mtDNA Haplogroup U

Evidence for Siberian gene flow into far north-eastern Europe.

At the 3,500 uncal. yBP site of aBOO, we observed 39% ‘European’ hgs: U5a (26%), U4 (9%), T (4%), and 61% ‘Central/East Siberian’ hgs: C (35%), Z (13%), D (13%). Concordant with this admixed hg make-up, PCA indicated a position close to present-day Siberians (Figure 2). This position did not change when potential maternal relationships among individuals were accounted for by excluding redundant haplotypes (Figure S2B). The genetic relationship between aBOO and Siberians was also evident on the genetic distance map, where the area representing the lowest genetic distance covered a broader area of Siberia than for aUzPo (Figure 3B). The extant populations that showed most genetic similarity to aBOO were found in Central and East Siberia. In contrast, the area of maximum similarity for aUzPo lay in West Siberia (Figure 3A); this observation however could be influenced by low sample size in aUzPo.


A Tuvinian girl

Haplotype sharing analyses for aBOO confirmed the genetic affinity with modern-day West and Central/East Siberians inferred from the PCA (Figure 4), but also identified a close relationship with the VUB population pool. The distribution of haplotype matches observed in pools of the VUB, West Siberia and Central/East Siberia was partly due to the presence of basal C* (16223T-16298C-16327T) and D* (16223T-16362C) haplotypes in these pools, whereas these types were absent in Middle Eastern and European pools. Central Siberian Tuvinians displayed the highest percentage of shared haplotypes with aBOO (12.2%) although all shared haplotypes belong to hgs C* and D*. A more explicit genetic link between aBOO and extant East Siberians was seen in the presence of the derived C5 haplotype (16148T-16223T-16288C-16298C-16311C-16327T) in aBOO and in one single Buryat individual of Central Siberia [54]. The Z1a haplotype (16129A-16185T-16223T-16224C-16260T-16298C) detected in aBOO had a broad but interesting distribution in Eurasia. It was found in all Central/East Siberian pools except in Tuvinians, but also in the Bashkirs of the Urals, in the VUB pool, as well as in Scandinavian and Baltic populations (Norwegians, Swedes, Finns, Ingrians, Karelians, and the Saami).

Although haplotype sharing analyses revealed genetic links between aBOO and extant populations of NEE, a strong genetic differentiation was obvious between aBOO, modern-day NEE and Saami. This genetic discontinuity was further supported by BayeSSC analyses (Figure 5; Table 3). Similarly to aUzPo, a better fit was obtained for the model involving a 10% migration from CE over the last 3,500 years (H1b; ω = 1.00E+0) than for the model of genetic continuity between aBOO and NEE (H0b; ω = 3.86E-10).


Figure 6. Percentages of haplotypes from aUzPo and aBOO matched in selected ancient Eurasian populations.

Previously described populations of hunter-gatherers of Central/East Europe (aHG [12], [14]) and Scandinavia (aPWC, [13]) were characterized by high frequencies and diversity of hg U4, U5a and U5b, which caused the two ancient datasets to group outside the cluster of extant European populations on the PCA plot (Figure 2). This matches previous studies that have shown that genetic continuity between hunter-gatherers and present-day Europeans can be rejected [12]–[13]. Like other European hunter-gatherers, aUzPo is characterized by high frequencies and diversity of hgs U4 and U5, but was genetically differentiated from aHG and aPWC due to the occurrence of hg C. Despite the fact that high frequencies of hgs U5b and V cluster the aHG and aPWC hunter-gatherer groups on the PCA plot (Figure 2), and that these hgs are also common in modern-day Saami, the ‘Saami motif’ is absent from aPWC and genetic continuity between aPWC and modern-day Saami was rejected [13].

Although the aBOO individuals were also characterized by high frequencies of hg U, the group appeared less close to the Palaeolithic/Mesolithic hunter-gatherers aHG and aPWC on the PCA plot than aUzPo. Haplotype sharing analyses (Figure 6) also showed that aBOO shared less haplotypes with aHG and aPWC than aUzPo (4.76% and 0.00%, respectively, versus 9.52% and 36.84%). This observation was confirmed by the analyses of our coalescent simulations, in which a model of genetic continuity between aHG, aPWC and aUzPo (ω = 9.91 E-1; H0d) was better supported than a model of genetic continuity between aHG, aPWC and aBOO (ω = 1.10 E-4; H0e). As demonstrated above, aBOO exhibited greater genetic affinities with extant populations of Siberia than aUzPo. Accordingly, aBOO shared more haplotypes with ancient samples from Siberia aEG (10.87% [55]) and aKUR (7.69% [56]) than aUzPo (0.00% and 7.69%, respectively; Figure 6).


Current distribution pattern of the Y-STR haplotypes found in the ancient Siberians under study. Each square represents a present-day individual sharing the same Y-haplotype of an ancient specimen.

