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.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
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.
Krause, J. et al. The complete mitochondrial DNA genome of an unknown hominin from southern Siberia. Nature 464, 894–897 (2010).
Reich, D. et al. Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468, 1053–1060 (2010).
Prüfer, K. et al. The complete genome sequence of a Neanderthal from the Altai Mountains. Nature 505, 43–49 (2014).
Slon, V. et al. The genome of the offspring of a Neanderthal mother and a Denisovan father. Nature 561, 113–116 (2018).
Prüfer, K. et al. A high-coverage Neandertal genome from Vindija Cave in Croatia. Science 358, 655–658 (2017).
Sawyer, S. et al. Nuclear and mitochondrial DNA sequences from two Denisovan individuals. Proc. Natl Acad. Sci. USA 112, 15696–15700 (2015).
Slon, V. et al. A fourth Denisovan individual. Sci. Adv. 3, e1700186 (2017).
Slon, V. et al. Neandertal and Denisovan DNA from Pleistocene sediments. Science 356, 605–608 (2017).
Derevianko, A. P., Laukhin, S. A., Kulikov, O. A., Gnibidenko, Z. N. & Shunkov, M. V. First Middle Pleistocene age determinations of the Paleolithic in the Altai Mountains. Dokl. Akad. Nauk 326, 497–501 (1992).
Jacobs, Z. et al. Timing of archaic hominin occupation of Denisova Cave in southern Siberia. Nature https://doi.org/10.1038/s41586-018-0843-2 (2019).
Brown, S. et al. Identification of a new hominin bone from Denisova Cave, Siberia using collagen fingerprinting and mitochondrial DNA analysis. Sci. Rep. 6, 23559 (2016).
Fu, Q. et al. Genome sequence of a 45,000-year-old modern human from western Siberia. Nature 514, 445–449 (2014).
Bronk Ramsey, C. Bayesian analysis of radiocarbon dates. Radiocarbon 51, 337–360 (2009).
Meyer, M. et al. A mitochondrial genome sequence of a hominin from Sima de los Huesos. Nature 505, 403–406 (2014).
Sankararaman, S., Mallick, S., Patterson, N. & Reich, D. The combined landscape of Denisovan and Neanderthal ancestry in present-day humans. Curr. Biol. 26, 1241–1247 (2016).
Malaspinas, A.-S. et al. A genomic history of Aboriginal Australia. Nature 538, 207–214 (2016).
Derevianko, A. P. The Upper Paleolithic in Africa and Eurasia and the Origin of Anatomically Modern Humans (in Russian) (SB RAS, Novosibirsk, 2011).
Reimer, P. J. et al. IntCal13 and Marine13 radiocarbon age calibration curves 0–50,000 years cal. bp. Radiocarbon 55, 1869–1887 (2013).
Lisiecki, L. E. & Raymo, M. E. A Pliocene-Pleistocene stack of 57 globally distributed benthic δ18O records. Paleoceanography 20, PA1003 (2005).
Brock, F. et al. Current pretreatment methods for AMS radiocarbon dating at the Oxford Radiocarbon Accelerator Unit (ORAU). Radiocarbon 52, 103–112 (2010).
Devièse, T., Comeskey, D., McCullagh, J., Bronk Ramsey, C. & Higham, T. New protocol for compound-specific radiocarbon analysis of archaeological bones. Rapid Commun. Mass Spectrom. 32, 373–379 (2018).
Bird, M. I. et al. Radiocarbon dating of “old” charcoal using a wet oxidation, stepped-combustion procedure. Radiocarbon 41, 127–140 (1999).
Buckley, M. & Kansa, S. W. Collagen fingerprinting of archaeological bone and teeth remains from Domuztepe, South Eastern Turkey. Archaeol. Anthropol. Sci. 3, 271–280 (2011).
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).
Korlević, P. et al. Reducing microbial and human contamination in DNA extractions from ancient bones and teeth. Biotechniques 59, 87–93 (2015).
Gansauge, M. T. et al. Single-stranded DNA library preparation from highly degraded DNA using T4 DNA ligase. Nucleic Acids Res. 45, e79 (2017).
Kircher, M., Sawyer, S. & Meyer, M. Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform. Nucleic Acids Res. 40, e3 (2012).
Fu, Q. et al. DNA analysis of an early modern human from Tianyuan Cave, China. Proc. Natl Acad. Sci. USA 110, 2223–2227 (2013).
Renaud, G., Stenzel, U. & Kelso, J. leeHom: adaptor trimming and merging for Illumina sequencing reads. Nucleic Acids Res. 42, e141 (2014).
Li, H. & Durbin, R. Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics 26, 589–595 (2010).
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.
Nature thanks R. Dennell, E. J. Rhodes and the other anonymous reviewer(s) for their contribution to the peer review of this work.
The authors declare no competing interests.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data figures and tables
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.
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.
Details of modelling are given in the Supplementary Information, section 9.
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.
About this article
Cite this article
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
The application of geometric-morphometric shape analysis to Middle Paleolithic bone retouchers from the Altai Mountains, Russia
Quaternary International (2020)
Journal of Human Evolution (2020)
Fabric Analysis and Chronology at Ga-Mohana Hill North Rockshelter, Southern Kalahari Basin: Evidence for In Situ, Stratified Middle and Later Stone Age Deposits
Journal of Paleolithic Archaeology (2020)
PLOS ONE (2020)