Article

Neolithic mitochondrial haplogroup H genomes and the genetic origins of Europeans

  • Nature Communications 4, Article number: 1764 (2013)
  • doi:10.1038/ncomms2656
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Abstract

Haplogroup H dominates present-day Western European mitochondrial DNA variability (>40%), yet was less common (~19%) among Early Neolithic farmers (~5450 BC) and virtually absent in Mesolithic hunter-gatherers. Here we investigate this major component of the maternal population history of modern Europeans and sequence 39 complete haplogroup H mitochondrial genomes from ancient human remains. We then compare this ‘real-time’ genetic data with cultural changes taking place between the Early Neolithic (~5450 BC) and Bronze Age (~2200 BC) in Central Europe. Our results reveal that the current diversity and distribution of haplogroup H were largely established by the Mid Neolithic (~4000 BC), but with substantial genetic contributions from subsequent pan-European cultures such as the Bell Beakers expanding out of Iberia in the Late Neolithic (~2800 BC). Dated haplogroup H genomes allow us to reconstruct the recent evolutionary history of haplogroup H and reveal a mutation rate 45% higher than current estimates for human mitochondria.

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Acknowledgements

We are indebted to Matt Kaplan and Ryan Spriggs at Arizona Research Laboratories, Division of Biotechnology, University of Arizona Genetics Core Facility, http://uagc.arl.arizona.edu/, Tyson Clark, Michael Brown, Kristi Spittle and Matthew Boitano (Pacific Biosciences) for sequencing work, Jeremy Timmis for help with DNA sonication protocols, and Robin Skeates, and Hubert Steiner for additional samples and contextual information. We thank the Australian Research Council (grant LP0882622), the Deutsche Forschungsgemeinschaft (Al 287/7-1 and Me 3245/1-1) and National Geographic’s Genographic Project for funding. M.v.O. was supported in part by the Netherlands Forensic Institute (NFI) and a grant from the Netherlands Genomics Initiative (NGI)/Netherlands Organization for Scientific Research (NWO) within the framework of the Forensic Genomics Consortium Netherlands (FGCN).

Author information

Author notes

    • Paul Brotherton
    •  & Wolfgang Haak

    These authors contributed equally to this work

    • Christina Jane Adler

    Present address: Institute of Dental Research, Westmead Centre for Oral Health, The University of Sydney, Sydney, New South Wales 2145, Australia

    • Clio Der Sarkissian

    Present address: Centre for Geogenetics, Natural History Museum of Denmark, 1350 Copenhagen, Denmark

Affiliations

  1. The Australian Centre for Ancient DNA, School of Earth and Environmental Sciences, University of Adelaide, Adelaide, South Australia 5005, Australia

    • Paul Brotherton
    • , Wolfgang Haak
    • , Jennifer Templeton
    • , Julien Soubrier
    • , Christina Jane Adler
    • , Stephen M. Richards
    • , Clio Der Sarkissian
    •  & Alan Cooper
  2. Archaeogenetics Research Group, School of Applied Sciences, University of Huddersfield, Huddersfield HD1 3DH, UK

    • Paul Brotherton
  3. Institute of Anthropology, Colonel-Kleinmann Weg 2, Johannes Gutenberg University Mainz, D-55128 Mainz, Germany

    • Guido Brandt
    •  & Kurt W. Alt
  4. State Office for Heritage Management and Archaeology Saxony-Anhalt/State Museum for Prehistory Halle, Richard-Wagner-Straße 9, D-06114 Halle/Saale, Germany

    • Robert Ganslmeier
    • , Susanne Friederich
    • , Veit Dresely
    •  & Harald Meller
  5. Department of Forensic Molecular Biology, Erasmus MC, University Medical Centre Rotterdam, 3000 CA Rotterdam, The Netherlands

    • Mannis van Oven
  6. SA Pathology, SA Health, Adelaide, South Australia 5000, Australia

    • Rosalie Kenyon
    •  & Mark B. Van der Hoek
  7. Pacific Biosciences, Menlo Park, California 94025, USA

    • Jonas Korlach
    •  & Khai Luong
  8. School of Biological Sciences, The University of Sydney, Sydney, New South Wales 2006, Australia

    • Simon Y.W. Ho
  9. Institut Pasteur, Unit of Evolutionary Genetics, 75015 Paris, France

