ISSN 1022-7954, Russian Journal of Genetics, 2018, Vol. 54, No. 6, pp. 717–731. © Pleiades Publishing, Inc., 2018. Original Russian Text © M.A. Gubina, V.N. Babenko, M.I. Voevoda, 2018, published in Genetika, 2018, Vol. 54, No. 6, pp. 694–709.
HUMAN GENETICS
Polymorphism of Mitochondrial DNA in Population of Siberian Tatars from Barabinsk Forest Steppe M. A. Gubinaa, *, V. N. Babenkoa, and M. I. Voevodaa, b a
Federal Research Center Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences, Novosibirsk, 630090 Russia b Institute of Internal and Preventive Medicine, Siberian Branch, Russian Academy of Sciences, Novosibirsk, 630099 Russia *e-mail:
[email protected] Received June 29, 2017; in final form, September 17, 2017
Abstract⎯The analysis of mtDNA polymorphism was carried out in the population of Siberian Tatars from the Barabinsk forest steppe living on the territory of Novosibirsk oblast (N = 199). As a result of the analysis of HVS I and HVS II nucleotide sequence, 101 haplotypes that refer to 22 mtDNA haplogroups were detected. The population of Baraba Tatars is represented by both East Eurasian (38.7%) and West Eurasian mtDNA lines (61.3%). H, T, U5, and J haplogroups prevail among West Eurasian haplogroups; C, D, G, M, and A haplogroups prevail among East Eurasian ones. According to the index of genetic diversity, Tatars from the Barabinsk forest steppe (0.9141) are the closest to Kazakhs (0.9108), Bashkirs (0.9165), and Tobol-Irtysh Tatars (0.9104). The greatest statistically significant interpopulation differences (FST) were detected between all studied samples; the smallest interpopulation differences were detected between all Tatar samples, as well as between Tatars and Komi, Mansi, Udmurts, Kazakhs, Chuvashes, and Bashkirs. The haplogroup H is the most common in populations that we studied. In the present study, was registered the haplotype 16126-16294 with the frequency of 4% (T cluster) previously found only in Caucasians. High frequency of haplogroups U4, U5, and H in the gene pool of Baraba Tatars brings them together not only with Samoyeds but also with Finno-Ugric populations. The highest intrapopulation genetic diversity was detected in Tatars from the Barabinsk forest steppe, Tobol-Irtysh Tatars, Kazakhs, and Bashkirs. The presence of the haplogroup B in the mitochondrial DNA genetic pool of Siberian Tatars brings them together with Turks that came from regions of Altai and Central Kazakhstan and inhabited the Western Siberian forest steppe in the 6th–9th centuries. The haplogroup U7, which is typical of populations of Jordan, Kuwait, Iran, and Saudi Arabia, could also have entered the territory of residence of Siberian Tatars in the middle of second millennium BC, when Iranian-speaking tribes entered Siberia. Keywords: population of Siberian Tatars, mitochondrial DNA, polymorphism, haplogroups, haplotypes DOI: 10.1134/S1022795418060066
INTRODUCTION The history of peoples of Western Siberia is traced to deep Neolithic antiquity. The population of any region develops to a large extent when it interacts with the nearest neighbors and often with the involvement of groups that are significantly remote geographically, but are involved in ethnogenesis by events of different nature: mass migration, interethnic relations, etc. [1]. The territories of the south of Western Siberia were from ancient times a zone of transgression of different population groups, including taiga West Siberian tribes and steppe nomads and members of traditional Siberian cultures and Central Asian state formations. As a result of such interactions, a Turkic-speaking ethnic community, Siberian Tatars, developed in the steppe and forest-steppe zones of medieval Western Siberia [2].
Siberian Tatars are a Turkic-speaking people occupying an extensive area of the steppe and forest-steppe zones of Siberia from the Urals to Altai. Owing to multiple contacts with different population groups, they are a suitable object for the study of genetic diversity and genetic history. Siberian Tatars came from medieval Kypchaks. They occupied a huge territory, and lived fairly disconnectedly. In the process of their ethnic development, they made contact with many peoples: the groups of Ugric origin, Samoyeds, Kets, peoples of the Altai-Sayan highland, Central Asia, and Kazakhstan [3]. Siberian Tatars consist of three ethnic groups: Tomsk, Baraba, and Tobol-Irtysh Tatars. Studies in which populations of Tobol-Irtysh Siberian Tatars were analyzed on the basis of classical genetic markers and mitochondrial DNA were conducted previously [4–6]. The gene pool of Yaskolbin TobolIrtysh Tatars was also studied according to the Y chro-
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mosome STR markers [7]. Therefore, the study of one more Siberian Tatar group—Baraba, is topical. MATERIALS AND METHODS Sample Collection and DNA Isolation DNA of Siberian Tatar members from the Barabinsk forest steppe residing in Tebisskoe, Belekhta, Koshkul’, and Tebis from Chanovsky district of Novosibirsk oblast, as well as Vorob’evo and Chargary from Vengerovsky district of Novosibirsk oblast, was the material for the study (Fig. 1). The sample of Baraba Tatars unrelated by maternal line was 199 individuals. After informed consent, blood samples were collected under sterile conditions from the ulnar vein in the members of Baraba Tatars (volunteers, adults and children over 10 years old) during the field work under the leadership of M.A. Gubina, senior researcher at the Institute of Cytology and Genetics (Siberian Branch, Russian Academy of Sciences). The ethnicity of individuals was established through questioning and additional cross-survey with the determination of the nationality of parents for at least three generations. Molecular Genetic Methods Total DNA was isolated from peripheral blood lymphocytes by a standard method of phenol-chloroform extraction using proteinase K [8].
