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Age estimates for hominin fossils and the onset of the Upper Palaeolithic at Denisova Cave

Nature volume 565, pages 640–644 (2019)Cite this article

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Abstract

Denisova Cave in the Siberian Altai (Russia) is a key site for understanding the complex relationships between hominin groups that inhabited Eurasia in the Middle and Late Pleistocene epoch. DNA sequenced from human remains found at this site has revealed the presence of a hitherto unknown hominin group, the Denisovans1,2, and high-coverage genomes from both Neanderthal and Denisovan fossils provide evidence for admixture between these two populations3. Determining the age of these fossils is important if we are to understand the nature of hominin interaction, and aspects of their cultural and subsistence adaptations. Here we present 50 radiocarbon determinations from the late Middle and Upper Palaeolithic layers of the site. We also report three direct dates for hominin fragments and obtain a mitochondrial DNA sequence for one of them. We apply a Bayesian age modelling approach that combines chronometric (radiocarbon, uranium series and optical ages), stratigraphic and genetic data to calculate probabilistically the age of the human fossils at the site. Our modelled estimate for the age of the oldest Denisovan fossil suggests that this group was present at the site as early as 195,000 years ago (at 95.4% probability). All Neanderthal fossils—as well as Denisova 11, the daughter of a Neanderthal and a Denisovan4—date to between 80,000 and 140,000 years ago. The youngest Denisovan dates to 52,000–76,000 years ago. Direct radiocarbon dating of Upper Palaeolithic tooth pendants and bone points yielded the earliest evidence for the production of these artefacts in northern Eurasia, between 43,000 and 49,000 calibrated years before present (taken as ad 1950). On the basis of current archaeological evidence, it may be assumed that these artefacts are associated with the Denisovan population. It is not currently possible to determine whether anatomically modern humans were involved in their production, as modern-human fossil and genetic evidence of such antiquity has not yet been identified in the Altai region.

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Fig. 1: Radiocarbon age determinations from East Chamber and Main Chamber, Denisova Cave.
Fig. 2: Comparison between the radiocarbon determinations obtained for the oldest bone points and tooth pendants from Denisova Cave and the two direct dates for the Ust’-Ishim modern human femur.
Fig. 3: Stratigraphic sequences for the southeast profiles exposed in the three chambers at Denisova Cave and images of human fossil remains.
Fig. 4: Age estimates for the human fossils from Denisova Cave as determined from Bayesian model 4, compared against the marine oxygen isotope curve from benthic δ18O records.

Data availability

Raw radiocarbon determinations and associated chemical data, calibrated age ranges and CQL codes for the Bayesian models are included in the Supplementary Information. All MALDI-ToF-MS raw data for the ZooMS analyses are available from the corresponding authors upon request. The mtDNA capture data for Denisova 11, Denisova 14 and Denisova 15 are available in the European Nucleotide Archive under accession number PRJEB29061. The mtDNA sequence of Denisova 15 can be downloaded from GenBank (accession number MK033602). All other relevant data are available from the corresponding authors or are included in the Letter or its Supplementary Information.

