Northeastern Siberia has been inhabited by humans for more than 40,000 years but its deep population history remains poorly understood. Here we investigate the late Pleistocene population history of northeastern Siberia through analyses of 34 newly recovered ancient genomes that date to between 31,000 and 600 years ago. We document complex population dynamics during this period, including at least three major migration events: an initial peopling by a previously unknown Palaeolithic population of ‘Ancient North Siberians’ who are distantly related to early West Eurasian hunter-gatherers; the arrival of East Asian-related peoples, which gave rise to ‘Ancient Palaeo-Siberians’ who are closely related to contemporary communities from far-northeastern Siberia (such as the Koryaks), as well as Native Americans; and a Holocene migration of other East Asian-related peoples, who we name ‘Neo-Siberians’, and from whom many contemporary Siberians are descended. Each of these population expansions largely replaced the earlier inhabitants, and ultimately generated the mosaic genetic make-up of contemporary peoples who inhabit a vast area across northern Eurasia and the Americas.
This is a preview of subscription content
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.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Source code with functions for calculating f-statistics is available as an R package at GitHub (https://github.com/martinsikora/admixr)
Fedorova, S. A. et al. Autosomal and uniparental portraits of the native populations of Sakha (Yakutia): implications for the peopling of Northeast Eurasia. BMC Evol. Biol. 13, 127 (2013).
Pugach, I. et al. The complex admixture history and recent southern origins of Siberian populations. Mol. Biol. Evol. 33, 1777–1795 (2016).
Wong, E. H. M. et al. Reconstructing genetic history of Siberian and Northeastern European populations. Genome Res. 27, 1–14 (2017).
Pitulko, V. V. et al. The Yana RHS site: humans in the Arctic before the last glacial maximum. Science 303, 52–56 (2004).
Pitulko, V. V., Nikolskiy, P. A., Basilyan, A. & Pavlova, E. Y. in Paleoamerican Odyssey (eds Graf, K. E. et al.) Ch. 2, 13–44 (Texas A&M Univ. Press, 2014).
Pitulko, V. V. et al. Early human presence in the Arctic: evidence from 45,000-year-old mammoth remains. Science 351, 260–263 (2016).
Pitulko, V., Pavlova, E. & Nikolskiy, P. Revising the archaeological record of the Upper Pleistocene Arctic Siberia: human dispersal and adaptations in MIS 3 and 2. Quat. Sci. Rev. 165, 127–148 (2017).
Rasmussen, S. O. et al. A stratigraphic framework for abrupt climatic changes during the Last Glacial period based on three synchronized Greenland ice-core records: refining and extending the INTIMATE event stratigraphy. Quat. Sci. Rev. 106, 14–28 (2014).
Derevi͡anko, A. P., Powers, W. R. & Shimkin, D. B. The Paleolithic of Siberia: New Discoveries and Interpretations (Institute of Archaeology and Ethnography, Siberian Division, Russian Academy of Sciences, 1998).
Pitulko, V. V. & Nikolskiy, P. A. The extinction of the woolly mammoth and the archaeological record in Northeastern Asia. World Archaeol. 44, 21–42 (2012).
Siska, V. et al. Genome-wide data from two early Neolithic East Asian individuals dating to 7700 years ago. Sci. Adv. 3, e1601877 (2017).
Dulik, M. C. et al. Y-chromosome analysis reveals genetic divergence and new founding native lineages in Athapaskan- and Eskimoan-speaking populations. Proc. Natl Acad. Sci. USA 109, 8471–8476 (2012).
Poznik, G. D. et al. Punctuated bursts in human male demography inferred from 1,244 worldwide Y-chromosome sequences. Nat. Genet. 48, 593–599 (2016).
Sikora, M. et al. Ancient genomes show social and reproductive behavior of early Upper Paleolithic foragers. Science 358, 659–662 (2017).
Fu, Q. et al. DNA analysis of an early modern human from Tianyuan Cave, China. Proc. Natl Acad. Sci. USA 110, 2223–2227 (2013).