mtDNA analysis. The analysis of nucleotide sequence of hypervariable segments I and II (HVS I, II) was performed in 199 individuals of Tatar ethnicity. Fragment of the mtDNA HVS I and II which corresponded to 15898–16 402 and 29–408 bp, respectively, according to Andrew’s numeration [9] were amplified by PCR method with oligonucleotide primers [9]. After electrophoresis of the PCR products and reprecipitation, direct sequencing was performed according to Sanger’s method. Mutations were detected by a method of comparison with the Cambridge reference sequence [9]. Haplogroups were determined by means of analysis of diagnostic restriction sites (RFLP) typical of each of the groups [10– 17]. Statistical methods. Multidimensional scaling based on the frequencies of different haplotypes was calculated by means of the XLStat program (Addinsoft, Inc., 2011). Genetic diversity h was estimated as k ⎛ ⎞ h = [n (n − 1)] ⎜1 − pi2 ⎟ , i =1 ⎝ ⎠ where n is total number of sequences, k is the number of haplotypes, and pi is the frequency of haplotypes. Genetic differentiation between different populations and its statistical significance were estimated by means of FST statistics (Hg and HVS I). The statistical significance of interpopulation differences by the hap-
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logroup frequencies was calculated by means of the exact test of population differentiation (the number of Markov chain steps 10000, the significance level P = 0.001). The mean genetic diversity by loci was determined by the methods of Tajima (1993) and Nei (1987) [18, 19]. The calculations of the diversity indices were conducted using the Arlequin 3.01 program [20]. RESULTS AND DISCUSSION An analysis of the HVS I and HVS II nucleotide sequence, was detected of 101 mtDNA haplotypes. On the basis of the data obtained, 22 haplogroups were determined. The haplotypes and haplogroups, as well as the haplotype frequencies in the studied population, are given in Table 1. The population of Baraba Tatars is represented by both East Eurasian (A, B, C, D, G, Z, N9, M) and West Eurasian mtDNA haplogroups (H, HV, V, U1, U2, U4, U5, U7, K, R, T, N1, I, J). Haplogroups H (16.6%), T (14.6%), U5 (9.0%), and J (5.5%) prevail among West Eurasian haplogroups. Among East Eurasian are the most frequent haplogroups C (9.5%), D (10.1%), G (6.0%), M (4.5%), and A (4.5%). The frequency of other haplogroups varies in the range from 0.5 to 2%. On the Western Eurasian haplogroups accounted 61.3% and East Eurasian—38.7% of the total mitochondrial diversity (Table 2). The haplogroup H in the population of Baraba Tatars was detected with the frequency of 16.6% (Table 2). High frequencies of this haplogroup were found in Europe (approximately 40%), in the VolgaUral region, it reaches 42% in Mordovians and 40% in Maris [21–23]. In populations of East Slavs, the haplogroup H varies in the range from 33.3% in Russians from Ryazan oblast to 54.6% in Russians from Tula oblast [24, 25]. Its frequency in the Altai-Sayan region ranges from 2.8% in Tuvinians to 21.4% in Shorians [26, 27]. In the populations of the Far East (Koryaks, Eskimos and Yukagirs) haplogroup H was not detected [28]. Haplogroups T and J are rooted to the Middle East [29]. The frequency haplogroup T in Baraba Tatars is 14.6% (Table 2). A high frequency of this haplogroup was found in Old Believers of Tyumen oblast (19.2%) [30]. It is quite common in populations of Udmurts (14.9%) and Mordovians (7.9%) [23]. Among East Slavs, this haplogroup was detected with different frequency in the range from 2.1% in Yaroslavl to 19.4% in Vladimir [24]. The haplogroup T is found in populations of Southern and Eastern Siberia less often than in the population that we studied: it was not found in Todzhins and Yakuts and is the most common in Tofalars (5.2%) [31]. In the Altai-Sayan region, the lowest occurrence among the Altaians (1.6%), the highest among the Kazakhs (4.8%) [27]. This haplogroup was not found in peoples of the Far East [28]. RUSSIAN JOURNAL OF GENETICS
