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An early modern human from Romania with a recent Neanderthal ancestor

Nature volume 524, pages 216–219 (2015)Cite this article

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Abstract

Neanderthals are thought to have disappeared in Europe approximately 39,000–41,000 years ago but they have contributed 1–3% of the DNA of present-day people in Eurasia1. Here we analyse DNA from a 37,000–42,000-year-old2 modern human from Peştera cu Oase, Romania. Although the specimen contains small amounts of human DNA, we use an enrichment strategy to isolate sites that are informative about its relationship to Neanderthals and present-day humans. We find that on the order of 6–9% of the genome of the Oase individual is derived from Neanderthals, more than any other modern human sequenced to date. Three chromosomal segments of Neanderthal ancestry are over 50 centimorgans in size, indicating that this individual had a Neanderthal ancestor as recently as four to six generations back. However, the Oase individual does not share more alleles with later Europeans than with East Asians, suggesting that the Oase population did not contribute substantially to later humans in Europe.

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Figure 1: Allele sharing between the Oase 1 individual and other genomes.
Figure 2: Spatial distribution of alleles matching Neanderthals in modern humans.

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Accession codes

Primary accessions

European Nucleotide Archive

Data deposits

The aligned sequences have been deposited in the European Nucleotide Archive under accession number PRJEB8987.

References

  1. Higham, T. et al. The timing and spatiotemporal patterning of Neanderthal disappearance. Nature 512, 306–309 (2014)

    Article  CAS  ADS  Google Scholar 

  2. Trinkaus, E. et al. An early modern human from the Pestera cu Oase, Romania. Proc. Natl Acad. Sci. USA 100, 11231–11236 (2003)

    Article  CAS  ADS  Google Scholar 

  3. Smith, F. H. et al. The assimilation model, modern human origins in Europe, and the extinction of Neandertals. Quat. Int. 137, 7–19 (2005)

    Article  Google Scholar 

  4. Zilhão, J. Neandertals and moderns mixed, and it matters. Evol. Anthropol. 15, 183–195 (2006)

    Article  Google Scholar 

  5. Hublin, J.-J. The modern human colonization of western Eurasia: when and where? Quat. Sci. Rev. 118, 194–210 (2014)

    Article  ADS  Google Scholar 

  6. Green, R. E. et al. A draft sequence of the Neandertal genome. Science 328, 710–722 (2010)

    Article  CAS  ADS  Google Scholar 

  7. Prüfer, K. et al. The complete genome sequence of a Neanderthal from the Altai Mountains. Nature 505, 43–49 (2014)

    Article  ADS  Google Scholar 

  8. Sankararaman, S. et al. The date of interbreeding between Neandertals and modern humans. PLoS Genet. 8, e1002947 (2012)

    Article  CAS  Google Scholar 

  9. Meyer, M. et al. A high-coverage genome sequence from an archaic Denisovan individual. Science 338, 222–226 (2012)

    Article  CAS  ADS  Google Scholar 

  10. Wall, J. D. et al. Higher levels of Neanderthal ancestry in East Asians than in Europeans. Genetics 194, 199–209 (2013)

    Article  Google Scholar 

  11. Kim, B. Y. & Lohmueller, K. E. Selection and reduced population size cannot explain higher amounts of Neandertal ancestry in East Asian than in European human populations. Am. J. Hum. Genet. 96, 454–461 (2015)

    Article  CAS  Google Scholar 

  12. Vernot, B. & Akey, J. M. Complex history of admixture between modern humans and Neandertals. Am. J. Hum. Genet. 96, 448–453 (2015)

    Article  CAS  Google Scholar 

  13. d’Errico, F. et al. Neanderthal acculturation in Western Europe? A critical review of the evidence and its interpretation. Curr. Anthropol. 39 (suppl.). S1–S44 (1998)

    Article  Google Scholar 

  14. Mellars, P. The impossible coincidence: a single-species model for the origins of modern human behavior in Europe. Evol. Anthropol. 14, 12–27 (2005)

    Article  Google Scholar 

  15. Fu, Q. et al. Genome sequence of a 45,000-year-old modern human from western Siberia. Nature 514, 445–449 (2014)

    Article  CAS  ADS  Google Scholar 

  16. Seguin-Orlando, A. et al. Paleogenomics. Genomic structure in Europeans dating back at least 36,200 years. Science 346, 1113–1118 (2014)

    Article  CAS  ADS  Google Scholar 

  17. Rougier, H. et al. Peştera cu Oase 2 and the cranial morphology of early modern Europeans. Proc. Natl Acad. Sci. USA 104, 1165–1170 (2007)