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Acknowledgements

Funding for this research was received from the European Research Council (ERC) under the European Union’s Seventh Framework Program (FP7/2007-2013); grant no. 324139 (PalaeoChron) awarded to T.H.; grant no. 715069 (FINDER) awarded to K.D.; grant no. 694707 (100 Archaic Genomes) awarded to S.P. The Max Planck Society provided support to S.P., V.S., F.M., M.M., J.K., K.D. and S.B. The Australian Research Council funded research fellowships to Z.J. (FT150100138), B.L. (FT14010038) and R.G.R. (FL130100116). The Royal Society funded a University Research Fellowship to M.B. B.V. was supported by the Social Sciences and Humanities Research Council (Canada). The archaeological field studies were funded by the Russian Science Foundation (project no. 14-50-00036 to A.P.D.) and the Russian Foundation for Basic Research (project no. 17-29-04206 to M.V.S. and M.B.K.). K.D., T.H. and T.D. thank Brasenose and Keble Colleges, University of Oxford, for funding and support. We thank staff at the Oxford Radiocarbon Accelerator Unit (ORAU), E. Gillespie and M. Higham Jenkins for their contribution to the radiocarbon dating and ZooMS work; and M. Ruddy for contributing to the marine oxygen isotope curve data used here (https://github.com/markruddy/ois5e-plot). D Challinor identified the charcoal before radiocarbon dating. I. Cartwright (University of Oxford) photographed Denisova 11, Denisova 14, Denisova 15 and Denisova 16. Y. Jafari, K. O’Gorman and T. Lachlan helped with optical-dating sample preparation and data analysis. S. Nagel, B. Nickel, B. Schellbach and A. Weihmann helped with DNA sample preparation; and A. Hübner gave input on the BEAST analysis.

Reviewer information

Nature thanks R. Dennell, E. J. Rhodes and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Authors and Affiliations

  1. Department of Archaeology, Max Planck Institute for the Science of Human History, Jena, Germany

    Katerina Douka & Samantha Brown

  2. Oxford Radiocarbon Accelerator Unit, Research Laboratory for Archaeology and the History of Art, University of Oxford, Oxford, UK

    Katerina Douka, Christopher Bronk Ramsey, Daniel Comeskey, Thibaut Devièse & Tom Higham

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

    Viviane Slon, Fabrizio Mafessoni, Matthias Meyer, Svante Pääbo & Janet Kelso

  4. Centre for Archaeological Science, School of Earth, Atmospheric and Life Sciences, University of Wollongong, Wollongong, New South Wales, Australia

    Zenobia Jacobs, Bo Li & Richard G. Roberts

  5. Australian Research Council (ARC) Centre of Excellence for Australian Biodiversity and Heritage, University of Wollongong, Wollongong, New South Wales, Australia

    Zenobia Jacobs, Bo Li & Richard G. Roberts

  6. Institute of Archaeology and Ethnography, Russian Academy of Sciences Siberian Branch, Novosibirsk, Russia

    Michael V. Shunkov, Anatoly P. Derevianko & Maxim B. Kozlikin

  7. Novosibirsk State University, Novosibirsk, Russia

    Michael V. Shunkov

  8. Altai State University, Barnaul, Russia

    Anatoly P. Derevianko

  9. Australian Research Centre for Human Evolution, Griffith University, Brisbane, Queensland, Australia

    Rainer Grün

  10. Department of Anthropology, University of Toronto, Toronto, Ontario, Canada

    Bence Viola

  11. Research School of Earth Sciences, The Australian National University, Canberra, Australian Capital Territory, Australia

    Leslie Kinsley

  12. Manchester Institute of Biotechnology, University of Manchester, Manchester, UK

    Michael Buckley

Authors
  1. Katerina Douka
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  2. Viviane Slon
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  3. Zenobia Jacobs
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  4. Christopher Bronk Ramsey
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Contributions

K.D., V.S., Z.J., B.L., D.C., L.K., T.D., S.B., B.V. and M.B. performed the laboratory work; K.D., T.H., C.B.R., D.C. and T.D. obtained and analysed the radiocarbon data. V.S., F.M., J.K., M.M. and S.P. analysed the genetic data; C.B.R., K.D. and T.H. designed and tested the Bayesian models. S.B. and M.B. analysed the ZooMS samples. B.V. carried out morphological analyses of the fossils. Z.J., B.L. and R.G.R. analysed the optical dating data. L.K. and R.G. obtained and analysed the U-series data. A.P.D., M.V.S. and M.B.K. excavated the site and analysed all archaeological data. K.D., T.H. and Z.J. wrote the manuscript with input from all authors.

Corresponding authors

Correspondence to Katerina Douka or Tom Higham.