Fu, Q. et al. The genetic history of Ice Age Europe. Nature 534, 200–205 (2016).
Posth, C. 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).
Raghavan, M. et al. Upper Palaeolithic Siberian genome reveals dual ancestry of Native Americans. Nature 505, 87–91 (2014).
Lipson, M. & Reich, D. A working model of the deep relationships of diverse modern human genetic lineages outside of Africa. Mol. Biol. Evol. 34, 889–902 (2017).
Yang, M. A. et al. 40,000-year-old individual from Asia provides insight into early population structure in Eurasia. Curr. Biol. 27, 3202–3208.e9 (2017).
Moreno-Mayar, J. V. et al. Terminal Pleistocene Alaskan genome reveals first founding population of Native Americans. Nature 553, 203–207 (2018).
Hoffecker, J. F., Elias, S. A., O’Rourke, D. H., Scott, G. R. & Bigelow, N. H. Beringia and the global dispersal of modern humans. Evol. Anthropol. 25, 64–78 (2016).
Rasmussen, M. et al. Ancient human genome sequence of an extinct Palaeo-Eskimo. Nature 463, 757–762 (2010).
Reich, D. et al. Reconstructing Native American population history. Nature 488, 370–374 (2012).
Loh, P.-R. et al. Inferring admixture histories of human populations using linkage disequilibrium. Genetics 193, 1233–1254 (2013).
Flegontov, P. et al. Genomic study of the Ket: a Paleo-Eskimo-related ethnic group with significant ancient North Eurasian ancestry. Sci. Rep. 6, 20768 (2016).
Flegontov, P. et al. Paleo-Eskimo genetic legacy across North America. Preprint at https://www.biorxiv.org/content/10.1101/203018v1 (2017).
Damgaard, P. de B. et al. The first horse herders and the impact of early Bronze Age steppe expansions into Asia. Science 360, eaar7711 (2018).
Pitulko, V. V., Pavlova, E. Y., Nikolskiy, P. A. & Ivanova, V. V. The oldest art of the Eurasian Arctic: personal ornaments and symbolic objects from Yana RHS, Arctic Siberia. Antiquity 86, 642–659 (2012).
Skoglund, P. et al. Genetic evidence for two founding populations of the Americas. Nature 525, 104–108 (2015).
Raghavan, M. et al. Genomic evidence for the Pleistocene and recent population history of Native Americans. Science 349, aab3884 (2015).
Moreno-Mayar, J. V. et al. Early human dispersals within the Americas. Science 362, eaav2621 (2018).
Dulik, M. C. et al. Mitochondrial DNA and Y chromosome variation provides evidence for a recent common ancestry between Native Americans and Indigenous Altaians. Am. J. Hum. Genet. 90, 229–246 (2012).
Malaspinas, A.-S. et al. A genomic history of Aboriginal Australia. Nature 538, 207–214 (2016).
Allentoft, M. E. et al. Population genomics of Bronze Age Eurasia. Nature 522, 167–172 (2015).
Damgaard, P. B. et al. Improving access to endogenous DNA in ancient bones and teeth. Sci. Rep. 5, 11184 (2015).
Orlando, L. et al. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature 499, 74–78 (2013).
Dabney, J. & Meyer, M. Length and GC-biases during sequencing library amplification: a comparison of various polymerase-buffer systems with ancient and modern DNA sequencing libraries. Biotechniques 52, 87–94 (2012).
Schubert, M., Lindgreen, S. & Orlando, L. AdapterRemoval v2: rapid adapter trimming, identification, and read merging. BMC Res. Notes 9, 88 (2016).
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
Schubert, M. et al. Improving ancient DNA read mapping against modern reference genomes. BMC Genomics 13, 178 (2012).
DePristo, M. A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491–498 (2011).
Jónsson, H., Ginolhac, A., Schubert, M., Johnson, P. L. F. & Orlando, L. mapDamage2.0: fast approximate Bayesian estimates of ancient DNA damage parameters. Bioinformatics 29, 1682–1684 (2013).