    Article  CAS  ADS  Google Scholar 

  18. Constantin, S. et al. Reconstructing the evolution of cave systems as a key to understanding the taphonomy of fossil accumulations: the case of Urşilor Cave (Western Carpathians, Romania). Quat. Int. 339–340, 25–40 (2014)

    Article  Google Scholar 

  19. Ackermann, R. R. Phenotypic traits of primate hybrids: Recognizing admixture in the fossil record. Evolutionary Anthropology: Issues, News, and Reviews 19. 258–270 (2010)

  20. Frayer, D. in Continuity or Replacement? Controversies in Homo sapiens Evolution (eds Bräuer, G. & Smith, F. H. ) (A.A. Balkema Publishers, 1992)

    Google Scholar 

  21. Trinkaus, E. et al. Life and Death at the Peştera cu Oase. A Setting for Modern Human Emergence in Europe (Oxford Univ. Press, 2013)

    Google Scholar 

  22. Briggs, A. W. et al. Removal of deaminated cytosines and detection of in vivo methylation in ancient DNA. Nucleic Acids Res. 38, e87 (2010)

    Article  Google Scholar 

  23. Fu, Q. et al. DNA analysis of an early modern human from Tianyuan Cave, China. Proc. Natl Acad. Sci. USA 110, 2223–2227 (2013)

    Article  CAS  ADS  Google Scholar 

  24. Sawyer, S. et al. Temporal patterns of nucleotide misincorporations and DNA fragmentation in ancient DNA. PLoS ONE 7, e34131 (2012)

    Article  CAS  ADS  Google Scholar 

  25. Meyer, M. et al. A mitochondrial genome sequence of a hominin from Sima de los Huesos. Nature 505, 403–406 (2014)

    Article  CAS  ADS  Google Scholar 

  26. Skoglund, P. et al. Separating endogenous ancient DNA from modern day contamination in a Siberian Neandertal. Proc. Natl Acad. Sci. USA 111, 2229–2234 (2014)

    Article  CAS  ADS  Google Scholar 

  27. Patterson, N. et al. Ancient admixture in human history. Genetics 192, 1065–1093 (2012)

    Article  Google Scholar 

  28. Lazaridis, I. et al. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513, 409–413 (2014)

    Article  CAS  ADS  Google Scholar 

  29. Reich, D. et al. Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468, 1053–1060 (2010)

    Article  CAS  ADS  Google Scholar 

  30. Trinkaus, E. European early modern humans and the fate of the Neandertals. Proc. Natl Acad. Sci. USA 104, 7367–7372 (2007)

    Article  CAS  ADS  Google Scholar 

  31. Dabney, J. et al. Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proc. Natl Acad. Sci. USA 110, 15758–15763 (2013)

    Article  CAS  ADS  Google Scholar 

  32. Gansauge, M. T. & Meyer, M. Single-stranded DNA library preparation for the sequencing of ancient or damaged DNA. Nature Protocols 8, 737–748 (2013)

    Article  Google Scholar 

  33. Briggs, A. W. et al. Patterns of damage in genomic DNA sequences from a Neandertal. Proc. Natl Acad. Sci. USA 104, 14616–14621 (2007)

    Article  CAS  ADS  Google Scholar 

  34. Dabney, J. & Meyer, M. Length and GC-biases during sequencing library amplification: a comparison of various polymerase-buffer systems with ancient and modern DNA sequencing libraries. Biotechniques 52, 87–94 (2012)

    Article  CAS  Google Scholar 

  35. Kircher, M., Sawyer, S. & Meyer, M. Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform. Nucleic Acids Res. 40, e3 (2012)

    Article  CAS  Google Scholar 

  36. Haak, W. et al. Massive migration from the steppe was a source for Indo-European languages in Europe. Nature 522, 207–211 (2015)

    Article  CAS  ADS  Google Scholar 

  37. The 1000 Genomes Project Consortium. An integrated map of genetic variation from 1,092 human genomes. Nature 491, 56–65 (2012)

  38. Paten, B., Herrero, J., Beal, K., Fitzgerald, S. & Birney, E. Enredo and Pecan: genome-wide mammalian consistency-based multiple alignment with paralogs. Genome Res. 18, 1814–1828 (2008)

    Article  CAS  Google Scholar 

  39. Paten, B. et al. Genome-wide nucleotide-level mammalian ancestor reconstruction. Genome Res. 18, 1829–1843 (2008)

    Article  CAS  Google Scholar 

  40. Raghavan, M. et al. Upper Palaeolithic Siberian genome reveals dual ancestry of Native Americans. Nature 505, 87–91 (2014)