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Extended data figures and tables

Extended Data Fig. 1 Human remains from Denisova Cave.

Red labels indicate Denisovans; blue labels indicate Neanderthals; and grey labels indicate Homo sp. bones that have not been assigned to a group. Denisova 11 is shown in red and blue. A further, unpublished Denisovan specimen (Denisova 13) is mentioned in the Supplementary Information, section 3. a, b, Denisova 2 in occlusal (a) and lingual (b) views. c, Denisova 3 in proximal view. d, e, Denisova 4 in mesial (d) and occlusal (e) views. f, Denisova 8 in occlusal view. g, Denisova 9 in palmar view. h, i, Renderings based on micro-computed tomography of Denisova 5 in lateral (h) and plantar (i) views. j, Denisova 15. k, Denisova 11. l, Denisova 14. m, Denisova 16. n, o, Denisova 6 in occlusal (n) and lingual (o) views.

Extended Data Fig. 2 Personal ornaments and bone points from Denisova Cave that were sampled for radiocarbon dating.

N28 was discovered during section cleaning and is not assigned to a specific layer. N282 did not produce enough collagen, and was not dated. N3856/66 was dated twice. Direct dates are listed in Extended Data Table 1.

Extended Data Fig. 3 Proteomic and genetic data for hominin bones discovered using ZooMS.

a–d, Collagen fingerprinting MALDI-ToF-MS spectra for Denisova 11, Denisova 14, Denisova 15 and Denisova 16. e–g, Average coverage of the human mitochondrial reference genome for Denisova 11, Denisova 14 and Denisova 15. The average coverage of the mitochondrial genome is twofold for the sequences from Denisova 14, and 62.7-fold for Denisova 15. The low collagen preservation indicated for Denisova 14 on the basis of its peptide fingerprint correlates well with the poor recovery of ancient DNA from the same specimen.

Extended Data Fig. 4 Inferred number of substitutions that occur on branches that lead to the mtDNA genomes of Denisovan and Neanderthal individuals, since their split from the common ancestor that they share with other archaic individuals.

Denisovan (DS) and Neanderthal (NS) split age estimates used in the Bayesian models to enable numerical calculation of the split times of the various points on this tree. Individuals from Denisova Cave are emphasized in bold. a, Denisovan mtDNA genomes (data taken from a previous publication7). b, Neanderthal mtDNA genomes; genomes used in this analysis are reported in Supplementary Table 6.

Extended Data Fig. 5 Bayesian age models (models 1 and 2).

Details of modelling are given in the Supplementary Information, section 9.

Extended Data Fig. 6 Bayesian age models (models 3 and 4).

Model 4 contains the most prior information and yielded very a high agreement index. We use this model to calculate and report the ages of the human fossils (Extended Data Table 2). Details of modelling are given in the Supplementary Information, section 9.

Extended Data Fig. 7 Comparison of hominin ages estimated on the basis of different types of data.

Models 1 to 4 include stratigraphic information, mitochondrial mutation rates, radiocarbon dates and 11 optical ages, and are described in the Supplementary Information, section 9. The green bars show hominin ages derived from a model based on optical ages only (not presented here), which includes all data reported elsewhere10. The red bars show schematic age ranges that were estimated using both mitochondrial and nuclear DNA data. All ages are at 95.4% probability.

Extended Data Table 1 Radiocarbon results from Denisova Cave
Full size table
Extended Data Table 2 Comparison of the modelled age estimates for human fossils obtained from Bayesian models 1 to 4
Full size table

Supplementary information

Supplementary Information

This file contains supplementary text 1-9 which includes figures S1-S30 and tables S1-S15.

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Douka, K., Slon, V., Jacobs, Z. et al. Age estimates for hominin fossils and the onset of the Upper Palaeolithic at Denisova Cave. Nature 565, 640–644 (2019). https://doi.org/10.1038/s41586-018-0870-z

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