Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2016 Jun 9;534(7606):200-5.
doi: 10.1038/nature17993. Epub 2016 May 2.

The Genetic History of Ice Age Europe

Qiaomei Fu  1   2   3 Cosimo Posth  4   5 Mateja Hajdinjak  3 Martin Petr  3 Swapan Mallick  2   6   7 Daniel Fernandes  8   9 Anja Furtwängler  4 Wolfgang Haak  5   10 Matthias Meyer  3 Alissa Mittnik  4   5 Birgit Nickel  3 Alexander Peltzer  4 Nadin Rohland  2 Viviane Slon  3 Sahra Talamo  11 Iosif Lazaridis  2 Mark Lipson  2 Iain Mathieson  2 Stephan Schiffels  5 Pontus Skoglund  2 Anatoly P Derevianko  12   13 Nikolai Drozdov  12 Vyacheslav Slavinsky  12 Alexander Tsybankov  12 Renata Grifoni Cremonesi  14 Francesco Mallegni  15 Bernard Gély  16 Eligio Vacca  17 Manuel R González Morales  18 Lawrence G Straus  18   19 Christine Neugebauer-Maresch  20 Maria Teschler-Nicola  21   22 Silviu Constantin  23 Oana Teodora Moldovan  24 Stefano Benazzi  11   25 Marco Peresani  26 Donato Coppola  27   28 Martina Lari  29 Stefano Ricci  30 Annamaria Ronchitelli  30 Frédérique Valentin  31 Corinne Thevenet  32 Kurt Wehrberger  33 Dan Grigorescu  34 Hélène Rougier  35 Isabelle Crevecoeur  36 Damien Flas  37 Patrick Semal  38 Marcello A Mannino  11   39 Christophe Cupillard  40   41 Hervé Bocherens  42   43 Nicholas J Conard  43   44 Katerina Harvati  43   45 Vyacheslav Moiseyev  46 Dorothée G Drucker  42 Jiří Svoboda  47   48 Michael P Richards  11   49 David Caramelli  29 Ron Pinhasi  8 Janet Kelso  3 Nick Patterson  6 Johannes Krause  4   5   43 Svante Pääbo  3 David Reich  2   6   7
Free PMC article

The Genetic History of Ice Age Europe

Qiaomei Fu et al. Nature. .
Free PMC article


Modern humans arrived in Europe ~45,000 years ago, but little is known about their genetic composition before the start of farming ~8,500 years ago. Here we analyse genome-wide data from 51 Eurasians from ~45,000-7,000 years ago. Over this time, the proportion of Neanderthal DNA decreased from 3-6% to around 2%, consistent with natural selection against Neanderthal variants in modern humans. Whereas there is no evidence of the earliest modern humans in Europe contributing to the genetic composition of present-day Europeans, all individuals between ~37,000 and ~14,000 years ago descended from a single founder population which forms part of the ancestry of present-day Europeans. An ~35,000-year-old individual from northwest Europe represents an early branch of this founder population which was then displaced across a broad region, before reappearing in southwest Europe at the height of the last Ice Age ~19,000 years ago. During the major warming period after ~14,000 years ago, a genetic component related to present-day Near Easterners became widespread in Europe. These results document how population turnover and migration have been recurring themes of European prehistory.

Conflict of interest statement

The authors declare no competing financial interests.


