Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Widespread Denisovan ancestry in Island Southeast Asia but no evidence of substantial super-archaic hominin admixture

Nature Ecology & Evolution volume 5, pages 616–624 (2021)Cite this article

Subjects

Abstract

The hominin fossil record of Island Southeast Asia (ISEA) indicates that at least two endemic ‘super-archaic’ species—Homo luzonensis and H. floresiensis—were present around the time anatomically modern humans arrived in the region >50,000 years ago. Intriguingly, contemporary human populations across ISEA carry distinct genomic traces of ancient interbreeding events with Denisovans—a separate hominin lineage that currently lacks a fossil record in ISEA. To query this apparent disparity between fossil and genetic evidence, we performed a comprehensive search for super-archaic introgression in >400 modern human genomes, including >200 from ISEA. Our results corroborate widespread Denisovan ancestry in ISEA populations, but fail to detect any substantial super-archaic admixture signals compatible with the endemic fossil record of ISEA. We discuss the implications of our findings for the understanding of hominin history in ISEA, including future research directions that might help to unlock more details about the prehistory of the enigmatic Denisovans.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Introgression signals in extant populations across ISEA.
Fig. 2: Results from coalescent simulations exploring the detection of archaic hominin introgressed sequences.
Fig. 3: Hominin occupation and megafauna survival in ISEA at the time of modern human arrival.

Data availability

The genetic datasets analysed during the current study were downloaded from, and are available at, the European Genome-phenome Archive (accession number EGAS00001003054; https://www.ebi.ac.uk/ega/home) and the Estonian Biocentre data archive (http://evolbio.ut.ee).

References

  1. Kaifu, Y. Archaic hominin populations in Asia before the arrival of modern humans: their phylogeny and implications for the ‘southern Denisovans’. Curr. Anthropol. 58, S418–S433 (2017).

    Article  Google Scholar 

  2. Morwood, M. J., O’Sullivan, P., Susanto, E. E. & Aziz, F. Revised age for Mojokerto 1, an early Homo erectus cranium from east Java, Indonesia. Aust. Archaeol. 57, 1–4 (2003).

    Article  Google Scholar 

  3. Rizal, Y. et al. Last appearance of Homo erectus at Ngandong, Java, 117,000–108,000 years ago. Nature 577, 381–385 (2020).

    Article  CAS  PubMed  Google Scholar 

  4. Matsu’ura, S. et al. Age control of the first appearance datum for Javanese in the Sangiran area. Science 367, 210–214 (2020).

    Article  PubMed  CAS  Google Scholar 

  5. Westaway, K. E. et al. An early modern human presence in Sumatra 73,000–63,000 years ago. Nature 548, 322–325 (2017).

    Article  CAS  PubMed  Google Scholar 

  6. Clarkson, C. et al. Human occupation of northern Australia by 65,000 years ago. Nature 547, 306–310 (2017).

    Article  CAS  PubMed  Google Scholar 

  7. Bowdler, S. ‘Human occupation of northern Australia by 65,000 years ago’ (Clarkson et al. 2017): a discussion. Aust. Archaeol. 83, 162–163 (2017).

    Article  Google Scholar 

  8. O’Connell, J. F. et al. When did Homo sapiens first reach Southeast Asia and Sahul? Proc. Natl Acad. Sci. USA 115, 8482–8490 (2018).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  9. Brown, P. et al. A new small-bodied hominin from the Late Pleistocene of Flores, Indonesia. Nature 431, 1055–1061 (2004).

    Article  CAS  PubMed  Google Scholar 

  10. Sutikna, T. et al. Revised stratigraphy and chronology for Homo floresiensis at Liang Bua in Indonesia. Nature 532, 366–369 (2016).

    Article  CAS  PubMed  Google Scholar 

  11. Détroit, F. et al. A new species of Homo from the Late Pleistocene of the Philippines. Nature 568, 181–186 (2019).

    Article  PubMed  CAS  Google Scholar 

  12. Brown, P. & Maeda, T. Liang Bua Homo floresiensis mandibles and mandibular teeth: a contribution to the comparative morphology of a new hominin species. J. Hum. Evol. 57, 571–596 (2009).

    Article  PubMed  Google Scholar 

  13. Argue, D., Groves, C. P., Lee, M. S. Y. & Jungers, W. L. The affinities of Homo floresiensis based on phylogenetic analyses of cranial, dental, and postcranial characters. J. Hum. Evol. 107, 107–133 (2017).

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Chen, F. et al. A late Middle Pleistocene Denisovan mandible from the Tibetan Plateau. Nature 569, 409–412 (2019).

    Article  CAS  PubMed  Google Scholar 

  17. Zhang, D. et al. Denisovan DNA in Late Pleistocene sediments from Baishiya Karst Cave on the Tibetan Plateau. Science 370, 584–587 (2020).