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In the studied population, the frequency of haplogroup J was 5.5%. (Table 2). In populations of the Volga-Ural region, its frequency varies from 2.0% in Udmurts to 7.8% in Mordovians [23]. It was detected with the frequency 8.6% in Tofalars [31]. This haplogroup frequency in Mansi is 12.2% [32]. The range of the frequency in the Altai-Sayan highlands is from 1.9% in Khakassians to 11.9% in Shorians [26]. In populations of East Slavs, the frequency varies from 2.6% in Russians from Vologda to 14.7% in Russians from Tver [25]. The Eskimos, Kets, Evenks, Tuvinians and Buryats did not have a haplogroup J [26, 28, 32]. Haplogroups of the cluster U are widespread in Europe. It is assumed that this cluster separated from the cluster R approximately 50000 years ago [33]. In the population of the Baraba Tatars, this cluster is represented by six haplogroups U1, U2, U4, U5, U7, K, and its frequency was 17.6%. The haplogroup U5 (9.0%) is the most common; it is represented by 11 haplotypes (Tables 1 and 2). This haplogroup is distributed with the highest frequency in Saami (53%), and it is also found in other Northern European populations [34]. It is quite common in the Volga-Ural region (from 8.9% in Udmurts to 15.7% in Mordovians) [23]. Among populations of the AltaiSayan region, the maximum frequency of this haplogroup was in Kazakhs (5.6%), while the minimum frequency was in Shorians (0.7%) [27]. In the population of East Slavs, the maximum frequency was registered in Novgorod (17.5%), while the minimum frequency was in Tambov (2.7%) [25]. Out of East Eurasian haplogroups, we detected haplogroups A, C, D, G, B, M, and Z. The haplogroup A is the most common among the peoples of Siberia and is rarely found or is absent in native peoples of Southeast Asia [35]. In the studied population, this haplogroup was detected at a frequency of 4.5%. High frequencies haplogroup A were previously registered in populations of Canadian and Asian Eskimos (100 and 85%, respectively) and in Chukchi, where its frequency varies from 41.5 to 68.2% (in different studies) [28, 36]. It is rare in the Volga-Ural region; the maximum frequency was found in Bashkirs (3.6%) [23]. Among East Slavs, this haplogroup was found only in four populations, its frequency ranges from 0.4% in Russians from Novosibirsk to 3.2% in Russians from Smolensk [25, 30]. The haplogroup C in Baraba Tatars was detected with the frequency 9.5%. According to the published data, the highest frequency haplogroup C (more than 50%) was detected in Yukagirs, Yakuts, Evenks, and Tofalars, while the minimum frequency was found in populations of the Volga-Ural region (0.7–3%) [23, 37–40]. In the population of Finno-Ugrians, this haplogroup was found in Mansi (17.3%) [27]. In the AltaiSayan highlands, the frequency varies from 5.6% in Kazakhs to 38% in Tuvinians [32]. This haplogroup was not detected in most East Slav populations, 2018
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Table 1. mtDNA HVS I and HVS II haplotypes in populations of Siberian Tatars from the Barabinsk forest steppe No. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45
Haplogroup A A A A6 B4 B4 B5 C C C C C4a2a1 C5b1 D D D4b1 D4b1 D4e5 D4h1 D4o1 G1a1 H H H H H H3b H1a H9a H20 H13a1d H7a1 H24 H5 H6 H H5a4 H1b1 H11a1 H11a1 H11a2a2 H11a2a2 H11a2a2 HV HV0
Haplotype (HVS I)
Haplotype (HVS II)
