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.

A weakly structured stem for human origins in Africa

A Publisher Correction to this article was published on 17 July 2023

This article has been updated

Abstract

Despite broad agreement that Homo sapiens originated in Africa, considerable uncertainty surrounds specific models of divergence and migration across the continent1. Progress is hampered by a shortage of fossil and genomic data, as well as variability in previous estimates of divergence times1. Here we seek to discriminate among such models by considering linkage disequilibrium and diversity-based statistics, optimized for rapid, complex demographic inference2. We infer detailed demographic models for populations across Africa, including eastern and western representatives, and newly sequenced whole genomes from 44 Nama (Khoe-San) individuals from southern Africa. We infer a reticulated African population history in which present-day population structure dates back to Marine Isotope Stage 5. The earliest population divergence among contemporary populations occurred 120,000 to 135,000 years ago and was preceded by links between two or more weakly differentiated ancestral Homo populations connected by gene flow over hundreds of thousands of years. Such weakly structured stem models explain patterns of polymorphism that had previously been attributed to contributions from archaic hominins in Africa2,3,4,5,6,7. In contrast to models with archaic introgression, we predict that fossil remains from coexisting ancestral populations should be genetically and morphologically similar, and that only an inferred 1–4% of genetic differentiation among contemporary human populations can be attributed to genetic drift between stem populations. We show that model misspecification explains the variation in previous estimates of divergence times, and argue that studying a range of models is key to making robust inferences about deep history.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Fig. 1: Proposed conceptual models of early human history in Africa.
Fig. 2: Genetic diversity across Africa.
Fig. 3: A weakly structured stem best describes two-locus statistics.
Fig. 4: Structure among stems is weak and present-day structure is generally recent.
Fig. 5: Model validation using independent statistics.

Data availability

Nama sequencing data are available from the European Genome-Phenome Archive (EGA), accession number EGAD00001006198. Data access is permitted for non-commercial, population origins or ancestry research upon application to the South African Data Access Committee with appropriate institutional review board approval. The African Diversity Reference Panel can be found at accession EGAS00001000960.

Code availability

Code for the software used in this paper is found at the following locations: moments-LD (https://bitbucket.org/simongravel/moments), Demes (https://github.com/popsim-consortium/demes-python), Relate (https://myersgroup.github.io/relate/), msprime (https://github.com/tskit-dev/msprime) and tskit (https://github.com/tskit-dev/tskit).

Change history

References

  1. Henn, B. M., Steele, T. E. & Weaver, T. D. Clarifying distinct models of modern human origins in Africa. Curr. Opin. Genet. Dev. 53, 148–156 (2018).

    Article  CAS  PubMed  Google Scholar 

  2. Ragsdale, A. P. & Gravel, S. Models of archaic admixture and recent history from two-locus statistics. PLoS Genet. 15, e1008204 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Plagnol, V. & Wall, J. D. Possible ancestral structure in human populations. PLoS Genet. 2, e105 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  4. Hammer, M. F., Woerner, A. E., Mendez, F. L., Watkins, J. C. & Wall, J. D. Genetic evidence for archaic admixture in Africa. Proc. Natl Acad. Sci. USA 108, 15123–15128 (2011).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  5. Hey, J. et al. Phylogeny estimation by integration over isolation with migration models. Mol. Biol. Evol. 35, 2805–2818 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Lorente-Galdos, B. et al. Whole-genome sequence analysis of a pan African set of samples reveals archaic gene flow from an extinct basal population of modern humans into sub-Saharan populations. Genome Biol. 20, 77 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  7. Durvasula, A. & Sankararaman, S. Recovering signals of ghost archaic introgression in African populations. Sci. Adv. 6, eaax5097 (2020).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  8. Hublin, J.-J. et al. New fossils from Jebel Irhoud, Morocco and the pan-African origin of Homo sapiens. Nature 546, 289–292 (2017).

    Article  ADS  CAS  PubMed  Google Scholar 

  9. White, T. D. et al. Pleistocene Homo sapiens from Middle Awash, Ethiopia. Nature 423, 742–747 (2003).

    Article  ADS  CAS  PubMed  Google Scholar 

  10. Deacon, H. J. Two Late Pleistocene-Holocene archaeological depositories from the Southern Cape, South Africa. S. Afr. Archaeol. Bull. 50, 121–131 (1995).

    Article  Google Scholar 

  11. Stringer, C. The origin and evolution of Homo sapiens. Phil. Trans. R. Soc. B 371, 20150237 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Scerri, E. M. L. et al. Did our species evolve in subdivided populations across Africa, and why does it matter? Trends Ecol. Evol. 33, 582–594 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Scerri, E. M. L., Chikhi, L. & Thomas, M. G. Beyond multiregional and simple out-of-Africa models of human evolution. Nat. Ecol. Evol. 3, 1370–1372 (2019).

    Article  PubMed  Google Scholar 

  14. Arredondo, A. et al. Inferring number of populations and changes in connectivity under the n-island model. Heredity 126, 896–912 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  15. Kamm, J., Terhorst, J., Durbin, R. & Song, Y. S. Efficiently inferring the demographic history of many populations with allele count data. J. Am. Stat. Assoc. 115, 1472–1487 (2020).

    Article  MathSciNet  CAS  PubMed  MATH  Google Scholar 

  16. Speidel, L., Forest, M., Shi, S. & Myers, S. R. A method for genome-wide genealogy estimation for thousands of samples. Nat. Genet. 51, 1321–1329 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Hsieh, P. et al. Model-based analyses of whole-genome data reveal a complex evolutionary history involving archaic introgression in Central African Pygmies. Genome Res. 26, 291–300 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. The 1000 Genomes Project Consortium. A global reference for human genetic variation. Nature 526, 68–74 (2015).

    Article  Google Scholar 

  19. Lipson, M. et al. Ancient DNA and deep population structure in sub-Saharan African foragers. Nature 603, 290–296 (2022).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  20. Gurdasani, D. et al. The African Genome Variation Project shapes medical genetics in Africa. Nature 517, 327–332 (2015).

    Article  ADS  CAS  PubMed  Google Scholar 

  21. Gopalan, S. et al. Hunter-gatherer genomes reveal diverse demographic trajectories during the rise of farming in Eastern Africa. Curr. Biol. 32, 1852–1860 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Pagani, L. et al. Tracing the route of modern humans out of Africa by using 225 human genome sequences from Ethiopians and Egyptians. Am. J. Hum. Genet. 96, 986–991 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Prüfer, K. et al. A high-coverage Neandertal genome from Vindija Cave in Croatia. Science 358, 655–658 (2017).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  24. Ragsdale, A. P. & Gravel, S. Unbiased estimation of linkage disequilibrium from unphased data. Mol. Biol. Evol. 37, 923–932 (2020).

    Article  CAS  PubMed  Google Scholar 

  25. Bergström, A., Stringer, C., Hajdinjak, M., Scerri, E. M. L. & Skoglund, P. Origins of modern human ancestry. Nature 590, 229–237 (2021).

    Article  ADS  PubMed  Google Scholar 

  26. Molinaro, L. et al. West Asian sources of the Eurasian component in Ethiopians: a reassessment. Sci. Rep. 9, 18811 (2019).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  27. Henn, B. M. et al. Y-chromosomal evidence of a pastoralist migration through Tanzania to southern Africa. Proc. Natl Acad. Sci. USA 105, 10693–10698 (2008).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  28. Breton, G. et al. Lactase persistence alleles reveal partial East African ancestry of southern African Khoe pastoralists. Curr. Biol. 24, 852–858 (2014).

    Article  CAS  PubMed  Google Scholar 

  29. Li, H. & Durbin, R. Inference of human population history from individual whole-genome sequences. Nature 475, 493–496 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Mazet, O., Rodríguez, W., Grusea, S., Boitard, S. & Chikhi, L. On the importance of being structured: instantaneous coalescence rates and human evolution—lessons for ancestral population size inference? Heredity 116, 362–371 (2016).

    Article  CAS  PubMed  Google Scholar 

  31. Momigliano, P., Florin, A.-B. & Merilä, J. Biases in demographic modeling affect our understanding of recent divergence. Mol. Biol. Evol. 38, 2967–2985 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Shchur, V., Brandt, D. Y. C., Ilina, A. & Nielsen, R. Estimating population split times and migration rates from historical effective population sizes. Preprint at https://www.biorxiv.org/content/10.1101/2022.06.17.496540v1 (2022).

  33. Blome, M. W., Cohen, A. S., Tryon, C. A., Brooks, A. S. & Russell, J. The environmental context for the origins of modern human diversity: a synthesis of regional variability in African climate 150,000–30,000 years ago. J. Hum. Evol. 62, 563–592 (2012).

    Article  PubMed  Google Scholar 

  34. Marean, C. W. et al. in Fynbos (ed. Allsopp, N.) Ch. 8 (Oxford Univ. Press, 2014).

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

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  36. Groucutt, H. S. et al. Rethinking the dispersal of Homo sapiens out of Africa. Evol. Anthropol. 24, 149–164 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  37. Prüfer, K. et al. A genome sequence from a modern human skull over 45,000 years old from Zlatý kůň in Czechia. Nat. Ecol. Evol. 5, 820–825 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Beyer, R. M., Krapp, M., Eriksson, A. & Manica, A. Climatic windows for human migration out of Africa in the past 300,000 years. Nat. Commun. 12, 4889 (2021).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  39. Wall, J. D., Ratan, A., Stawiski, E. & GenomeAsia 100K Consortium. Identification of African-specific admixture between modern and archaic humans. Am. J. Hum. Genet. 105, 1254–1261 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Grün, R. et al. Dating the skull from Broken Hill, Zambia, and its position in human evolution. Nature 580, 372–375 (2020).

    Article  ADS  PubMed  Google Scholar 

  41. Petr, M., Pääbo, S., Kelso, J. & Vernot, B. Limits of long-term selection against Neandertal introgression. Proc. Natl Acad. Sci. USA 116, 1639–1644 (2019).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  42. Zhang, X. et al. The history and evolution of the Denisovan-EPAS1 haplotype in Tibetans. Proc. Natl Acad. Sci. USA 118, e2020803118 (2021).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  43. Schrider, D. R. & Kern, A. D. Soft sweeps are the dominant mode of adaptation in the human genome. Mol. Biol. Evol. 34, 1863–1877 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Relethford, J. H. Craniometric variation among modern human populations. Am. J. Biol. Anthropol. 95, 53–62 (1994).

    Article  CAS  Google Scholar 

  45. Weaver, T. D., Roseman, C. C. & Stringer, C. B. Close correspondence between quantitative- and molecular-genetic divergence times for Neandertals and modern humans. Proc. Natl Acad. Sci. USA 105, 4645–4649 (2008).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  46. von Cramon-Taubadel, N. Congruence of individual cranial bone morphology and neutral molecular affinity patterns in modern humans. Am. J. Phys. Anthropol. 140, 205–215 (2009).

    Article  Google Scholar 

  47. Harvati, K. et al. The Later Stone Age calvaria from Iwo Eleru, Nigeria: morphology and chronology. PLoS ONE 6, e24024 (2011).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  48. Crevecoeur, I., Brooks, A., Ribot, I., Cornelissen, E. & Semal, P. Late Stone Age human remains from Ishango (Democratic Republic of Congo): new insights on Late Pleistocene modern human diversity in Africa. J. Hum. Evol. 96, 35–57 (2016).