    Article  ADS  Google Scholar 

  41. Olalde, I. et al. Derived immune and ancestral pigmentation alleles in a 7,000-year-old Mesolithic European. Nature 507, 225–228 (2014)

    Article  CAS  ADS  Google Scholar 

Download references

Acknowledgements

We thank E. Trinkaus for facilitating the sampling of Oase 1, J. Krause for help with sampling and initial DNA analyses, A. Aximu for help with DNA hybridization captures and library preparation, and E. Trinkaus and L. Vigilant for critical reading of the manuscript. Q.F. is funded in part by the Chinese Academy of Sciences (XDA05130202) and the Special Foundation of the President of the Chinese Academy of Sciences (2015-2016). O.T.M. and S.C. are supported by the Romanian National Research Council through project PCCE 31/2010 (Karst Climate Archives). D.R. is supported by US National Science Foundation HOMINID grant BCS-1032255, US National Institutes of Health grant GM100233, and the Howard Hughes Medical Institute. The laboratory work was funded by the Presidential Innovation Fund of the Max Planck Society.

Author information

Author notes

  1. Qiaomei Fu and Mateja Hajdinjak: These authors contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, IVPP, CAS, Beijing, 100044, China

    Qiaomei Fu

  2. Department of Genetics, Harvard Medical School, Boston, 02115, Massachusetts, USA

    Qiaomei Fu, Swapan Mallick, Pontus Skoglund, Nadin Rohland, Iosif Lazaridis & David Reich

  3. Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Anthropology, Leipzig, 04103, Germany

    Qiaomei Fu, Mateja Hajdinjak, Birgit Nickel, Bence Viola, Kay Prüfer, Matthias Meyer, Janet Kelso & Svante Pääbo

  4. “Emil Racoviţă” Institute of Speleology, Cluj Branch, Cluj, 400006, Romania

    Oana Teodora Moldovan

  5. Department of Geospeleology and Paleontology, “Emil Racoviţă” Institute of Speleology, Bucharest 12, 010986, Romania

    Silviu Constantin

  6. Broad Institute of MIT and Harvard, Cambridge, 02142, Massachusetts, USA

    Swapan Mallick, Nick Patterson & David Reich

  7. Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, 04103, Germany

    Swapan Mallick & Bence Viola

  8. Department of Anthropology, University of Toronto, Toronto, M5S 2S2, Ontario, Canada

    Bence Viola

  9. Howard Hughes Medical Institute, Harvard Medical School, Boston, 02115, Massachusetts, USA

    David Reich

Authors
  1. Qiaomei Fu
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Contributions

N.P., K.P., M.M., J.K., D.R. and S.P. supervised the study. S.C. and O.T.M. collected and analysed archaeological material. Q.F., M.H. and B.N. performed laboratory work. Q.F., M.H., S.M., P.S., N.P., N.R., I.L., B.V., K.P., J.K. and D.R. analysed data. Q.F., S.M., M.M. and D.R. designed capture probes. D.R. and S.P. wrote the manuscript with the help of all co-authors.

Corresponding authors

Correspondence to David Reich or Svante Pääbo.

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Competing interests

The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Mitochondrial DNA tree for Oase 1 and other modern humans.

The consensus sequences for all Oase 1 fragments and for deaminated fragments are shown. The tree is rooted with a Neanderthal mtDNA (Vindija33.25).

Extended Data Table 1 Allele sharing between early modern humans and other humans
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Extended Data Table 2 Allele sharing between early modern humans and other humans (transversions only)
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Extended Data Table 3 Testing whether archaic genomes share more alleles with Oase 1 than with other modern humans
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Extended Data Table 4 Estimated fraction of the Oase 1 genome that derives from Neanderthals
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Extended Data Table 5 Counts of putative Neanderthal alleles in six modern humans
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Extended Data Table 6 Ancient DNA libraries made from the Oase 1 mandible
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Extended Data Table 7 Sequencing metrics on the five libraries for the four capture probe panels
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Extended Data Table 8 Effect of filtering on amount of nuclear data available
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Extended Data Table 9 Genomes merged with the Oase 1 data
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Supplementary information

Supplementary Information

This file contains Supplementary Notes 1-5 and Supplementary References. (PDF 1303 kb)

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Fu, Q., Hajdinjak, M., Moldovan, O. et al. An early modern human from Romania with a recent Neanderthal ancestor. Nature 524, 216–219 (2015). https://doi.org/10.1038/nature14558

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