Renaud, G., Slon, V., Duggan, A. T. & Kelso, J. Schmutzi: estimation of contamination and endogenous mitochondrial consensus calling for ancient DNA. Genome Biol. 16, 224 (2015).
Korneliussen, T. S., Albrechtsen, A. & Nielsen, R. ANGSD: analysis of next generation sequencing data. BMC Bioinformatics 15, 356 (2014).
Weissensteiner, H. et al. HaploGrep 2: mitochondrial haplogroup classification in the era of high-throughput sequencing. Nucleic Acids Res. 44, W58–W63 (2016).
Li, H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27, 2987–2993 (2011).
Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
Meyer, M. et al. A high-coverage genome sequence from an archaic Denisovan individual. Science 338, 222–226 (2012).
Lazaridis, I. et al. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513, 409–413 (2014).
Rasmussen, M. et al. The genome of a Late Pleistocene human from a Clovis burial site in western Montana. Nature 506, 225–229 (2014).
Raghavan, M. et al. The genetic prehistory of the New World Arctic. Science 345, 1255832 (2014).
Prüfer, K. et al. The complete genome sequence of a Neanderthal from the Altai Mountains. Nature 505, 43–49 (2014).
Fu, Q. et al. Genome sequence of a 45,000-year-old modern human from western Siberia. Nature 514, 445–449 (2014).
Seguin-Orlando, A. et al. Genomic structure in Europeans dating back at least 36,200 years. Science 346, 1113–1118 (2014).
Olalde, I. et al. Derived immune and ancestral pigmentation alleles in a 7,000-year-old Mesolithic European. Nature 507, 225–228 (2014).
Gamba, C. et al. Genome flux and stasis in a five millennium transect of European prehistory. Nat. Commun. 5, 5257 (2014).
Rasmussen, M. et al. The ancestry and affiliations of Kennewick Man. Nature 523, 455–458 (2015).
Gallego Llorente, M. et al. Ancient Ethiopian genome reveals extensive Eurasian admixture throughout the African continent. Science 350, 820–822 (2015).
Ayub, Q. et al. The Kalash genetic isolate: ancient divergence, drift, and selection. Am. J. Hum. Genet. 96, 775–783 (2015).
Fu, Q. et al. An early modern human from Romania with a recent Neanderthal ancestor. Nature 524, 216–219 (2015).
Jones, E. R. et al. Upper Palaeolithic genomes reveal deep roots of modern Eurasians. Nat. Commun. 6, 8912 (2015).
Broushaki, F. et al. Early Neolithic genomes from the eastern Fertile Crescent. Science 353, 499–503 (2016).
Mondal, M. et al. Genomic analysis of Andamanese provides insights into ancient human migration into Asia and adaptation. Nat. Genet. 48, 1066–1070 (2016).
Kılınç, G. M. et al. The demographic development of the first farmers in Anatolia. Curr. Biol. 26, 2659–2666 (2016).
Jeong, C. et al. Long-term genetic stability and a high-altitude East Asian origin for the peoples of the high valleys of the Himalayan arc. Proc. Natl Acad. Sci. USA 113, 7485–7490 (2016).
Hofmanová, Z. et al. Early farmers from across Europe directly descended from Neolithic Aegeans. Proc. Natl Acad. Sci. USA 113, 6886–6891 (2016).
Mallick, S. et al. The Simons Genome Diversity Project: 300 genomes from 142 diverse populations. Nature 538, 201–206 (2016).
Jones, E. R. et al. The Neolithic transition in the Baltic was not driven by admixture with early European farmers. Curr. Biol. 27, 576–582 (2017).
Mathieson, I. et al. Genome-wide patterns of selection in 230 ancient Eurasians. Nature 528, 499–503 (2015).
Patterson, N., Price, A. L. & Reich, D. Population structure and eigenanalysis. PLoS Genet. 2, e190 (2006).
Patterson, N. et al. Ancient admixture in human history. Genetics 192, 1065–1093 (2012).
