Ancient DNA reveals prehistoric gene-flow from Siberia in the complex human population history of north east Europe

North East Europe harbors a high diversity of cultures and languages, suggesting a complex genetic history. Archaeological, anthropological, and genetic research has revealed a series of influences from Western and Eastern Eurasia in the past. While genetic data from modern-day populations is commonly used to make inferences about their origins and past migrations, ancient DNA provides a powerful test of such hypotheses by giving a snapshot of the past genetic diversity. In order to better understand the dynamics that have shaped the gene pool of North East Europeans, we generated and analyzed 34 mitochondrial genotypes from the skeletal remains of three archaeological sites in northwest Russia. These sites were dated to the Mesolithic and the Early Metal Age (7,500 and 3,500 uncalibrated years Before Present). We applied a suite of population genetic analyses (principal component analysis, genetic distance mapping, haplotype sharing analyses) and compared past demographic models through coalescent simulations using Bayesian Serial SimCoal and Approximate Bayesian Computation. Comparisons of genetic data from ancient and modern-day populations revealed significant changes in the mitochondrial makeup of North East Europeans through time. Mesolithic foragers showed high frequencies and diversity of haplogroups U (U2e, U4, U5a), a pattern observed previously in European hunter-gatherers from Iberia to Scandinavia. In contrast, the presence of mitochondrial DNA haplogroups C, D, and Z in Early Metal Age individuals suggested discontinuity with Mesolithic hunter-gatherers and genetic influx from central/eastern Siberia. We identified remarkable genetic dissimilarities between prehistoric and modern-day North East Europeans/Saami, which suggests an important role of post-Mesolithic migrations from Western Europe and subsequent population replacement/extinctions. This work demonstrates how ancient DNA can improve our understanding of human population movements across Eurasia. It contributes to the description of the spatio-temporal distribution of mitochondrial diversity and will be of significance for future reconstructions of the history of Europeans.Clio Der Sarkissian, Oleg Balanovsky, Guido Brandt, Valery Khartanovich, Alexandra Buzhilova, Sergey Koshel, Valery Zaporozhchenko, Detlef Gronenborn, Vyacheslav Moiseyev, Eugen Kolpakov, Vladimir Shumkin, Kurt W. Alt, Elena Balanovska, Alan Cooper, Wolfgang Haak, the Genographic Consortiu

Map of Eurasia showing the approximate location of ancient (uncalibrated dates) and present-day Eurasian samples.

<p>Red dots represent the archaeological sites sampled for ancient mitochondrial DNA in this study: aUZ, Yuzhnyy Oleni Ostrov; aPo, Popovo; aBOO, Bol'shoy Oleni Ostrov. Black circles represent ancient populations abbreviated as follows: aEG, Confederated nomads of the Xiongnu (2,200–2,300 yBP); aKAZ, Nomads from Kazakhstan (2,100–3,400 yBP); aKOS, Kostenski individual (30,000 yBP); aKUR, Siberian Kurgans (1,600–3,800 yBP); aLOK, Lokomotiv Kitoi Neolithic individuals (6,130–7,140 yBP); aPWC, Scandinavian Pitted-Ware Culture foragers (4,500–5,300 yBP); aUST, Ust'Ida Neolithic population (4,000–5,800 yBP). Smaller black dots signify the location of Palaeolithic/Mesolithic sites sampled for ancient mitochondrial DNA in aHG (4,250–15,400 yBP). Present-day populations are abbreviated as follows: alt, Altaians; BA, Bashkirs; BU, Buryats; CU, Chuvash; EST, Estonians; FIN, Finns; ket, Kets; kham, Khamnigans; khan, Khants; KK, Khakhassians; KO, Komis; KR, Karelians; LTU, Lithuanians; LVA, Latvians; man, Mansi; ME, Mari; MO, Mordvinians; MNG, Mongolians; NEN, Nenets; nga, Nganasans; NOR, Norwegians; tof, Tofalars; tuv, Tuvinians; UD, Udmurts; SA, Yakuts; saa, Saami; sel, Selkups; SWE, Swedes. The approximate location of the Volga-Ural Basin and of the different regions of Russian Siberia are also indicated.</p

Results for mitochondrial DNA typing.

a<p>Transitions are reported with upper-case letters, transversions with lower-case letters.</p>b<p>E, number of samples from which DNA was independently extracted; I, results replicated in an independent laboratory; C, number of HVR-I clones; Q, HVR-I DNA quantification performed.</p>c<p>Position 390R was not included in population genetics analyses.</p><p>Hg, haplogroup; HVR-I, hypervariable region I; np, nucleotide positions; yBP, years Before Present.</p

Graphical representation and Akaike Information Criterions of the demographic models compared by coalescent simulation analyses.

