The genetic history of Ice Age Europe

Abstract

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.

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. 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. 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. 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. 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. 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. 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. 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.