Abstract

Aboriginal Australians represent one of the longest continuous cultural complexes known. Archaeological evidence indicates that Australia and New Guinea were initially settled approximately 50 thousand years ago (ka); however, little is known about the processes underlying the enormous linguistic and phenotypic diversity within Australia. Here we report 111 mitochondrial genomes (mitogenomes) from historical Aboriginal Australian hair samples, whose origins enable us to reconstruct Australian phylogeographic history before European settlement. Marked geographic patterns and deep splits across the major mitochondrial haplogroups imply that the settlement of Australia comprised a single, rapid migration along the east and west coasts that reached southern Australia by 49–45 ka. After continent-wide colonization, strong regional patterns developed and these have survived despite substantial climatic and cultural change during the late Pleistocene and Holocene epochs. Remarkably, we find evidence for the continuous presence of populations in discrete geographic areas dating back to around 50 ka, in agreement with the notable Aboriginal Australian cultural attachment to their country.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Accessions

Primary accessions

European Nucleotide Archive

References

  1. 1.

    , & Thermoluminescence dating of a 50,000-year-old human occupation site in northern Australia. Nature 345, 153–156 (1990)

  2. 2.

    & The process, biotic impact, and global implications of the human colonization of Sahul about 47,000 years ago. J. Archaeol. Sci. 56, 73–84 (2015)

  3. 3.

    , , , & Post-glacial sea-level changes around the Australian margin: a review. Quat. Sci. Rev. 74, 115–138 (2013)

  4. 4.

    & Peopling of Sahul: mtDNA variation in aboriginal Australian and Papua New Guinean populations. Am. J. Hum. Genet. 65, 808–828 (1999)

  5. 5.

    et al. An Aboriginal Australian genome reveals separate human dispersals into Asia. Science 334, 94–98 (2011)

  6. 6.

    . et al. A re-appraisal of the early Andean human remains from Lauricocha in Peru. PloS One. 10, e0127141 (2015)

  7. 7.

    et al. Deep roots for Aboriginal Australian Y chromosomes. Curr. Biol. 26, 809–813 (2016)

  8. 8.

    et al. Antiquity and diversity of aboriginal Australian Y-chromosomes. Am. J. Phys. Anthropol. 159, 367–381 (2016)

  9. 9.

    et al. Revealing the prehistoric settlement of Australia by Y chromosome and mtDNA analysis. Proc. Natl Acad. Sci. USA 104, 8726–8730 (2007)

  10. 10.

    Genetic evidence for the colonization of Australia. Quat. Int. 285, 44–56 (2013)

  11. 11.

    et al. Ancient mtDNA sequences from the First Australians revisited. Proc. Natl Acad. Sci. USA 113, 6892–6897 (2016)

  12. 12.

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

  13. 13.

    et al. Palaeoenvironmental change in tropical Australasia over the last 30,000 years—a synthesis by the OZ-INTIMATE group. Quat. Sci. Rev. 74, 97–114 (2013)

  14. 14.

    et al. Late Quaternary palaeoenvironmental change in the Australian drylands. Quat. Sci. Rev. 74, 78–96 (2013)

  15. 15.

    , , , & Holocene demographic changes and the emergence of complex societies in prehistoric Australia. PLoS One 10, e0128661 (2015)

  16. 16.

    ‘Complexity’ and the Australian continental narrative: themes in the archaeology of Holocene Australia. Quat. Int. 285, 182–192 (2013)

  17. 17.

    Native title in Australia: an ethnographic perspective. (Cambridge Univ. Press, 2003)

  18. 18.

    et al. A revised timescale for human evolution based on ancient mitochondrial genomes. Curr. Biol. 23, 553–559 (2013)

  19. 19.

    et al. IntCal13 and marine13 radiocarbon age calibration curves 0–50,000 years cal BP. Radiocarbon 55, 1869–1887 (2013)

  20. 20.

    in Sunda and Sahul: Prehistoric Studies in Southeast Asia, Melanesia and Australia (eds , & ) 205–246 (Academic Press, 1977)

  21. 21.

    , & Humans, water, and the colonization of Australia. Proc. Natl Acad. Sci. USA 113, 11477–11482 (2016)

  22. 22.

    , & Brief communication: the Australian Barrineans and their relationship to Southeast Asian negritos: an investigation using mitochondrial genomics. Hum. Biol. 85, 485–502 (2013)

  23. 23.