<p>The timeline indicates the age of populations in generations (G). For models H0a to H0e, genetic continuity is tested between combinations of ancient populations and present-day populations of North East Europe (NEE) or Saami (saa), as indicated in the column ‘P₀’. For models H1a and H1b, genetic discontinuity between aUzPo or aBOO, and NEE is tested assuming a migration from Central Europe (CE). The percentage of migrants from the source population into the sink population (10%, 50% and 75%) is indicated in the column ‘%’. The cells containing Akaike Information Criterion (AIC) values were colored according to the gradient of AIC represented below the figure: from white for the highest value of AIC (worst model fit, 199.1 for H0b) to red for the lowest value of AIC (best model fit, 81.9 for H0a).</p

Principal Component Analysis of mitochondrial haplogroup frequencies.

<p>The first two dimensions account for 41.5% of the total variance. Grey arrows represent haplogroup loading vectors, i.e., the contribution of each haplogroup. Red dots represent ancient populations described in this study: aUzPo, Yuzhnyy Oleni Ostrov and Popovo (7,500 uncal. yBP); aBOO, Bol'shoy Oleni Ostrov (3,500 uncal. yBP). Other ancient populations were labeled as follows: aEG, Confederated nomads of the Xiongnu (4,250-2,300 yBP); aHG, Palaeolithic/Mesolithic hunter-gatherers of Central/East Europe (4,250-30,000 yBP); aKAZ, Nomads from Kazakhstan (2,100–3,400 yBP); aKUR, Siberian Kurgans (1,600–3,800 yBP); aLBK, Neolithic individuals from Germany (7,000–7,500 yBP); aLOK, Lokomotiv Kitoi Neolithic individuals (6,130–7,140 yBP); aSP, Neolithic individuals from Spain (5,000–5,500 yBP); aPWC, Scandinavian Pitted-Ware Culture foragers (4,500–5,300 yBP); aUST, Ust'Ida Neolithic population (4,000–5,800 yBP). Extant populations were abbreviated as follows: ALB, Albanians; ale, Aleuts; alt, Altaians; ARM, Armenians; aro, Arorums; AUT, Austrians; AZE, Azerbaijani; BA, Bashkirs; bas, Basques; BEL, Belarusians; BGR, Bulgarians; BIH, Bosnians; BU, Buryats; CHE, Swiss; CHU, Chukchi; CU, Chuvashes; CYP, Cypriots; CZE, Czechs; DEU, Germans; esk, Eskimos; ESP, Spanish; EST, Estonians; eve, Evenks; evn, Evens; FIN, Finns; FRA, French; GBR, British; GEO, Georgians; GRC, Greeks; HRV, Croatians; HUN, Hungarians; ing, Ingrians; IRL, Irish; IRN, Iranians; IRQ, Iraqi; ISL, Icelanders; IT-88, Sardinians; ITA, Italians; JOR, Jordanians; kab, Kabardians; ket, Kets; kham, Khamnigans; khan, Khants; KK, Khakhassians; KO, Komi; kor, Koryaks; KR, Karelians; kur, Kurds; LTU, Lithuanians; LVA, Latvians; man, Mansi; ME, Mari; MNG, Mongolians; MO, Mordvinians; NEN_A, eastern Nenets; NEN_E, western Nenets; nga, Nganasans; niv, Nivkhs; nog, Nogays; NOR, Norwegians; POL, Poles; PRT, Portuguese; PSE, Palestinans; ROU, Romanians; RUS, Russians; SA, Yakuts; saa, Saami; SAU, Saudi Arabians; SE, Ossets; sel, Selkups; sho, Shors; SVK, Slovakians; SVN, Slovenians; SWE, Swedes; SYR, Syrians; TA, Tatars; tel, Telenghits; tof, Tofalars; tub, Tubalars; TUR, Turks; tuv, Tuvinians; UD, Udmurts; UKR, Ukrainians; ulc, Ulchi; vep, Vepses; yuk, Yukaghirs.</p

Percentages of haplotypes from aUzPo and aBOO matched in modern-day Eurasian population pools.

<p>Percentages of matches for the haplotypes from aBOO are represented by white bars. Percentages of matches for the haplotypes from aUzPo are independently represented by superimposed black bars.</p

Relative model likelihood of the demographic models simulated in Bayesian Serial SimCoal, as indicated by Akaike weights ω.

<p>For each hypothesis tested, models are ordered from the least likely (lowest ω) to the most likely model (highest ω). NEE, North East Europe; CE, Central Europe.</p

Population parameters and statistics used in Bayesian Serial SimCoal coalescent simulation analyses.

<p>Population parameters and statistics used in Bayesian Serial SimCoal coalescent simulation analyses.</p