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Upper Palaeolithic Siberian genome reveals dual ancestry of Native Americans

Naturevolume 505, pages87–91 (2014)Cite this article

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Abstract

The origins of the First Americans remain contentious. Although Native Americans seem to be genetically most closely related to east Asians1,2,3, there is no consensus with regard to which specific Old World populations they are closest to4,5,6,7,8. Here we sequence the draft genome of an approximately 24,000-year-old individual (MA-1), from Mal’ta in south-central Siberia9, to an average depth of 1×. To our knowledge this is the oldest anatomically modern human genome reported to date. The MA-1 mitochondrial genome belongs to haplogroup U, which has also been found at high frequency among Upper Palaeolithic and Mesolithic European hunter-gatherers10,11,12, and the Y chromosome of MA-1 is basal to modern-day western Eurasians and near the root of most Native American lineages5. Similarly, we find autosomal evidence that MA-1 is basal to modern-day western Eurasians and genetically closely related to modern-day Native Americans, with no close affinity to east Asians. This suggests that populations related to contemporary western Eurasians had a more north-easterly distribution 24,000 years ago than commonly thought. Furthermore, we estimate that 14 to 38% of Native American ancestry may originate through gene flow from this ancient population. This is likely to have occurred after the divergence of Native American ancestors from east Asian ancestors, but before the diversification of Native American populations in the New World. Gene flow from the MA-1 lineage into Native American ancestors could explain why several crania from the First Americans have been reported as bearing morphological characteristics that do not resemble those of east Asians2,13. Sequencing of another south-central Siberian, Afontova Gora-2 dating to approximately 17,000 years ago14, revealed similar autosomal genetic signatures as MA-1, suggesting that the region was continuously occupied by humans throughout the Last Glacial Maximum. Our findings reveal that western Eurasian genetic signatures in modern-day Native Americans derive not only from post-Columbian admixture, as commonly thought, but also from a mixed ancestry of the First Americans.

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Figure 1: Sample locations and MA-1 genetic affinities.
Figure 2: Admixture graph for MA-1 and 16 complete genomes.
Figure 3: Evidence of gene flow from a population related to MA-1 and western Eurasians into Native American ancestors.

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Accession codes

Accessions

Gene Expression Omnibus

Sequence Read Archive

Data deposits

Sequence data for MA-1 and AG-2, produced in this study, are available for download through NCBI SRA accession numberSRP029640. Data from the Illumina genotyping analysis generated in this study are available through GEO Series accession numberGSE50727; PLINK files can be accessed fromhttp://www.ebc.ee/free_data. In addition, the above data and alignments for the published modern genomes, Denisova genome, Tianyuan individual and the two ancient genomes are available athttp://www.cbs.dtu.dk/suppl/malta. Raw reads and alignments for the four modern genomes sequenced in this study are available for demographic research under data access agreement with E.W.

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Acknowledgements

We thank the Hermitage State Museum for providing access to the Mal’ta and Afontova Gora-2 human remains. We also thank the Danish National High-Throughput DNA Sequencing Centre and T. Reisberg for technical assistance. This work was supported by the Danish National Research Foundation and the Lundbeck Foundation (E.W. and M.R.) and the Arctic Social Sciences Program, National Science Foundation (grant PLR-1003725 to K.E.G.). R.V., M.M., M.K., E.M., K.T., S.Ro. and R.M. were supported by the European Regional Development Fund (European Union) through the Centre of Excellence in Genomics to Estonian Biocentre and University of Tartu and Estonian Basic Research grant SF0270177As08. M.M. thanks the Estonian Science Foundation grant no. 8973 and Baltic-American Freedom Foundation Research Scholarship program and M.I.V. thanks the Government of Russian Federation grant no. 14.B25.31.0033 (to E. I. Rogaev). M.D. was supported by the US National Science Foundation (grant DBI-1103639). Computational analyses were carried out at the High Performance Computing Center, University of Tartu, and the Swedish National Infrastructure for Computing (SNIC-UPPMAX, project b2012063).