    Article  CAS  PubMed  Google Scholar 

  18. Reich, D. et al. Denisova admixture and the first modern human dispersals into Southeast Asia and Oceania. Am. J. Hum. Genet. 89, 516–528 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Jinam, T. A. et al. Discerning the origins of the Negritos, First Sundaland People: deep divergence and archaic admixture. Genome Biol. Evol. 9, 2013–2022 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Browning, S. R., Browning, B. L., Zhou, Y., Tucci, S. & Akey, J. M. Analysis of human sequence data reveals two pulses of archaic Denisovan admixture. Cell 173, 53–61.e9 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Mondal, M., Bertranpetit, J. & Lao, O. Approximate Bayesian computation with deep learning supports a third archaic introgression in Asia and Oceania. Nat. Commun. 10, 246 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Jacobs, G. S. et al. Multiple deeply divergent Denisovan ancestries in Papuans. Cell 177, 1010–1021.e32 (2019).

    Article  CAS  PubMed  Google Scholar 

  23. Teixeira, J. C. & Cooper, A. Using hominin introgression to trace modern human dispersals. Proc. Natl Acad. Sci. USA 116, 15327–15332 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Bergström, A. et al. Insights into human genetic variation and population history from 929 diverse genomes. Science 367, eaay5012 (2020).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. van den Bergh, G. D. et al. Earliest hominin occupation of Sulawesi, Indonesia. Nature 529, 208–211 (2016).

    Article  PubMed  CAS  Google Scholar 

  26. Wallace, A. R. On the physical geography of the Malay Archipelago. Proc. R. Geographical Soc. Lond. 33, 217–234 (1863).

    Google Scholar 

  27. Kaifu, Y. et al. Craniofacial morphology of Homo floresiensis: description, taxonomic affinities, and evolutionary implication. J. Hum. Evol. 61, 644–682 (2011).

    Article  PubMed  Google Scholar 

  28. Kaifu, Y. et al. Unique dental morphology of Homo floresiensis and its evolutionary implications. PLoS ONE 10, e0141614 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. van den Bergh, G. D. et al. Homo floresiensis-like fossils from the early Middle Pleistocene of Flores. Nature 534, 245–248 (2016).

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  31. Mondal, M. et al. Genomic analysis of Andamanese provides insights into ancient human migration into Asia and adaptation. Nat. Genet. 48, 1066–1070 (2016).

    Article  CAS  PubMed  Google Scholar 

  32. Skoglund, P., Mallick, S., Patterson, N. & Reich, D. No evidence for unknown archaic ancestry in South Asia. Nat. Genet. 50, 632–633 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Mondal, M., Casals, F., Majumder, P. P. & Bertranpetit, J. Reply to ‘No evidence for unknown archaic ancestry in South Asia’. Nat. Genet. 50, 1637–1639 (2018).

    Article  CAS  PubMed  Google Scholar 

  34. Skov, L. et al. Detecting archaic introgression using an unadmixed outgroup. PLoS Genet. 14, e1007641 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Lawson, D. J., Hellenthal, G., Myers, S. & Falush, D. Inference of population structure using dense haplotype data. PLoS Genet. 8, e1002453 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  37. Racimo, F. et al. Archaic adaptive introgression in TBX15/WARS2. Mol. Biol. Evol. 34, 509–524 (2017).

    CAS  PubMed  Google Scholar 

  38. Berger, L. R. et al. Homo naledi, a new species of the genus Homo from the Dinaledi Chamber, South Africa. eLife 4, e09560 (2015).

    Article  PubMed Central  Google Scholar 

  39. Key, F. M., Teixeira, J. C., de Filippo, C. & Andrés, A. M. Advantageous diversity maintained by balancing selection in humans. Curr. Opin. Genet. Dev. 29, 45–51 (2014).

    Article  CAS  PubMed  Google Scholar 

  40. Hubisz, M. J., Williams, A. L. & Siepel, A. Mapping gene flow between ancient hominins through demography-aware inference of the ancestral recombination graph. PLoS Genet. 16, e1008895 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Kelleher, J., Barton, N. H. & Etheridge, A. M. Coalescent simulation in continuous space. Bioinformatics 29, 955–956 (2013).

    Article  CAS  PubMed  Google Scholar 

  42. Malaspinas, A.-S. et al. A genomic history of Aboriginal Australia. Nature 538, 207–214 (2016).

    Article  CAS  PubMed  Google Scholar 

  43. Tucci, S. et al. Evolutionary history and adaptation of a human pygmy population of Flores Island, Indonesia. Science 361, 511–516 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Vernot, B. et al. Excavating Neandertal and Denisovan DNA from the genomes of Melanesian individuals. Science 352, 235–239 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Brumm, A. et al. Age and context of the oldest known hominin fossils from Flores. Nature 534, 249–253 (2016).

    Article  CAS  PubMed  Google Scholar 

  46. Ingicco, T. et al. Earliest known hominin activity in the Philippines by 709 thousand years ago. Nature 557, 233–237 (2018).

    Article  CAS  PubMed  Google Scholar 

  47. O’Connell, J. F. & Allen, J. The restaurant at the end of the universe: modelling the colonisation of Sahul. Aust. Archaeol. 74, 5–31 (2012).