Extended Data Figure 1
Extended Data Figure 1. A decrease in Neanderthal ancestry in the last 45,000 years
This is similar to Figure 2, except we use ancestry estimates from rates of alleles matching to Neanderthal rather than f4-ratios, as described in Supplementary Information section 3). The least squares fit excludes Oase1 (as an outlier with recent Neanderthal ancestry) and Europeans (known to have reduce Neanderthal ancestry). The regression slope is significantly negative (P=0.00004, Extended Data Table 3).
Extended Data Fig. 2
Extended Data Fig. 2. Heat matrix of pairwise f3(X, Y; Mbuti) for selected ancient samples
We analyze only samples with at least 30,000 SNPs covered at least once, which pass our quality control.
Extended Data Fig. 3
Extended Data Fig. 3. Studying how the relatedness of non-European populations to pairs of European hunter-gatherers changes over time
We examine statistics of the form D(W, X; Y, Mbuti), with the Z-score given on the y-axis, where W is an early European hunter-gatherer, X is another European hunter-gatherer (in chronological order on the x-axis), and Y is a non-European population (see legend). A: W=Kostenki14. B: W=GoyetQ116-1. C: W=Vestonice16. D: W=ElMiron. |Z|>3 scores are considered statistically significant (horizontal line). The similar Figure 4b gives absolute D-statistic values rather than Z-scores (for W=Kostenki14) and uses pooled regions rather than individual populations Y.
Extended Data Figure 4
Extended Data Figure 4. An Admixture Graph model that fits the data for Satsurblia, an Upper Paleolithic sample from the Caucasus
This model uses 127,057 SNPs covered in all populations. Estimated genetic drifts are give along the solid lines in units of f2-distance (parts per thousand), and estimated mixture proportions are given along the dotted lines. All three models provide an fit to the allele frequency correlation data among Mbuti, UstIshim, Kostenki14, Vestonice16, Malta1, ElMiron and Satsurblia to within the limits of our resolution, in the sense that all empirical f2-, f3- and f4-statistics relating the samples are within three standard errors of the expectation of the model. Models in which Satsurblia is modeled as unadmixed cannot be fit.
Figure 1
Figure 1. Location and age of 51 ancient samples
Each bar corresponds to a sample, the color code designates the genetically defined sample cluster, and the height is proportional to sample age (the background grid shows a projection of longitude against sample age). To help in visualization, we add jitter for sites with multiple samples from nearby locations. Four samples that are from Siberia are plotted at the far eastern edge of the map.
Figure 2
Figure 2. Decrease of Neanderthal ancestry over time
Plot of radiocarbon date against Neanderthal ancestry for samples with at least >200,000 SNPs covered, along with present-day Eurasians (standard errors are from a Block Jackknife). The least squares fit (gray) excludes the data from Oase1 (an outlier with recent Neanderthal ancestry) and three present-day European populations (known to have less Neanderthal ancestry than East Asians). The slope is significantly negative for all eleven subsets of samples we analyzed (10−29<P<10−11 based on a Block Jackknife) (Extended Data Table 3).
Figure 3
Figure 3. Genetic clustering
(A) Shared genetic drift measured by f3(X,Y; Mbuti) among samples with at least 30,000 SNPs covered (for AfontovaGora3, ElMiron, Falkenstein, GoyetQ-2, GoyetQ53-1, HohleFels49, HohleFels79, LesCloseaux13, Ofnet, Ranchot88 and Rigney1, we use all sequences for higher resolution). Lighter colors indicate more shared drift. (B) Multidimensional Dimensional Scaling (MDS) analysis, computed using the R software cmdscale package, highlights the main genetic groupings analyzed in this study: Vestonice Cluster (brown), Mal’ta Cluster (pink), El Mirón Cluster (yellow), Villabruna Cluster (light blue), and Satsurblia Cluster (dark purple). The affinity of GoyetQ116-1 (green) to the El Mirón Cluster is evident in both views of the data.
Figure 4
Figure 4. Population history inferences
(A) Admixture Graph relating selected high coverage samples. Dashed lines show inferred admixture events; the estimated mixture proportions fitted using the ADMIXTUREGRAPH software are labeled (the estimated genetic drift on each branch is given in a version of this graph shown in Supplementary Information section 6). The samples are positioned vertically based on their radiocarbon date, but we caution that the population split times are not accurately known. We use color to highlight important early branches of the European founder population: the Kostenki14 lineage is modeled as the predominant contributor to the Vestonice Cluster (green); the GoyetQ116-1 lineage as the predominant contributor to the El Mirón Cluster (red); and the Villabruna lineage as broadly represented across many clusters. (B) Drawing together of European and Near Eastern populations ~14,000 years ago. Plot of affinity of each pre-Neolithic European population X to non-Africans outside Europe Y moving forward in time, comparing to Kostenki14 as a baseline; values Z<-3 standard errors below zero are indicated with filled symbols (we restricted to individuals with >50,000 SNPs). We observe an affinity to Near Easterners beginning with the Villabruna Cluster, and another to East Asians that affects a subset of the Villabruna Cluster.