Author information

Author notes

  1. Maanasa Raghavan and Pontus Skoglund: These authors contributed equally to this work.

Authors and Affiliations

  1. Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5–7, 1350 Copenhagen, Denmark ,

    Maanasa Raghavan, Thomas W. Stafford Jr, Ludovic Orlando, Paula F. Campos & Eske Willerslev

  2. Department of Evolutionary Biology, Uppsala University, Norbyvägen 18D, Uppsala 752 36, Sweden,

    Pontus Skoglund & Mattias Jakobsson

  3. Center for the Study of the First Americans, Texas A&M University, TAMU-4352, College Station, Texas 77845-4352, USA ,

    Kelly E. Graf

  4. Estonian Biocentre, Evolutionary Biology group, Tartu 51010, Estonia ,

    Mait Metspalu, Monika Karmin, Kristiina Tambets, Siiri Rootsi, Sergey Litvinov, Toomas Kivisild & Richard Villems

  5. Department of Integrative Biology, University of California, Berkeley, 94720, California, USA

    Mait Metspalu, Michael DeGiorgio & Rasmus Nielsen

  6. Department of Evolutionary Biology, University of Tartu, Tartu 51010, Estonia,

    Mait Metspalu, Ene Metspalu, Monika Karmin & Richard Villems

  7. Department of Biology, The Bioinformatics Centre, University of Copenhagen, Ole Maaløes Vej 5, Copenhagen 2200, Denmark,

    Anders Albrechtsen & Ida Moltke

  8. Department of Human Genetics, The University of Chicago, Chicago, 60637, Illinois, USA

    Ida Moltke

  9. Center for Biological Sequence Analysis, Technical University of Denmark, Kongens Lyngby 2800, Denmark ,

    Simon Rasmussen, Thomas Sicheritz-Ponten & Søren Brunak

  10. Department of Physics and Astronomy, AMS 14C Dating Centre, University of Aarhus, Ny Munkegade 120, Aarhus DK-8000, Denmark,

    Thomas W. Stafford Jr

  11. Estonian Genome Center, University of Tartu, Tartu 51010, Estonia ,

    Reedik Mägi

  12. Research Centre for Medical Genetics, Russian Academy of Medical Sciences, Moskvorechie Street 1, Moscow 115479, Russia ,

    Elena Balanovska & Oleg Balanovsky

  13. Vavilov Institute of General Genetics, Russian Academy of Sciences, Gubkina Street 3, Moscow 119991, Russia ,

    Oleg Balanovsky

  14. Institute of Biochemistry and Genetics, Ufa Scientific Centre, Russian Academy of Sciences, Ufa, Bashkorostan 450054, Russia ,

    Elza Khusnutdinova & Sergey Litvinov

  15. Biology Department, Bashkir State University, Ufa, Bashkorostan 450074, Russia,

    Elza Khusnutdinova

  16. The Institute of Cytology and Genetics, Center for Brain Neurobiology and Neurogenetics, Siberian Branch of the Russian Academy of Sciences, Lavrentyeva Avenue, Novosibirsk 630090, Russia ,

    Ludmila P. Osipova & Mikhail I. Voevoda

  17. Department of Molecular Genetics, Yakut Research Center of Complex Medical Problems, Russian Academy of Medical Sciences and North-Eastern Federal University, Yakutsk, Sakha (Yakutia) 677010, Russia,

    Sardana A. Fedorova

  18. Institute of Internal Medicine, Siberian Branch of the Russian Academy of Medical Sciences, Borisa Bogatkova 175/1, Novosibirsk 630089, Russia ,

    Mikhail I. Voevoda

  19. Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Kongens Lyngby 2800, Denmark ,

