doi: 10.1038/nature25778. Epub 2018 Feb 21.
The genomic history of southeastern Europe
Iain Mathieson 1, Songül Alpaslan-Roodenberg 1, Cosimo Posth 2 3, Anna Szécsényi-Nagy 4, Nadin Rohland 1, Swapan Mallick 1 5, Iñigo Olalde 1, Nasreen Broomandkhoshbacht 1 5, Francesca Candilio 6, Olivia Cheronet 6 7, Daniel Fernandes 6 8, Matthew Ferry 1 5, Beatriz Gamarra 6, Gloria González Fortes 9, Wolfgang Haak 2 10, Eadaoin Harney 1 5, Eppie Jones 11 12, Denise Keating 6, Ben Krause-Kyora 2, Isil Kucukkalipci 3, Megan Michel 1 5, Alissa Mittnik 2 3, Kathrin Nägele 2, Mario Novak 6 13, Jonas Oppenheimer 1 5, Nick Patterson 14, Saskia Pfrengle 3, Kendra Sirak 6 15, Kristin Stewardson 1 5, Stefania Vai 16, Stefan Alexandrov 17, Kurt W Alt 18 19 20, Radian Andreescu 21, Dragana Antonović 22, Abigail Ash 6, Nadezhda Atanassova 23, Krum Bacvarov 17, Mende Balázs Gusztáv 4, Hervé Bocherens 24 25, Michael Bolus 26, Adina Boroneanţ 27, Yavor Boyadzhiev 17, Alicja Budnik 28, Josip Burmaz 29, Stefan Chohadzhiev 30, Nicholas J Conard 25 31, Richard Cottiaux 32, Maja Čuka 33, Christophe Cupillard 34 35, Dorothée G Drucker 25, Nedko Elenski 36, Michael Francken 37, Borislava Galabova 38, Georgi Ganetsovski 39, Bernard Gély 40, Tamás Hajdu 41, Veneta Handzhyiska 42, Katerina Harvati 25 37, Thomas Higham 43, Stanislav Iliev 44, Ivor Janković 13 45, Ivor Karavanić 45 46, Douglas J Kennett 47, Darko Komšo 33, Alexandra Kozak 48, Damian Labuda 49, Martina Lari 16, Catalin Lazar 21 50, Maleen Leppek 51, Krassimir Leshtakov 42, Domenico Lo Vetro 52 53, Dženi Los 29, Ivaylo Lozanov 42, Maria Malina 26, Fabio Martini 52 53, Kath McSweeney 54, Harald Meller 20, Marko Menđušić 55, Pavel Mirea 56, Vyacheslav Moiseyev 57, Vanya Petrova 42, T Douglas Price 58, Angela Simalcsik 59, Luca Sineo 60, Mario Šlaus 61, Vladimir Slavchev 62, Petar Stanev 36, Andrej Starović 63, Tamás Szeniczey 41, Sahra Talamo 64, Maria Teschler-Nicola 7 65, Corinne Thevenet 32, Ivan Valchev 42, Frédérique Valentin 66, Sergey Vasilyev 67, Fanica Veljanovska 68, Svetlana Venelinova 69, Elizaveta Veselovskaya 67, Bence Viola 70 71, Cristian Virag 72, Joško Zaninović 73, Steve Zäuner 74, Philipp W Stockhammer 2 51, Giulio Catalano 60, Raiko Krauß 75, David Caramelli 16, Gunita Zariņa 76, Bisserka Gaydarska 77, Malcolm Lillie 78, Alexey G Nikitin 79, Inna Potekhina 48, Anastasia Papathanasiou 80, Dušan Borić 81, Clive Bonsall 54, Johannes Krause 2 3, Ron Pinhasi 6 7, David Reich 1 5 14
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- PMID:29466330
- PMCID: PMC6091220
- DOI: 10.1038/nature25778
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The genomic history of southeastern Europe
Iain Mathieson et al. Nature..
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Abstract
Farming was first introduced to Europe in the mid-seventh millennium bc, and was associated with migrants from Anatolia who settled in the southeast before spreading throughout Europe. Here, to understand the dynamics of this process, we analysed genome-wide ancient DNA data from 225 individuals who lived in southeastern Europe and surrounding regions between 12000 and 500 bc. We document a west-east cline of ancestry in indigenous hunter-gatherers and, in eastern Europe, the early stages in the formation of Bronze Age steppe ancestry. We show that the first farmers of northern and western Europe dispersed through southeastern Europe with limited hunter-gatherer admixture, but that some early groups in the southeast mixed extensively with hunter-gatherers without the sex-biased admixture that prevailed later in the north and west. We also show that southeastern Europe continued to be a nexus between east and west after the arrival of farmers, with intermittent genetic contact with steppe populations occurring up to 2,000 years earlier than the migrations from the steppe that ultimately replaced much of the population of northern Europe.
Figures
PCA of 486 ancient individuals, projected onto principal components defined by 777 present-day West Eurasian individuals (grey points). This differs from Figure 1B in that the plot is not cropped and the present-day individuals are shown.