    & A Prehistory of Australia, New Guinea, and Sahul. (Academic Press, 1982)

  24. 24.

    et al. Cultural innovation and megafauna interaction in the early settlement of arid Australia. Nature 539, 280–283 (2016)

  25. 25.

    et al. Climate change not to blame for late Quaternary megafauna extinctions in Australia. Nat. Commun. 7, 10511 (2016)

  26. 26.

    et al. New ages for the last Australian megafauna: continent-wide extinction about 46,000 years ago. Science 292, 1888–1892 (2001)

  27. 27.

    et al. Synergistic roles of climate warming and human occupation in Patagonian megafaunal extinctions during the last deglaciation. Sci. Adv. 2, e1501682 (2016)

  28. 28.

    , , , & Human refugia in Australia during the Last Glacial Maximum and terminal Pleistocene: a geospatial analysis of the 25–12ka Australian archaeological record. J. Archaeol. Sci. 40, 4612–4625 (2013)

  29. 29.

    The Archaeology of Australia’s Deserts (Cambridge Univ. Press, 2013)

  30. 30.

    et al. Ancient mitochondrial DNA provides high-resolution time scale of the peopling of the Americas. Sci. Adv. 2, e1501385 (2016)

  31. 31.

    & BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214 (2007)

  32. 32.

    et al. Pleistocene mitochondrial genomes suggest a single major dispersal of non-Africans and a late glacial population turnover in Europe. Curr. Biol. 26, 827–833 (2016)

  33. 33.

    et al. Time-dependent rates of molecular evolution. Mol. Ecol. 20, 3087–3101 (2011)

  34. 34.

    & Inferences from tip-calibrated phylogenies: a review and a practical guide. Mol. Ecol. 25, 1911–1924 (2016)

  35. 35.

    , , , & Symbolic behaviour and the peopling of the southern arc route to Australia. Quat. Int. 202, 59–68 (2009)

  36. 36.

    & Paleontology. Did the Denisovans cross Wallace’s Line? Science 342, 321–323 (2013)

  37. 37.

    & Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb. Protoc. 2010, pdb.prot5448 (2010)

  38. 38.

    , & Generating barcoded libraries for multiplex high-throughput sequencing. Methods Mol. Biol. 840, 155–170 (2012)

  39. 39.

    , , , & Partial uracil-DNA-glycosylase treatment for screening of ancient DNA. Phil. Trans. R. Soc. Lond. B 370, 20130624 (2015)

  40. 40.

    et al. Characterization of ancient and modern genomes by SNP detection and phylogenomic and metagenomic analysis using PALEOMIX. Nat. Protocols 9, 1056–1082 (2014)

  41. 41.

    AdapterRemoval: easy cleaning of next-generation sequencing reads. BMC Res. Notes 5, 337 (2012)

  42. 42.

    et al. A “Copernican” reassessment of the human mitochondrial DNA tree from its root. Am. J. Hum. Genet. 90, 675–684 (2012)

  43. 43.

    & Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009)

  44. 44.

    , , , & mapDamage2.0: fast approximate Bayesian estimates of ancient DNA damage parameters. Bioinformatics 29, 1682–1684 (2013)

  45. 45.

    et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649 (2012)

  46. 46.

    & Updated comprehensive phylogenetic tree of global human mitochondrial DNA variation. Hum. Mutat. 30, E386–E394 (2009)

  47. 47.

    , , & Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012)

  48. 48.

    & mtDB: Human mitochondrial genome database, a resource for population genetics and medical sciences. Nucleic Acids Res. 34, D749–D751 (2006)

  49. 49.

    BLAT—the BLAST-like alignment tool. Genome Res. 12, 656–664 (2002)

  50. 50.

    , , , & Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol. Biol. 6, 29 (2006)

  51. 51.

    , & Smooth skyride through a rough skyline: Bayesian coalescent-based inference of population dynamics. Mol. Biol. Evol. 25, 1459–1471 (2008)

  52. 52.

    , , & Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88 (2006)

  53. 53.

    , & Population structure and eigenanalysis. PLoS Genet. 2, e190 (2006)

  54. 54.

    & in Encyclopedia of Measurement and Statistics (ed. ) 651–657 (Thousand Oaks, 2007)

  55. 55.

    Correspondence Analysis in Practice. (CRC Press, 2007)

  56. 56.

