Gudjugudju

AU - Gerbault, Pascale

AU - Injie, Darren

AU - Koki, George

AU - Leavesley, Matthew

AU - Logan, Betty

AU - Lynch, Aubrey

AU - Matisoo-Smith, Elizabeth A.

AU - McAllister, Peter J.

AU - Mentzer, Alexander J.

AU - Metspalu, Mait

AU - Migliano, Andrea B.

AU - Murgha, Les

AU - Phipps, Maude E.

AU - Pomat, William

AU - Reynolds, Doc

AU - Ricaut, Francois-Xavier

AU - Siba, Peter

AU - Thomas, Mark G.

AU - Wales, Thomas

AU - Wall, Colleen Ma’run

AU - Oppenheimer, Stephen J.

AU - Tyler-Smith, Chris

AU - Durbin, Richard

AU - Dortch, Joe

AU - Manica, Andrea

AU - Schierup, Mikkel H.

AU - Foley, Robert A.

AU - Lahr, Marta Mirazón

AU - Bowern, Claire

AU - Wall, Jeffrey D.

AU - Mailund, Thomas

AU - Stoneking, Mark

AU - Nielsen, Rasmus

AU - Sandhu, Manjinder S.

AU - Excoffier, Laurent

AU - Lambert, David M.

AU - Willerslev, Eske

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank all sample donors for contributing to this study. We thank Macrogen (http://www.macrogen.com/) for sequencing of the Aboriginal Australian genomes, M. Rasmussen, C. Der Sarkissian, M. Allentoft, D. Cooper, R. Gray, S. Greenhill, A. Seguin-Orlando, T. Carstensen, M. Przeworski, J. D. Jensen and L. Orlando for helpful discussions. We thank E. Thorsby for sample collection and contributing the DNA extract for the P2077 genome, I. Lissimore for support with data storage and distribution. We thank T. Parks, K. Auckland, K. Robson, A. V. Hill, J. B. Clegg, D. Higgs, D. J. Weatherall and M. Alpers for assistance in sample collection and discussion. L.E., V.C.S., I.A., I.D. and S.P. are grateful to the High Performance Computation platform of the University of Bern for providing access to the UBELIX cluster. This work was supported by the Danish National Research Foundation, the Lundbeck Foundation, the KU2016 grant and the Australian Research Council. A.-S.M. was supported by an ambizione grant with reference PZ00P3_154717 from the Swiss National Science Foundation (SNSF). M.C.W. was supported by the Australian Research Council (ARC) Discovery grants DP110102635 and DP140101405 and by a Linkage grant LP140100387. V.C.S., I.D. and S.P. were supported by SNSF grants to L.E. with references 31003A-143393 and CRSII3_141940. O.L. was supported by a Ramón y Cajal grant from the Spanish Ministerio de Economia y Competitividad (MINECO) with reference RYC-2013-14797 and by a BFU2015-68759-P (MINECO/FEDER) grant. I.A. was supported by a grant with reference SFRH/BD/73150/2010 from the Portuguese Foundation for Science and Technology (FCT). A.B., S.Sc., Y.X., C.T.-S. and R.D. were supported by a Wellcome Trust grant with reference WT098051. E.M., C.Ba., I.P., S.N. and M.St. acknowledge the Max Planck Society. S.Su. was supported by an ARC Discovery grant with reference DP140101405. J.L.W. was supported by a PhD scholarship from Griffith University. A.A. acknowledges the Villum foundation. I.M. was supported by a grant from the Danish Council for Independent Research with reference DFF–4090-00244. J.V.M.-M. acknowledges the Consejo Nacional de Ciencia y Tecnología (Mexico) for funding. N.B. and F.-X.R. were supported by the French Ministry of Foreign and European Affairs and French ANR with the grant ANR14-CE31-0013-01. S.B. was supported by a Novo Nordisk Foundation grant with reference NNF14CC0001. P.G. and A.B.M. were supported by a Leverhulme Programme grant number RP2011-R-045 to A.B.M. at UCL Department of Anthropology and M.G.T. at UCL Department of Genetics, Evolution and Environment. A.J.M. was supported by a Wellcome Trust grant with reference 106289/Z/14/Z. M.M. acknowledges the EU European Regional Development Fund through the Centre of Excellence in Genomics to Estonian Biocentre; Estonian Institutional Research grant IUT24-1. M.G.T. was supported by a Wellcome Trust Senior Investigator Award with grant number 100719/Z/12/Z. S.J.O. was supported by a Wellcome Trust Core Award Grant Number 090532/Z/09/Z. A.Man. was supported by an ERC Consolidator Grant 647787 ‘LocalAdaptation’. M.E.P. would like to acknowledge the cardio-metabolic research cluster at Jeffrey Cheah School of Medicine & Health Sciences, Monash University Malaysia and Ministry of Science, Technology & Innovation, Malaysia for research grant 100-RM1/BIOTEK 16/6/2B. M.H.S. was supported by a grant from the Danish Independence Research Council with reference FNU 12-125062. R.A.F. was supported by the Leverhulme Trust. M.M.L. is supported by an ERC Advanced Grant 295907 ‘In-Africa’. C.Bo. was supported by USA National Science Foundation (NSF) grants BCS-0844550 and BCS-1423711, awarded to C.Bo. and Yale University. T.M. was supported by a grant from the Danish Independence Research Council with reference FNU 1323-00749. M.S.S. was supported by a Wellcome Trust grant with reference WT098051. L.E. was supported by Swiss NSF grant number 31003A-143393, D.M.L. was supported by ARC Discovery Grants DP110102635 and DP140101405 and Linkage grants LP140100387, LP120200144 and LP150100583. E.W. is grateful to St John’s College in Cambridge for help and support.