Supervised ADMIXTURE analysis modeling each ancient individual (one per row), as a mixture of populations represented by clusters that are constrained to contain Anatolian Neolithic (grey), Yamnaya from Samara (yellow), EHG (pink) and WHG (green) populations. Dates in parentheses indicate approximate range of individuals in each population. This differs from Figure 1D in that it contains some previously published samples, and includes sample IDs.
Unsupervised ADMIXTURE plot from k=4 to 12, on a dataset consisting of 1099 present-day individuals and 476 ancient individuals. We show newly reported ancient individuals and some previously published individuals for comparison.
Spatial structure in hunter-gatherers. Estimated effective migration surface (EEMS). This fits a model of genetic relatedness where individuals move (in a random direction) from generation to generation on an underlying grid so that genetic relatedness is determined by distance. The migration parameterm defines the local rate of migration, varies on the grid and is inferred. This plot showslog10(m), scaled relative to the average migration rate (which is arbitrary). Thuslog10(m)=2, for example, implies that the rate of migration at this point on the grid is 100 times higher than average. To restrict as much as possible to hunter-gatherer structure, the migration surface is inferred using data from 116 individuals that date to earlier than ~5000 BCE and have no NW Anatolian-related ancestry. Though the migration surface is sensitive to sampling, and fine-scale features may not be interpretable, the migration “barrier” (region of low migration) running north-south and separating populations with primarily WHG from primarily EHG ancestry seems to be robust, and consistent with inferred admixture proportions. This analysis suggests that Mesolithic hunter-gatherer population structure was clustered and not smoothly clinal, in the sense that genetic differentiation did not vary consistently with distance. Superimposed on this background, pies show the WHG, EHG and CHG ancestry proportions inferred for populations used to construct the migration surface (another way of visualizing the data in Figure 2, Supplementary Table 3.1.3 – we use two population models if they fit with p>0.01, and three population models otherwise). Pies with only a single color are those that were fixed to be the source populations.
log-likelihood surfaces for the proportion of female (x-axis) and male (y-axis) ancestors that are hunter-gatherer-related for the combined populations analyzed in Figure 3C, and the two populations with the strongest evidence for sex-bias. Numbers in parentheses give the number of individuals in each group. Log-likelihood scale ranges from 0 to -10, where 0 is the feasible point with the highest likelihood.
A: Locations of newly reported individuals.B: Ancient individuals projected onto principal components defined by 777 present-day West Eurasians (shown in Extended Data Figure 1). Includes selected published individuals (faded circles, labeled) and newly reported individuals (other symbols, outliers enclosed in black circles). Colored polygons cover individuals that had cluster memberships fixed at 100% for supervised admixture analysis.C: Date (direct or contextual) for each sample and approximate chronology of southeastern Europe.D: Supervised ADMIXTURE analysis, modeling each ancient individual (one per row), as a mixture of population clusters constrained to contain Anatolian Neolithic (grey), Yamnaya from Samara (yellow), EHG (pink) and WHG (green) populations. Dates in parentheses indicate approximate range of individuals in each population. See Extended Data Figure 2 for individual sample IDs. Map data inA from theR packagemaps.
Inferred ancestry proportions for populations modeled as a mixture of WHG, EHG and CHG (Supplementary Table S3.1.3). Dashed lines show populations from the same geographic region. Percentages indicate proportion of WHG+EHG ancestry. Standard errors range from 1.5-8.3% (Supplementary Table S3.1.3).
A: Populations modeled as a mixture of NW Anatolia Neolithic, WHG, and EHG. Dashed lines show temporal relationships between populations from the same geographic region. Percentages indicate proportion of WHG+EHG ancestry. Standard errors range from 0.7-6.0% (Supplementary Table S3.2.2).B: Z-scores for the difference in hunter-gatherer-related ancestry on the autosomes compared to the X chromosome when populations are modeled as a mixture of NW Anatolia Neolithic and WHG (N=126 individuals, group sizes in parentheses). Positive values indicate more hunter-gatherer-related ancestry on the autosomes and thus male-biased hunter-gatherer ancestry. “Combined” populations merge all individuals from different times from a geographic area.C: Hunter-gatherer-related ancestry proportions on the autosomes, X chromosome, mitochondrial DNA (i.e. mt haplogroup U), and the Y chromosome (i.e. Y chromosome haplogroups I2, R1 and C1). Points showqpAdm (autosomes and X chromosome) or maximum likelihood (MT and Y chromosome) estimates and bars show approximate 95% confidence intervals (N=109 individuals, group sizes in parentheses).
References
- Tringham RE. In: The Transition to Agriculture in Prehistoric Europe. Price D, editor. Cambridge University Press; 2000. pp. 19–56.
- Bellwood P. First Farmers: The Origins of Agricultural Societies. 2nd. Wiley-Blackwell; 2004.
- Golitko M. In: Ancient Europe, 8000 BC to AD 1000: An Encyclopedia of the Barbarian World. Bogucki P, Crabtree PJ, editors. Charles Scribners & Sons; 2003. pp. 259–266.
- Vander Linden M. In: Investigating Archaeological Cultures: Material Culture, Variability, and Transmission. Roberts BW, Linden M Vander, editors. Springer; 2012. pp. 289–319.
- Bramanti B, et al. Genetic discontinuity between local hunter-gatherers and central Europe’s first farmers. Science. 2009;326:137–140. - PubMed
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