    , & FactoMineR: an R package for multivariate analysis. J. Stat. Softw. 25, 1–18 (2008)

  57. 57.

    Least squares quantization in PCM. IEEE Trans. Inf. Theory 28, 129–137 (1982)

  58. 58.

    & Clustering by means of medoids. Statistical Data Analysis Based on the L 1-Norm and Related Methods. First International Conference 405–416416 (1987)

  59. 59.

    Silhouettes: a graphical aid to the interpretation and validation of cluster analysis. J. Comput. Appl. Math. 20, 53–65 (1987)

  60. 60.

    , , , & Cluster Analysis Basics and Extensions. R package version 2.0.4. CRAN (2016)

  61. 61.

    R Development Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria (2013)

  62. 62.

    & Comparison of the Mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data. Mol. Ecol. Resour. 10, 831–844 (2010)

  63. 63.

    & Algorithm AS 89: The upper tail probabilities of Spearman’s Rho. Appl. Stat. 24, 377–379 (1975)

  64. 64.

    VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927–930 (2003)

  65. 65.

    et al. Early human occupation at Devil’s Lair, southwestern Australia 50,000 years ago. Quat. Res. 55, 3–13 (2001)

  66. 66.

    & Review of Devil’s Lair artefact classification and radiocarbon chronology. Aust. Archaeol. 43, 28–32 (1996)

  67. 67.

    Devil’s Lair, an example of prolonged cave use in South-Western Australia. World Archaeol. 10, 258–279 (1979)

  68. 68.

    & Recent and planned developments of the program OxCal. Radiocarbon 55, 720–730 (2013)

  69. 69.

    Dealing with outliers and offsets in radiocarbon dating. Radiocarbon 57, 1023–1045 (2009)

  70. 70.

    et al. SHCal13 Southern Hemisphere calibration, 0–50,000 years cal BP. Radiocarbon 55, 1889–1903 (2013)

  71. 71.

    , & New ΔR values for the southwest Pacific Ocean. Radiocarbon 46, 1005–1014 (2004)

  72. 72.

    , , , & Pre-bomb marine reservoir variability in the Kimberley region, Western Australia. Radiocarbon 52, 1158–1165 (2010)

  73. 73.

    Oceanic reservoir correction for marine radiocarbon dates from northwestern Australia. Aust. Archaeol. 20, 58–67 (1985)

  74. 74.

    et al. The human colonisation of Australia: optical dates of 53,000 and 60,000 years bracket human arrival at Deaf Adder Gorge, Northern Territory. Quat. Sci. Rev. 13, 575–583 (1994)

  75. 75.

    et al. Single-aliquot and single-grain optical dating confirm thermoluminescence age estimates at Malakunanja II rock shelter in northern Australia. Anc. TL 16, 19–24 (1998)

  76. 76.

    et al. Radiocarbon dating of organic- and carbonate-carbon in Genyornis and Dromaius eggshell using stepped combustion and stepped acidification. Quat. Sci. Rev. 22, 1805–1812 (2003)

  77. 77.

    , , & A 40,000 year-old human occupation site at Huon Peninsula, Papua New Guinea. Nature 324, 453–455 (1986)

  78. 78.

    Luminescence dating in archaeology: from origins to optical. Radiat. Meas. 27, 819–892 (1997)

Download references

Acknowledgements

We acknowledge the support and involvement of the Point Pearce, Cherbourg and Koonibba communities and the individual families. We also acknowledge the work of N. Tindale, J. Birdsell and members of the original Board for Archaeological Research expeditions collecting the specimens. We thank the South Australian Museum, Australian Research Council, University of Adelaide Environment Institute, the Genographic Project and Bioplatforms Australia for support, and S. Ulm, G. Gower, I. Mathieson, L. O’Brien, S. Easteal, M. Vilar, C. Stringer and ACAD colleagues for helpful comments and advice. The Aboriginal Heritage Project webpage is https://www.adelaide.edu.au/acad/ahp/, and this work was carried out under the auspices of the University of Adelaide Human Research Ethics Committee, project approval H-2014-252.

Author information

Author notes

    • Ray Tobler
    •  & Adam Rohrlach

    These authors contributed equally to this work.

    • Wolfgang Haak
    •  & Alan Cooper

    These authors jointly supervised this work.