Manichaikul, A. et al. Robust relationship inference in genome-wide association studies. Bioinformatics 26, 2867–2873 (2010).
Browning, B. L. & Browning, S. R. Detecting identity by descent and estimating genotype error rates in sequence data. Am. J. Hum. Genet. 93, 840–851 (2013).
Kelleher, J., Etheridge, A. M. & McVean, G. Efficient coalescent simulation and genealogical analysis for large sample sizes. PLoS Comput. Biol. 12, e1004842 (2016).
Excoffier, L., Dupanloup, I., Huerta-Sánchez, E., Sousa, V. C. & Foll, M. Robust demographic inference from genomic and SNP data. PLoS Genet. 9, e1003905 (2013).
Scally, A. The mutation rate in human evolution and demographic inference. Curr. Opin. Genet. Dev. 41, 36–43 (2016).
Fenner, J. N. Cross-cultural estimation of the human generation interval for use in genetics-based population divergence studies. Am. J. Phys. Anthropol. 128, 415–423 (2005).
Lawson, D. J., Hellenthal, G., Myers, S. & Falush, D. Inference of population structure using dense haplotype data. PLoS Genet. 8, e1002453 (2012).
Delaneau, O., Zagury, J.-F. & Marchini, J. Improved whole-chromosome phasing for disease and population genetic studies. Nat. Methods 10, 5–6 (2013).
Hellenthal, G. et al. A genetic atlas of human admixture history. Science 343, 747–751 (2014).
Akimova, E. et al. A new direct radiocarbon AMS date for an Upper Palaeolithic human bone from Siberia. Archaeometry 52, 1122–1130 (2010).
Alekseev, V. P. in The Palaeolithic in Siberia (ed. Derev’anko, A. P.) 329–33 (Univ. of Illinois Press, 1998).
Chikisheva, T. et al. An Upper Paleolithic human mandible and a first cervical vertebra from Afontova Gora II. Archaeol., Ethnol. Anthropol. Eurasia 44, 150–157 (2016).
Khaldeyeva, N. et al. An Upper Paleolithic mandible from Listvenka, Siberia: a revision. Archaeol., Ethnol. Anthropol. Eurasia 44, 147–156 (2016).
Pitulko, V. V., Ivanova, V. V., Kasparov, A. K. & Pavlova, E. Y. Reconstructing prey selection, hunting strategy and seasonality of the early Holocene frozen site in the Siberian High Arctic: a case study on the Zhokhov site faunal remains, De Long Islands. Environ. Archaeol. 20, 120–157 (2015).
Zubova, A. V. & Chikisheva, T. A. The morphology of human teeth from Afontova Gora II, Southern Siberia, and their status relative to the dentition of other Upper Paleolithic Northern Eurasians. Archaeol., Ethnol. Anthropol. Eurasia 43, 135–143 (2015).
Zubova, A. V. Chikisheva, T. A. & Shunkov, M. V. The morphology of permanent molars from the Paleolithic layers of Denisova Cave. Archaeol., Ethnol. Anthropol. Eurasia 45, 121–134 (2017).
Reich, D. et al. Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468, 1053–1060 (2010).
Hubberten, H. W. et al. The periglacial climate and environment in northern Eurasia during the Last Glaciation. Quat. Sci. Rev. 23, 1333–1357 (2004).
Svendsen, J. I. Late Quaternary ice sheet history of northern Eurasia. Quat. Sci. Rev. 23, 1229–1271 (2004).
Pitulko, V. V. et al. Landscape–climatic changes in Yana Palaeolithic site area on western part of Yana–Indighirka lowland during late Pleistocene–Holocene. Bull. North-East Sci. Center Russ. Acad. Sci. Far East Branch 1, 16–29 (2013).