To date, all studies on ancient Mesolithic/Palaeolithic hunter-gatherers from Europe have reported large proportions of hg U: 64% in aUzPo, 73% in aHG, 74% in aPWC; and hg U was also found in three out of five Mesolithic individuals of Spain [20], [57]. On the basis of the distribution of hg U5b, it was proposed that the Mesolithic population has remained genetically homogeneous over a wide geographical area and for a long period of time [57]. The new data from aUzPo suggests that hg U5a may be a representative of Central and North East Europe's Mesolithic mtDNA diversity, whereas elevated frequencies of hg U4 appear more characteristic of populations of the peri-Baltic area (aUzPo and aPWC). Haplogroup U also represents a significant genetic component of aBOO (35%), as well as Bronze Age Central Asians (14% in aKAZ; 2,700–3,400 yBP), and pre-Iron Age Siberians (54% in aKUR; Andronovo and Karasuk cultures; 2,800–3,800 yBP). Today, hg U is found in 7% of Europeans and displays a wide distribution in Europe, West Siberia, south west Asia, the Near East and North Africa [5]. Both the widespread distribution and high variability of hg U in extant and prehistoric populations are consistent with the description of hg U as one of the oldest hgs in Europe. On the basis of modern genetic data, hg U was proposed to have originated in the Near East and spread throughout Eurasia during the initial peopling by anatomically modern humans in the early Upper Palaeolithic (around 45,000 yBP, [5]). It is then plausible that hg U constituted the major part of the Palaeolithic/Mesolithic mtDNA substratum from Southern, Central and North East Europe to Central Siberia. It can also be suggested that the Palaeolithic/Mesolithic mtDNA substratum has been preserved longer in NEE than in Central and southern parts of Europe, where new lineages arrived with incoming farmers during the Neolithisation from the Near East [16]. This is supported by ancient genomic data obtained from hunter-gatherers of Scandinavia [58] and Spain [57], that shows a genetic affinity between Mesolithic individuals and present-day northern Europeans and supports genetic discontinuity between Mesolithic and Neolithic populations of Europe.

The genetic links between the sample populations of aUzPo/aBOO and the extant populations of Siberia follow a general pattern discussed for the early and mid-Holocene (6,000–10,000 yBP). Facilitated by the East-West extension of vegetation zones between the Russian Far East and Eastern Europe [65], long-distance contacts and connections across Eurasia have been proposed for a number of cases. For example, the North East and East European hunter-gatherer pottery is thought to have originated in the early ceramic traditions of the Russian Far East and Siberia [66]–[68]. An eastern Asian origin followed by a westward expansion was also discussed for domesticated broomcorn millet (Panicum miliaceum L.) [69]. While the exact scenario behind these two examples of long-distance connections is unclear, migrations are a common interpretative model for evidence from later periods [70]. In any case, long-distance connections across Eurasia are not unusual. A later migration from the East was associated with the spread of the Imiyakhtakhskaya culture from Yakutia (East Siberia) through northwestern Siberia to the Kola Peninsula during the Early Metal Age (3,000–4,000 yBP, [24]). Interestingly, one individual of the aBOO site (grave 10, not sampled for aDNA here) was archaeologically associated with this culture, but its cultural relationships to other individuals of the same site remain unclear.

Der Sarkissian C, Balanovsky O, Brandt G, Khartanovich V, Buzhilova A, Koshel S, et al. (2013) Ancient DNA Reveals Prehistoric Gene-Flow from Siberia in the Complex Human Population History of North East Europe. PLoS Genet 9(2): e1003296. doi:10.1371/journal.pgen.1003296

Figure 3: Bayesian Skyline Plots of Haplogroups U7, U7a and U7b.

Central Asia has four regionally specific clades (U7a12–15), whilst U7a11 is shared with South Asia (Fig. 1B and Supplementary Figure S1). U7 is distributed unevenly in Central Asia; it is most frequent in its southern areas adjacent to the Near East and South Asia (Fig. 2), with Afghanistan forming a “buffer zone”. Despite this geographical proximity, there are very few instances of shared lineages among the three regions, which, combined with the early coalescence date for U7a12 (~12 kya) (Supplementary Table S4), is consistent with a regional differentiation prior to the Holocene.

In contrast to U7a, U7b shows signs of a significantly (t-test p < 0.001) later expansion and is characterized by low frequencies in the Near East, South Asia, and Central Asia, while it has a higher frequency in Europe (Table 1, Supplementary Tables S3 and S4). This differentiation is also reflected in the number of U7b subclades that are restricted to Europe – four out of nine subclades identified in the current phylogeny (Fig. 1C and Supplementary Figure S1). In addition, many single lineages (eight out of eighteen) in U7b are from Europe. The major sub-branches of U7b are characterized by star-like radiations and growth ~8–5 kya (Fig. 3). Subclades U7b1c and U7b1d, which are exclusive to Europe, expanded ~5 kya (Supplementary Figure S1). Hence, we consider this time as a minimum age for the presence of U7b in Europe. Taking into account the U7b coalescence age in Europe (Table 1), we think that U7b may have appeared there between 5 and 10 kya. This timeframe overlaps significantly with the time of the Neolithic demographic transition in Europe.



Expansions within this timeframe are also observed for the European-specific clades U7a17 and U7a19, whose distributions are centred on Mediterranean and Southeast Europe, along one of the preferred routes for the initial dispersal of farming46,47,48,49. Elevated frequencies in the Mediterranean area are also witnessed for many subsets of U7b (Fig. 2C), and the age of U7b in Europe (5–10 kya) is incompatible with its presence there prior to the Holocene. To date, aDNA studies have not found any example of U7 in either Neolithic or pre-Neolithic contexts. In contrast, other clades of hg U were common during the postglacial re-expansion period, including U8a, which is extremely rare today24. However, the number of analysed ancient samples from the Mediterranean area, where U7b has elevated frequencies today, is still rather small.

The reduction in frequency of U7 in Europe from south to north is mirrored by the main components of hg K (a sister clade of U8b1). These have also been argued to have arrived into Europe during the early Neolithic from the Near East2,59,60,61, and display a clear northward frequency cline23,62. According to aDNA evidence, Neolithic populations in Europe display a distinct mtDNA lineage make-up, argued to be derived from Near Eastern sources. This early colonisation was probably followed by a complex process of assimilation of autochthonous hunter-gatherer diversity, seen most clearly in the autosomes. Notably, the distribution of nuclear genetic variants from Neolithic migrants among modern-day European populations3,55,64,65,66,67,68,69,70,71 resembles the phylogeography of hg U7 in Europe today.