Affiliations

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

    • Ray Tobler
    • , Julien Soubrier
    • , Pere Bover
    • , Bastien Llamas
    • , Matthew Williams
    • , Stephen M. Richards
    • , Wolfgang Haak
    •  & Alan Cooper
  2. School of Mathematical Sciences, The University of Adelaide, Adelaide, South Australia 5005, Australia

    • Adam Rohrlach
    • , Jonathan Tuke
    •  & Nigel Bean
  3. ARC Centre of Excellence for Mathematical and Statistical Frontiers, The University of Adelaide, Adelaide, South Australia 5005, Australia

    • Adam Rohrlach
    • , Jonathan Tuke
    •  & Nigel Bean
  4. Genetics and Molecular Pathology, SA Pathology, Adelaide, South Australia 5000, Australia

    • Julien Soubrier
  5. South Australian Museum, Adelaide, South Australia 5005, Australia

    • Ali Abdullah-Highfold
    • , Shane Agius
    • , Amy O’Donoghue
    • , Isabel O’Loughlin
    • , Peter Sutton
    • , Fran Zilio
    •  & Keryn Walshe
  6. School of Biological Sciences, The University of Adelaide, Adelaide, South Australia 5005, Australia

    • Peter Sutton
  7. Palaeontology, Geobiology and Earth Archives Research Centre, and Climate Change Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales 2052, Australia

    • Alan N. Williams
    •  & Chris S. M. Turney
  8. School of Archaeology and Anthropology, College of Arts and Social Sciences, Australian National University, Canberra, Australian Capital Territory 0200, Australia

    • Matthew Williams
  9. Department of Biochemistry and Genetics, La Trobe University, Melbourne, Victoria 3086, Australia

    • Robert J. Mitchell
  10. Alfred Deakin Institute, Deakin University, Melbourne, Victoria 3125, Australia

    • Emma Kowal
  11. Australian Genome Research Facility, The Waite Research Precinct, Adelaide, South Australia 5064, Australia

    • John R. Stephen
  12. Community Elder and Cultural Advisor, Cherbourg, Queensland, Australia

    • Lesley Williams
  13. Department of Archeogenetics, Max Planck Institute for the Science of Human History, 07745 Jena, Germany

    • Wolfgang Haak
  14. Environment Institute, The University of Adelaide, Adelaide, South Australia 5005, Australia

    • Alan Cooper

Authors

  1. Search for Ray Tobler in:

  2. Search for Adam Rohrlach in:

  3. Search for Julien Soubrier in:

  4. Search for Pere Bover in:

  5. Search for Bastien Llamas in:

  6. Search for Jonathan Tuke in:

  7. Search for Nigel Bean in:

  8. Search for Ali Abdullah-Highfold in:

  9. Search for Shane Agius in:

  10. Search for Amy O’Donoghue in:

  11. Search for Isabel O’Loughlin in:

  12. Search for Peter Sutton in:

  13. Search for Fran Zilio in:

  14. Search for Keryn Walshe in:

  15. Search for Alan N. Williams in:

  16. Search for Chris S. M. Turney in:

  17. Search for Matthew Williams in:

  18. Search for Stephen M. Richards in:

  19. Search for Robert J. Mitchell in:

  20. Search for Emma Kowal in:

  21. Search for John R. Stephen in:

  22. Search for Lesley Williams in:

  23. Search for Wolfgang Haak in:

  24. Search for Alan Cooper in:

Contributions

The project was conceived by A.C., W.H. and P.S. and directed by A.C. and W.H. Archival research and community outreach was led by I.O., A.A-H., S.A., A.O., F.Z. and L.W. with A.C., W.H., R.T. and R.J.M. The genetic sequencing was performed and coordinated by W.H., P.B., M.W., S.R. and J.R.S., and the genetic analysis by W.H., R.T., A.R., J.S., J.T., N.B., B.L. and A.C. Archaeological and anthropological interpretations were provided by P.S., C.T., A.N.W. and K.W. The manuscript was written by A.C. and R.T., with critical input from P.S., C.T., A.N.W., A.R., J.S., W.H. and all other co-authors. R.T., J.S., A.N.W. and A.R. compiled the Supplementary Information.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Alan Cooper.

Reviewer Information Nature thanks P. Bellwood, C. Lalueza-Fox and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Text, legends for Supplementary Tables 1-4 (see separate excel file) and additional references.

Excel files

  1. 1.

    Supplementary Tables

    This file contains Supplementary Tables 1-4 (see Supplementary Information file for legends).

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature21416

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.