We thank F. Shidlovskiy (Ice Age Museum, Moscow) for providing access to the Kolyma1 sample. E.W., D.J.M. and M.S. thank St. John’s College (Cambridge University) for providing a congenial environment for scientific discussions. This work was supported by the Lundbeck Foundation, the Danish National Research Foundation, KU2016, the Novo Nordisk Foundation and the Wellcome Trust (GeoGenetics). I.D. and V.C.S. were supported by Swiss NSF grants 310030B-166605 and 31003A-143393 to L.E., and V.C.S. was further supported by Portuguese FCT (UID/BIA/00329/2013). V.V.P., E.Y.P. and P.A.N. are supported by Russian Science Foundation project N 16-18-10265-RNF. P.A.N. is supported by the Federal research program no. 0135-2016-0024. V.V.P., E.Y.P. and V.G.C thank the Rock Foundation of New York, USA for long-term support of the Yana research. D.J.M. is supported by the Quest Archaeological Research Program. P.S.G., A.I.L. and B.A.M. are funded by RFBR (19-09-00144). A.Y.F. was supported by the IAET SB RAS project no. 0329-2019-0001. R.M. was supported by an EMBO Long-Term Fellowship (ALTF 133-2017) and R.D. by Wellcome grant WT207492. M. Peyrot is supported by an ERC starting grant ERC-2017-STG 758855. S.R. was supported by the Novo Nordisk Foundation (NNF14CC0001). Q.F. was supported by NSFC (91731303, 41672021, 41630102). V.I.K. and V.M. are funded by RFBR (18-09-00349), A.S. thanks Medicinska understödsföreningen Liv och Hälsa r.f. and the Finnish Society of Sciences and Letters for financial support. M.E.A. was funded by the Villum Foundation (Young Investigator, grant no. 10120). M.M.L. was supported by an ERC advanced grant (no. 295907).
Nature thanks Pontus Skoglund 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
Extended Data Fig. 1 Geographical, chronological and archaeological context for the earliest human remains discovered in northern Siberia.
a, Map of known 14C-dated anatomically modern human fossils of late Pleistocene and early Holocene age (yellow dots) found in Siberia54,82,83,84,85,86,87. Yellow star, Yana RHS site; red triangle, Denisova Cave, which has yielded Neanderthal and Denisovan remains88,89; white line, reconstructed maximum ice sheet extent at about 60 ka; blue filling, ice sheet extent during the LGM, around 20 ka (refs 90,91); potentially glaciated areas are cross-hatched. b, General view of the Northern Point excavation area at the Yana RHS site4. c, Cultural layer in H29 unit in which the human tooth was found. d, Cryolithological profile for Northern Point of Yana RHS92. e, Human tooth found during the excavations in unit 2V26 shown in occlusal and lateral view (e1); human tooth found in unit X26 shown in occlusal view (e2); and human tooth found in unit H29 shown in occlusal and lateral view (e3). The samples e2 (Yana2 genome) and e3 (Yana1 with high-coverage (25.6×) genome sequence) are used in this study. In the key for d (bottom): 1, sand with small pebbles; 2, sandy silt; 3, clayey-sand silt; 4, sandy-clayey silt; 5, interbedding of clayey silt bands and sandy-clayey silt with beds and lenses of peat; 6, soil–vegetation layer; 7, cultural layer; 8, polygonal ice wedges; 9, boundary of seasonally active layer; 10, location of bones of Pleistocene animals sampled for 14С dating; 11, location of 14С samples of plant remains; 12, radiocarbon date and laboratory code.
Maximum likelihood tree of Y chromosome sequences for modern and ancient individuals, with major haplogroups highlighted. Numbers on internal nodes show bootstrap support values from 100 replicates for nodes with bootstrap values < 100.
a–c, Geographical heat maps depicting the outgroup-f3 statistics for Yana1 (a), Tianyuan (b) and Sunghir3 (c) individuals with 167 worldwide populations. d, f4-statistics contrasting allele sharing of Yana RHS individuals and other selected Upper Palaeolithic groups with early West Eurasians (represented by the Kostenki 14 individual) or East Asians (represented by the Tianyuan individual). e, f4-statistics for highlighting groups with affinities to both early West Eurasians and East Asians (joined with dashed lines). Error bars indicate ± 3 s.e., obtained using a block jackknife (Methods). f, Admixture graph models of ancient and modern populations for western Eurasia (left) and East Asia and the Americas (right). Newly reported individuals are highlighted with a coloured background. Early Upper Palaeolithic individuals were modelled allowing for a possible additional Neanderthal contribution to account for higher levels of Neanderthal ancestry (dotted lines).