    Thomas Sicheritz-Ponten & Søren Brunak

  20. The State Hermitage Museum, 2, Dvortsovaya Ploshchad, St. Petersberg 190000, Russia ,

    Svetlana Demeshchenko

  21. Department of Biological Anthropology, University of Cambridge, Cambridge CB2 1QH, UK,

    Toomas Kivisild

  22. Estonian Academy of Sciences, Tallinn 10130, Estonia ,

    Richard Villems

  23. Science for Life Laboratory, Uppsala University, Norbyvägen 18D, 752 36 Uppsala, Sweden ,

    Mattias Jakobsson

Authors
  1. Maanasa Raghavan
  2. Pontus Skoglund
  3. Kelly E. Graf
  4. Mait Metspalu
  5. Anders Albrechtsen
  6. Ida Moltke
  7. Simon Rasmussen
  8. Thomas W. Stafford Jr
  9. Ludovic Orlando
  10. Ene Metspalu
  11. Monika Karmin
  12. Kristiina Tambets
  13. Siiri Rootsi
  14. Reedik Mägi
  15. Paula F. Campos
  16. Elena Balanovska
  17. Oleg Balanovsky
  18. Elza Khusnutdinova
  19. Sergey Litvinov
  20. Ludmila P. Osipova
  21. Sardana A. Fedorova
  22. Mikhail I. Voevoda
  23. Michael DeGiorgio
  24. Thomas Sicheritz-Ponten
  25. Søren Brunak
  26. Svetlana Demeshchenko
  27. Toomas Kivisild
  28. Richard Villems
  29. Rasmus Nielsen
  30. Mattias Jakobsson
  31. Eske Willerslev

Contributions

E.W. and K.E.G. conceived the project. E.W. headed the project. E.W. and M.R. designed the experimental research project setup. S.D. and K.E.G. provided access to the Mal’ta and Afontova Gora-2 samples, and K.E.G. provided archaeological context for the samples. T.W.S. Jr performed AMS dating. E.B. and O.B. (Tajik individual), E.K. and S.L. (Mari and Avar individuals) provided modern DNA extracts for complete genome sequencing. E.K. and S.L. (Kazakh, Kirghiz, Uzbek and Mari individuals), L.P.O. (Selkup individuals), S.A.F. (Even, Dolgan and Yakut individuals) and M.I.V. (Altai individuals) provided access to modern DNA extracts for genotyping. R.V. carried out Illumina chip analysis on modern samples. P.F.C. performed DNA extraction from the Indian individual. M.R. performed the ancient extractions and library constructions on the modern and ancient samples —the latter with input from L.O. M.R. coordinated the sequencing. M.R. and S.Ra. performed mapping of MA-1 and AG-2 data sets with input from L.O. S.Ra., T.S.-P. and S.B. provided super-computing resources, developed the next-generation sequencing pipeline and performed mapping and genotyping for all the modern genomes. M.R. performed DNA damage analysis with input from L.O. M.M. performed the admixture analysis. M.M., E.M., K.T. and R.V. performed the mtDNA analysis. M.M., M.K., S.Ro., T.K., R.V. and R.M. performed the Y-chromosome analysis. A.A. and I.M. performed the autosomal contamination estimates, error rate estimates,D-statistics tests based on sequence reads and ngsAdmix analyses. P.S. performed biological sexing, mtDNA contamination estimates, PCA, TreeMix, MixMapper,D-statistic tests based on allele frequencies,f3-statistics and phenotypic analyses, and analysis of AG-2 using nucleotide misincorporation patterns under the supervision of R.N. and M.J. M.R., P.S. and E.W. wrote the majority of the manuscript with critical input from R.N., M.J., M.M., K.E.G., A.A., I.M. and M.D. M.M., A.A. and I.M. contributed equally to this work.

Corresponding author

Correspondence toEske Willerslev.

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Competing interests

The authors declare no competing financial interests.

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Raghavan, M., Skoglund, P., Graf, K.et al. Upper Palaeolithic Siberian genome reveals dual ancestry of Native Americans.Nature505, 87–91 (2014). https://doi.org/10.1038/nature12736

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Editorial Summary

Intertwining roots of the First Americans

Where did the First Americans come from, and who were they? On both counts the interpretation of the genetic and archaeological evidence causes controversy. The publication of the draft genome of a 24,000-year-old human specimen from Mal'ta in south-central Siberia — the earliest modern human genome sequence reported to date — may help to clarify matters. Eske Willerslev and colleagues find that the Mal'ta individual is genetically closely related to modern-day Native Americans and basal to modern-day western Eurasians, but has no close affinity to east Asians. This implies that populations related to modern-day western Eurasians had a more northeasterly distribution in the past than commonly thought. The authors estimate that between 14 and 38% of Native American ancestry originates from this ancient Mal'ta group and is therefore not of east Asian but rather of western Eurasian ancestry, which may explain why several First American crania have been reported as bearing non-east Asian features.

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