    Article  Google Scholar 

  48. Kealy, S., Louys, J. & O’Connor, S. Islands under the sea: a review of early modern human dispersal routes and migration hypotheses through Wallacea. J. Isl. Coast. Archaeol. 11, 364–384 (2016).

    Article  Google Scholar 

  49. Kealy, S., Louys, J. & O’Connor, S. Reconstructing palaeogeography and inter-island visibility in the Wallacean Archipelago during the likely period of Sahul colonization, 65–45000 years ago. Archaeol. Prospect. 24, 259–272 (2017).

    Article  Google Scholar 

  50. Kealy, S., Louys, J. & O’Connor, S. Least-cost pathway models indicate northern human dispersal from Sunda to Sahul. J. Hum. Evol. 125, 59–70 (2018).

    Article  PubMed  Google Scholar 

  51. Bird, M. I. et al. Palaeogeography and voyage modeling indicates early human colonization of Australia was likely from Timor-Roti. Quat. Sci. Rev. 191, 431–439 (2018).

    Article  Google Scholar 

  52. Bird, M. I. et al. Early human settlement of Sahul was not an accident. Sci. Rep. 9, 8220 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

We thank C. Huber and J. Schmidt for useful discussions on the genetic analyses, and K. Mitchell and F. Racimo for comments on the manuscript. This work was supported by ARC Indigenous Discovery Grant IN180100017 (J.C.T. and R.T.) and ARC Laureate Fellowships FL100100195 (C.S.M.T.) and FL140100260 (A.C.). C.S. acknowledges funding from the Calleva Foundation and The Human Origins Research Fund. G.S.J. acknowledges support from a Presidential Postdoctoral Fellowship from Nanyang Technological University.

Author information

Author notes

  1. These authors contributed equally: Raymond Tobler, Chris S. M. Turney, Alan Cooper, Kristofer M. Helgen.

Authors and Affiliations

  1. Australian Centre for Ancient DNA, School of Biological Sciences, The University of Adelaide, Adelaide, South Australia, Australia

    João C. Teixeira, Gludhug A. Purnomo & Raymond Tobler

  2. ARC Centre of Excellence for Australian Biodiversity and Heritage (CABAH), The University of Adelaide, Adelaide, South Australia, Australia

    João C. Teixeira & Raymond Tobler

  3. Complexity Institute, Nanyang Technological University, Singapore, Singapore

    Guy S. Jacobs

  4. Department of Archaeology, University of Cambridge, Cambridge, UK

    Guy S. Jacobs

  5. Centre for Human Evolution Research, Department of Earth Sciences, Natural History Museum, London, UK

    Chris Stringer

  6. School of Mathematical Sciences, The University of Adelaide, Adelaide, South Australia, Australia

    Jonathan Tuke

  7. Statistics and Bioinformatics Group, School of Fundamental Sciences, Massey University, Palmerston North, New Zealand

    Georgi Hudjashov & Murray P. Cox

  8. Genome Diversity and Diseases Laboratory, Eijkman Institute for Molecular Biology, Jakarta, Indonesia

    Gludhug A. Purnomo & Herawati Sudoyo

  9. Department of Medical Biology, Faculty of Medicine, University of Indonesia, Jakarta, Indonesia

    Herawati Sudoyo

  10. Sydney Medical School, University of Sydney, Sydney, New South Wales, Australia

    Herawati Sudoyo

  11. Chronos 14Carbon-Cycle Facility, Earth and Sustainability Science Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales, Australia

    Chris S. M. Turney

  12. ARC Centre of Excellence for Australian Biodiversity and Heritage (CABAH), University of New South Wales, Sydney, New South Wales, Australia

    Chris S. M. Turney & Kristofer M. Helgen

  13. South Australian Museum, Adelaide, South Australia, Australia

    Alan Cooper

  14. BlueSky Genetics, Ashton, South Australia, Australia

    Alan Cooper

  15. Australian Museum Research Institute, Australian Museum, Sydney, New South Wales, Australia

    Kristofer M. Helgen

Authors
  1. João C. Teixeira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guy S. Jacobs
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chris Stringer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jonathan Tuke
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Georgi Hudjashov
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gludhug A. Purnomo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Herawati Sudoyo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Murray P. Cox
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Raymond Tobler
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Chris S. M. Turney
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Alan Cooper
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Kristofer M. Helgen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J.C.T., K.M.H., G.S.J., M.P.C., G.H., G.A.P. and J.T. designed the methods and undertook the analyses. J.C.T., K.M.H., R.T., G.S.J., H.S., A.C., C.S., C.S.M.T. and M.P.C. wrote the manuscript with input from all authors.

Corresponding author

Correspondence to João C. Teixeira.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Ecology & Evolution thanks Laurits Skov and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–15.

Reporting Summary

Supplementary Tables

Supplementary Tables 1–5.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Teixeira, J.C., Jacobs, G.S., Stringer, C. et al. Widespread Denisovan ancestry in Island Southeast Asia but no evidence of substantial super-archaic hominin admixture. Nat Ecol Evol 5, 616–624 (2021). https://doi.org/10.1038/s41559-021-01408-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-021-01408-0

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing