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Genome sequences of 36,000- to 37,000-year-old modern humans at Buran-Kaya III in Crimea

An Author Correction to this article was published on 22 January 2024

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Abstract

Populations genetically related to present-day Europeans first appeared in Europe at some point after 38,000–40,000 years ago, following a cold period of severe climatic disruption. These new migrants would eventually replace the pre-existing modern human ancestries in Europe, but initial interactions between these groups are unclear due to the lack of genomic evidence from the earliest periods of the migration. Here we describe the genomes of two 36,000–37,000-year-old individuals from Buran-Kaya III in Crimea as belonging to this newer migration. Both genomes share the highest similarity to Gravettian-associated individuals found several thousand years later in southwestern Europe. These genomes also revealed that the population turnover in Europe after 40,000 years ago was accompanied by admixture with pre-existing modern human populations. European ancestry before 40,000 years ago persisted not only at Buran-Kaya III but is also found in later Gravettian-associated populations of western Europe and Mesolithic Caucasus populations.

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Fig. 1: Genomic affinities between Buran-Kaya III and other ancient individuals.
Fig. 2: Relationships among individuals and genetic clusters of MUP Europe.
Fig. 3: Detection of Zlatý Kůň gene flow and Buran-Kaya III population modelling.
Fig. 4: Genomic affinity to CHG ancestry relative to the two Buran-Kaya III individuals and shared CHG/Zlatý Kůň-like ancestry.

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Data availability

Sequence data generated in this study are available through the EBI Sequence Read Archive PRJEB64496. The mitochondrial sequences are available through GenBank (accession number MK934322 and OR327029).

Code availability

No new code and sequence analysis methods were developed. Details on the analysis settings are provided in Methods section.

Change history

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Acknowledgements

The palaeogenomic facility of the Institut Jacques Monod obtained support from the University Paris Diderot within the programme ‘Actions de recherches structurantes’. The sequencing facility of the Institut Jacques Monod, Paris, is supported by grants from the University Paris Diderot, the Fondation pour la Recherche Médicale (DGE20111123014) and the Région Ile-de-France (11015901). Moreover, we acknowledge support from the French national research centre CNRS and EUR G.E.N.E. (ANR-17-EURE-0013; IdEx #ANR-18-IDEX-0001 l’Université de Paris; Programme d’Investissements d’Avenir) for supporting the PhD fellowship extension of O.P. We thank the National Academy of Sciences of Ukraine for permission to excavate at Buran-Kaya III and all the team members of the excavations. We also thank the French National Research Agency (ANR-05-JCJC-0240-01), the Fyssen Foundation, the Muséum national d’Histoire naturelle and the Centre National de la Recherche Scientifique (CNRS) for their financial support (excavations and anthropological analyses). We thank O. Gorgé for assistance with some of the sequencing.

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Contributions

E.-M.G., S. Prat and S. Péan initiated the project. E.-M.G. and T.G. supervised the study. E.A.B., E.-M.G. and T.G. produced data. O.P. and E.A.B. performed formal analyses. O.P., E.A.B., T.G. and E.-M.G. interpreted the data. S. Prat, S. Péan, L.C. and A.Y. provided samples and information to the archaeological context. E.A.B. wrote the paper with input from all authors.

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Correspondence to Thierry Grange or Eva-Maria Geigl.

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Extended data

Extended Data Fig. 1 Recalibration of comparative AMS 14C dates of Buran-Kaya III.

Buran-Kaya III (BuKa3) layers 6-1 and 6-2 with Upper Palaeolithic samples. All dates were calibrated using the software OxCal v4.4.4 based on the IntCal20 calibration data set. Climatic events are represented by the orange band, the Campanian Ignimbrite (CI) volcanic super-eruption event by the darker orange band, the Heinrich Event 4 by the lighter orange band.

Extended Data Fig. 2 Bayesian phylogenetic tree of mitochondrial sequences.

Excluding Hyper-Variable Regions, from Early and Mid-Upper Palaeolithic individuals including those from Buran-Kaya III (red). Posterior probability indicated at the nodes. Scale bar denotes substitutions per site. Sources for mitochondrial sequences are listed in Supplementary Table 3. Additional ancient and canonical N sequences are included to give branching details. Inset gives detailed mutation information from mtphyl v.5.003 (https://sites.google.com/site/mtphyl/home) for both BuKa3 individuals. References for mitochondrial sequences are given in Supplementary Table 11.

Extended Data Fig. 3 Neanderthal ancestry calculated for ancient individuals.

Neanderthal ancestry calculated using direct f4-ratio test78. α values calculated in the form of (Vindija33.19, Chimp; test, Mbuti)/(Vindija33.19, Chimp; Chagyrskaya, Mbuti). The error bars represent ±1 standard error, which were calculated using weighted block jackknife and a block size of 5 Mb.

Extended Data Fig. 4 Genetic affinities between Buran-Kaya III and present-day populations.

Heatmap showing the shared genetic drift calculated by f3-statistics in the form of f3(Mbuti; BuKa3, modern). Higher f3 values indicate greater allele sharing between Buran-Kaya III (BuKa3) and populations from the HGDP dataset. The left half of the circles shows f3 values tested with BuKa3C while the right side show those tested with BuKa3A. The map was created with ggmap76 using Stamen Design map tiles.

Extended Data Fig. 5 2D Multidimensional scaling (MDS).

MDS calculated using the pairwise genetic distance matrix coming from inverted f3 values (1-f3) in the form of f3(Mbuti; ancient1, ancient2), for the first three dimensions representing 8, 6 and 5% of the total variance. See also Supplementary Video 1 and Supplementary Fig. 2.

Extended Data Fig. 6 Summary of f4 statistics involving BuKa3 and pre-CI genomes.

A. Results of f4(Mbuti, pre-CI; BuKa3, pre-CI) B. Results of f4(Mbuti, BuKa3; pre-CI, pre-CI). Full results in Supplementary Table 5.

Extended Data Fig. 7 Modeling BuKa3 ancestry by qpGraph without admixture.

Best-fitting qpGraph models of BuKa3A (A) and BuKa3C (B) without admixture (compare with Fig. 3b). Buran-Kaya III individuals modeled with pre-LGM shotgun genomes using allsnps: NO parameters. The Z-score for the worst f4-statistic residuals is indicated.

Supplementary information

Supplementary Information

Supplementary Figs. 1–7 and Notes 1 and 2.

Reporting Summary

Peer Review File

Supplementary Tables

Supplementary Tables 1–11 in Excel file.

Supplementary Video 1

Animation of the 3D MDS scatterplot featured in Fig. 1c.

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Bennett, E.A., Parasayan, O., Prat, S. et al. Genome sequences of 36,000- to 37,000-year-old modern humans at Buran-Kaya III in Crimea. Nat Ecol Evol 7, 2160–2172 (2023). https://doi.org/10.1038/s41559-023-02211-9

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