    • Lluis Quintana-Murci
  10. Rambam Medical Centre, 31096 Haifa, Israel

    • Doron M. Behar
  11. The Genographic Laboratory, School of Biological Sciences, Madurai Kamaraj University, Madurai 625 021, Tamil Nadu, India

    • Syama Adhikarla
    • , Arun Kumar Ganesh Prasad
    • , Ramasamy Pitchappan
    •  & Arun Varatharajan Santhakumari
  12. Research Centre for Medical Genetics, Russian Academy of Medical Sciences, 115478 Moscow, Russia

    • Elena Balanovska
    •  & Oleg Balanovsky
  13. Institut de Biologia Evolutiva (CSIC-UPF), Departament de Ciences de la Salut i de la Vida, Universitat Pompeu Fabra, 08003 Barcelona, Spain

    • Jaume Bertranpetit
    • , David Comas
    • , Begoña Martínez-Cruz
    •  & Marta Melé
  14. Department of Anatomy, University of Otago, Dunedin 9054, New Zealand

    • Andrew C. Clarke
    •  & Elizabeth A. Matisoo-Smith
  15. Department of Anthropology, University of Pennsylvania, Philadelphia, Pennsylvania, 19104-6398, USA

    • Matthew C. Dulik
    • , Jill B. Gaieski
    • , Amanda C. Owings
    • , Theodore G. Schurr
    •  & Miguel G. Vilar
  16. National Health Laboratory Service, Sandringham 2131, Johannesburg, South Africa

    • Angela Hobbs
    •  & Himla Soodyall
  17. IBM, Yorktown Heights, New York 10598, USA

    • Asif Javed
    • , Laxmi Parida
    • , Daniel E. Platt
    •  & Ajay K. Royyuru
  18. School of Life Sciences and Institutes of Biomedical Sciences, Fudan University, Shanghai 200433, People’s Republic of China

    • Li Jin
    •  & Shilin Li
  19. Arizona Research Laboratories, University of Arizona, Tucson, Arizona 85721, USA

    • Matthew E. Kaplan
    •  & Nirav C. Merchant
  20. Department of Genetics, School of Molecular Sciences, La Trobe University, Melbourne, Victoria 3086, Australia

    • R John Mitchell
  21. McDonald Institute for Archaeological Research, University of Cambridge, Cambridge, CB2 3ER, UK

    • Colin Renfrew
  22. Departamento de Biologia Geral, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, CEP 31270-901, Brazil

    • Daniela R. Lacerda
    •  & Fabrício R Santos
  23. National Geographic Society, Washington, District of Columbia 20036-4688, USA

    • David F. Soria Hernanz
    •  & R Spencer Wells
  24. IBM, Somers, New York 10589, USA

    • Pandikumar Swamikrishnan
  25. Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, CB10 1SA, UK

    • Chris Tyler-Smith
  26. Universidade Federal do Rio de Janeiro, Rio de Janeiro, CEP 21941-901, Brazil

    • Pedro Paulo Vieira
  27. Applied Biosystems, Foster City, California 94494, USA

    • Janet S. Ziegle

Consortia

  1. The Genographic Consortium

    A full list of authors for the Genographic Consortium and their affiliations appears at the end of the paper.

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Contributions

P.B., W.H. and A.C. conceived and designed the project. P.B. designed and developed the DNA extraction, DNA library construction and hybridisation-based DNA-capture protocols (with assistance from J.T.). P.B., J.T. and W.H. generated and analysed the data. S.M.R., C.D., R.K. and M.B.v.d.H. contributed experimental steps and C.J.A., J.S., S.Y.W.H., J.K. and K.L. contributed analytical steps. G.B., R.G., S.F., V.D., M.v.O., L.Q., D.M.B., H.M. and K.W.A. provided ancient samples, contextual information, radiocarbon dating and access to critical population data. P.B., W.H. and A.C. wrote the manuscript with input from C.J.A., J.S., S.Y.W.H., S.M.R., J.K. and members of the Genographic Consortium. All authors discussed the paper and gave comments.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Paul Brotherton or Wolfgang Haak.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Figures S1-S4, Supplementary Tables S1-S8, Supplementary Methods and Supplementary References

Excel files

  1. 1.

    Supplementary Data 1

    Details on contamination rate estimates from next generation sequencing data for six ancient hg H samples

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