    Article  CAS  PubMed  Google Scholar 

  49. Crevecoeur, I. in Modern Origins: A North African Perspective (eds. Hublin, J. J. & McPherron, S. P.) 205–219 (Springer, 2012).

  50. Day, M. H. Early Homo sapiens remains from the Omo River region of South-west Ethiopia: Omo human skeletal remains. Nature 222, 1135–1138 (1969).

    Article  ADS  CAS  PubMed  Google Scholar 

  51. Vidal, C. M. et al. Age of the oldest known Homo sapiens from eastern Africa. Nature 601, 579–583 (2022).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  52. Richter, D. et al. The age of the hominin fossils from Jebel Irhoud, Morocco, and the origins of the Middle Stone Age. Nature 546, 293–296 (2017).

    Article  ADS  CAS  PubMed  Google Scholar 

  53. 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  PubMed Central  Google Scholar 

  54. Dirks, P. H. et al.The age of Homo naledi and associated sediments in the Rising Star Cave, South Africa.eLife 6, e24231 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  55. Kelleher, J., Etheridge, A. M. & McVean, G. Efficient coalescent simulation and genealogical analysis for large sample sizes. PLoS Comput. Biol. 12, e1004842 (2016).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  56. Baumdicker, F. et al. Efficient ancestry and mutation simulation with msprime 1.0. Genetics 220, iyab229 (2022).

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank participants for the DNA contributions that enabled this study; in particular, we wish to highlight the generous participation of the Richtersveld Nama community in South Africa and help from local research assistants W. De Klerk and H. Kaimann. Additional assistance and community engagement was conducted by J. Myrick, C. Gignoux, C. Uren and C. Werely. We thank the African Genome Diversity Project for data generation, including T. Carensten, D. Gurdasani and M. Sandhu; L. Anderson-Trocmé and G. Femerling for assistance in creating the map in Fig. 2 and Supplementary Fig. 2, respectively; and N. M. Morales-Garcia for data visualization discussion and designing Figs. 1 and 3. This research was supported by CIHR project grant 437576, Natural Sciences and Engineering Research Council of Canada (NSERC) grant RGPIN-2017-04816, the Canada Research Chair program to S.G. and the Canada Foundation for Innovation, and an NIH grant R35GM133531 to B.M.H.; and E.G.A. was supported by NIH K01 MH121659 and K12 GM102778. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. M.M. and E.H. acknowledge the support of the DSI-NRF Centre of Excellence for Biomedical Tuberculosis Research, the South African Medical Research Council Centre for Tuberculosis Research, and the Division of Molecular Biology and Human Genetics at Stellenbosch University, Cape Town, South Africa.

Author information

Authors and Affiliations

Authors

Contributions

A.P.R., B.M.H. and S.G. designed the study. B.M.H., E.H. and M.M. designed recruitment protocols and recruited participants. B.M.H. and E.G.A. performed data quality control. A.P.R., B.M.H. and S.G. designed the statistical analyses. A.P.R. conducted the statistical analyses. A.P.R., T.D.W., B.M.H. and S.G. interpreted the results and wrote the first draft of the article. All authors read and edited the paper.

Corresponding authors

Correspondence to Brenna M. Henn or Simon Gravel.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature thanks Marta Mirazon Lahr and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

Additional information

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

Supplementary information

Supplementary Information

This file contains further discussion, methods and data, Supplementary Tables S1–S8, Supplementary Figs. S1–S40, and Supplementary References.

Reporting Summary

Peer Review File

Supplementary Data

This zipped file contains inferred demographic models in Demes format for all models presented in the main text and all alternative models used in validation of our main results that are discussed in the Supplementary Information.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ragsdale, A.P., Weaver, T.D., Atkinson, E.G. et al. A weakly structured stem for human origins in Africa. Nature 617, 755–763 (2023). https://doi.org/10.1038/s41586-023-06055-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41586-023-06055-y

This article is cited by

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.

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