Similar articles

  • Higher levels of neanderthal ancestry in East Asians than in Europeans.
    Wall JD, Yang MA, Jay F, Kim SK, Durand EY, Stevison LS, Gignoux C, Woerner A, Hammer MF, Slatkin M. Wall JD, et al. Genetics. 2013 May;194(1):199-209. doi: 10.1534/genetics.112.148213. Epub 2013 Feb 14. Genetics. 2013. PMID: 23410836 Free PMC article.
  • An early modern human from Romania with a recent Neanderthal ancestor.
    Fu Q, Hajdinjak M, Moldovan OT, Constantin S, Mallick S, Skoglund P, Patterson N, Rohland N, Lazaridis I, Nickel B, Viola B, Prüfer K, Meyer M, Kelso J, Reich D, Pääbo S. Fu Q, et al. Nature. 2015 Aug 13;524(7564):216-9. doi: 10.1038/nature14558. Epub 2015 Jun 22. Nature. 2015. PMID: 26098372 Free PMC article.
  • The evolutionary history of human populations in Europe.
    Lazaridis I. Lazaridis I. Curr Opin Genet Dev. 2018 Dec;53:21-27. doi: 10.1016/j.gde.2018.06.007. Epub 2018 Jun 28. Curr Opin Genet Dev. 2018. PMID: 29960127 Review.
  • Reconstructing the genetic history of late Neanderthals.
    Hajdinjak M, Fu Q, Hübner A, Petr M, Mafessoni F, Grote S, Skoglund P, Narasimham V, Rougier H, Crevecoeur I, Semal P, Soressi M, Talamo S, Hublin JJ, Gušić I, Kućan Ž, Rudan P, Golovanova LV, Doronichev VB, Posth C, Krause J, Korlević P, Nagel S, Nickel B, Slatkin M, Patterson N, Reich D, Prüfer K, Meyer M, Pääbo S, Kelso J. Hajdinjak M, et al. Version 2. Nature. 2018 Mar 29;555(7698):652-656. doi: 10.1038/nature26151. Epub 2018 Mar 21. Nature. 2018. PMID: 29562232 Free PMC article.
  • Ancestry of modern Europeans: contributions of ancient DNA.
    Lacan M, Keyser C, Crubézy E, Ludes B. Lacan M, et al. Cell Mol Life Sci. 2013 Jul;70(14):2473-87. doi: 10.1007/s00018-012-1180-5. Epub 2012 Oct 11. Cell Mol Life Sci. 2013. PMID: 23052219 Review.
See all similar articles

Cited by 142 articles

See all "Cited by" articles


    1. Gamble C, Davies W, Pettitt P, Richards M. Climate change and evolving human diversity in Europe during the last glacial. Philosophical transactions of the Royal Society of London. Series B, Biological sciences. 2004;359:24–53. doi: 10.1098/rstb.2003.1396. discussion 253–244. - DOI - PMC - PubMed
    1. Jones ER, et al. Upper Palaeolithic genomes reveal deep roots of modern Eurasians. Nature communications. 2015;6:8912. doi: 10.1038/ncomms9912. - DOI - PMC - PubMed
    1. Fu Q, et al. An early modern human from Romania with a recent Neanderthal ancestor. Nature. 2015 doi: 10.1038/nature14558. - DOI - PMC - PubMed
    1. Seguin-Orlando A, et al. Paleogenomics. Genomic structure in Europeans dating back at least 36,200 years. Science. 2014;346:1113–1118. doi: 10.1126/science.aaa0114. - DOI - PubMed
    1. Dabney J, et al. Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proc Natl Acad Sci U S A. 2013;110:15758–15763. doi: 10.1073/pnas.1314445110. - DOI - PMC - PubMed

Publication types

MeSH terms