a, Kinship coefficient and R1 ratio (number of double-heterozygous (Aa/Aa) sites divided by the total number of discordant genotypes) for newly reported ancient groups with multiple individuals per site. b, Number and length of homozygosity-by-descent (HBD) segments in ancient and modern individuals. Grey ellipses indicate 95% confidence region obtained from simulations of 100 haploid genomes of indicated effective population size. c, Distribution of total identity-by-descent (IBD) lengths for simulations of varying effective population sizes. Observed values for pairs from the Sunghir and Yana individuals are indicated by dashed lines.
a, b, Geographical heat maps depicting genetic affinities of the Kolyma1 individual using outgroup-f3 statistics with 167 modern populations (a) and total length of haplotype chunks donated to 206 modern populations in chromosome painting (b). c, Chromosome-painting symmetry statistic contrasting the total length of haplotypes donated from ancient and modern non-American donor groups to pairs of Native American populations, for two different datasets (1240K and WGS; Supplementary Information 3). The top panels show a greater excess in donations to Athabascans from Kolyma1. The bottom panels show the same statistic for West Greenland Inuit, a population with known affinity to Palaeo-Eskimos, which is reflected in the excess donations observed from the Saqqaq individual. Error bars indicate ± 3 s.e., obtained using a block jackknife.
Maps showing regions that are climatically suitable for human occupation, across temporal and spatial dimensions. Projections are bounded from 60° E to 180° E and from 38° N to 80° N. The colour key represents suitability values; darker colours correspond to higher—and lighter colours to lower—suitability values. a, Examples of climatic suitability for human occupation for different time slices. b, Median and s.d. of climatic suitability across 23 climatic periods of millennial or bimillennial time resolution. c, Regions that are highly climatically suitable for humans are shown in red; regions of low suitability are shown in grey; and regions with periods of both high and low suitability are shown in orange.
a, Maps showing locations and ancestry proportions of ancient (left) and modern (right) groups. b–d, Ancestry proportions and fit for all possible two-way (b), three-way (c) and four-way (d) reference population combinations. Transparent shading indicates model fit, with lighter transparency indicating models accepted with 0.05 > P ≥ 0.01 in qpAdm. Numbers of individuals for source and target populations are given in parentheses.
a, Principal component analysis of 93 ancient individuals projected onto a set of 587 modern Eurasian and Native American individuals. b, c, Multidimensional scaling (MDS) plots of 715 individuals from 91 modern populations, obtained from the chromosome-painting co-ancestry matrix using modern Africans and high-coverage ancient individuals as donors, based on total length of chunks (b) or total number of chunks (c).
This file contains Supplementary Information Sections 1-9 and an Appendix
This file contains Supplementary Data Tables 1-5. Supplementary Data Table 1 contains details of the newly sequenced individuals; Supplementary Data Table 2 shows sequencing statistics; Supplementary Data Table 3 contains panels of ancient individuals used in the analyses; Supplementary Data Table 4 contains panels of modern individuals used in the analyses and Supplementary Data Table 5 shows full qpAdm results for all 2-, 3- and 4-way models
About this article
Cite this article
Sikora, M., Pitulko, V.V., Sousa, V.C. et al. The population history of northeastern Siberia since the Pleistocene. Nature 570, 182–188 (2019). https://doi.org/10.1038/s41586-019-1279-z
Different historical generation intervals in human populations inferred from Neanderthal fragment lengths and mutation signatures
Nature Communications (2021)
Denisovans, Neanderthals, and Early Modern Humans: A Review of the Pleistocene Hominin Fossils from the Altai Mountains (Southern Siberia)
Journal of Archaeological Research (2021)