PY - 2016/9/21

Y1 - 2016/9/21

N2 - The population history of Aboriginal Australians remains largely uncharacterized. Here we generate high-coverage genomes for 83 Aboriginal Australians (speakers of Pama-Nyungan languages) and 25 Papuans from the New Guinea Highlands. We find that Papuan and Aboriginal Australian ancestors diversified 25-40 thousand years ago (kya), suggesting pre-Holocene population structure in the ancient continent of Sahul (Australia, New Guinea and Tasmania). However, all of the studied Aboriginal Australians descend from a single founding population that differentiated ∼10-32 kya. We infer a population expansion in northeast Australia during the Holocene epoch (past 10,000 years) associated with limited gene flow from this region to the rest of Australia, consistent with the spread of the Pama-Nyungan languages. We estimate that Aboriginal Australians and Papuans diverged from Eurasians 51-72 kya, following a single out-of-Africa dispersal, and subsequently admixed with archaic populations. Finally, we report evidence of selection in Aboriginal Australians potentially associated with living in the desert. © 2016 Macmillan Publishers Limited, part of Springer Nature. All rights reserved

AB - The population history of Aboriginal Australians remains largely uncharacterized. Here we generate high-coverage genomes for 83 Aboriginal Australians (speakers of Pama-Nyungan languages) and 25 Papuans from the New Guinea Highlands. We find that Papuan and Aboriginal Australian ancestors diversified 25-40 thousand years ago (kya), suggesting pre-Holocene population structure in the ancient continent of Sahul (Australia, New Guinea and Tasmania). However, all of the studied Aboriginal Australians descend from a single founding population that differentiated ∼10-32 kya. We infer a population expansion in northeast Australia during the Holocene epoch (past 10,000 years) associated with limited gene flow from this region to the rest of Australia, consistent with the spread of the Pama-Nyungan languages. We estimate that Aboriginal Australians and Papuans diverged from Eurasians 51-72 kya, following a single out-of-Africa dispersal, and subsequently admixed with archaic populations. Finally, we report evidence of selection in Aboriginal Australians potentially associated with living in the desert. © 2016 Macmillan Publishers Limited, part of Springer Nature. All rights reserved

UR - http://hdl.handle.net/10754/622366

UR - http://www.nature.com/nature/journal/v538/n7624/full/nature18299.html

UR - http://www.scopus.com/inward/record.url?scp=84991632770&partnerID=8YFLogxK

U2 - 10.1038/nature18299

DO - 10.1038/nature18299

M3 - Article

C2 - 27654914

SN - 0028-0836

VL - 538

SP - 207

EP - 214

JO - Nature

JF - Nature

IS - 7624

ER -

A genomic history of Aboriginal Australia

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