129-140-223-290-319-362 129-140-223-290-319-362 192-223-290-319-362 189-223-290-319-356-362 150-186-189-217-234 150-186-189-217-234 129-140-183-189-217-335 223-298-327 223-298-327 223-298-327 223-298-327 86-171-223-298-327-344-357 148-223-288-298-327 223-362 223-254-295-362 108-223-319-362 223-319-362 209-223-274-362 174-223-362 176-183-223-274-290-319-342-362 129-223-325-362-365 CRS CRS CRS CRS CRS 129 162 168 218 234 261 293 304 362 093-209 294-304 189-356-362 189-293-311 278-293-311 140-265-293-311 140-265-293-311 092-140-265-293-311 093-244-311 298
073-146-152-235-263 063-146-152-235-263 073-152-235-263 073-151-263 073-151-197-263 073-150-195-263 073-151-152-249d-263 073-151-152-263 073-249d-263 073-263 073-195-249d-263 064-073-249d-263 073-263 073-146-199-263 073-263 073-263 073-263 073-263 073-195-263 073-150-263 263 199-263 152-263 073-263 263 073-263 152-263 093-263 152-263 263 263 239-263 152-263 263 263 195-263 146-195-263 073-152-229-263 195 195-263 263 072-263
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Frequency Sample size 1.5 0.5 2.0 0.5 0.5 0.5 0.5 1.5 1.5 2.5 0.5 1.0 2.5 0.5 1.5 0.5 5.0 0.5 1.0 1.0 6.0 1.5 0.5 0.50 1.0 0.5 1.0 1.0 0.5 1.5 1.5 0.5 0.5 0.5 1.0 0.5 0.5 0.5 1.0 0.5 0.5 0.5 0.5 0.5 1.5 Vol. 54
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Table 1. (Contd.) No. 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90
Haplogroup HV6 HV9b I1a I1a J J J1c2 J1c2 J J1c3f J1c2i J1b1a1 J1b1a1 K1c M10a2 M7b1a1 M7b1a1 M7b1a1 N1a3a N9a1 R2 T T T T T2b T2b T2b T2i T2 T1a1'3 T1a1'3 T1a1'3 U1 U1a2 U1b U2d U2d U4 U4 U4a1 U4a1 U4c2 U5 U5a1
Haplotype (HVS I)
Haplotype (HVS II)
172-311 249-311 129-172-223-311-391 129-172-223-311-391 126 69-126 126-235 69-126-235 63-69-126 63-69-126-149 69-126-147-242 69-126-172-222-261 69-126-145-172-222-261 179-224-311 66-86-92-223-311 93-129-192-223-297 93-129-192-223-297-309 129-192-223-297-309 201-223-265 111-129-223-257C/A-261 37-71-172 126-294 126-294 126-294 126-294 126-294-304 126-294-296-304 126-271-294-296-304 126-294-296-362 126-209-294-296 126-186-189-261-294 126-163-186-189-261-294 126-163-186-189-261-294 192-249-311 108-129-162-172-189-249-288-362 111-214C/A-249-327 129-183A/C-189-234-294 129-183A/C-189-234-294 356 356 134-356 134-356 261-356 270 256-270
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263 263 073-146-151-152-263 073-199-202-203-204-250-263 073-228-263 073-185-263-295 073-185-188-228-263 073-95C-185-188-228-263 073-185-263-295 073-185-263 073-185-188-228-263 073-185-242-263 073-185-242-263 073-146-152-263 073-152-263 073-150-199-263 073-150-199-263 073-150-199-263 073-189-195-204-207-210-263 073-150-263 073-152-263 073-194-200-263 073-152-194-200-263 073-195-263 073-263 073-263 073-263 073-263 263 073-152-195-263 073-152-195-263 073-195-221-263 073-150-263 073-263 073-146-263 073-195-263 073-152-199 073-195-215-263 073-195-263 073-152-195-263 073-152-195-198-263 073-195-263 073-263 073-263 2018
Frequency Sample size 1.0 0.5 0.5 1.0 0.5 0.5 0.5 0.5 1.0 0.5 0.5 0.5 1.0 1.5 3.0 0.5 0.5 0.5 0.5 1.5 2.0 2.5 0.5 0.5 0.5 1.0 0.5 0.5 1.5 0.5 1.0 5.0 0.5 0.5 0.5 0.5 0.5 0.5 1.5 0.5 0.5 0.5 1.0 0.5 1.0
2 1 1 2 1 1 1 1 2 1 1 1 2 3 6 1 1 1 1 3 4 5 1 1 1 2 1 1 3 1 2 10 1 1 1 1 1 1 3 1 1 1 2 1 2
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Table 1. (Contd.) No.
Haplogroup
Haplotype (HVS I)
Haplotype (HVS II)
Frequency Sample size
91
U5b1a
189-192-270
073-150-217-263
0.5
1
92 93 94 95 96 97 98 99 100 101
U5b1a U5b1d2 U5a2a U5a2a U5b1a U5b U5b U5b1 U7 Z
183-189-270-294 86-192-239-270 114A-192-256-270-294 114A-192-256-270-294 92-183C-189-270-294 241-270-287-304-325 241-256-270-287-304-325 92-183-189-270-294 309-318A/T 223-224-260-298-327
073-150-152-263 073-150-263 073-263 064-073-263 073-150-152-263 073-263 073-263 073-150-152-263 073-151-152-263 073-146-152-263
0.5 0.5 2.0 0.5 0.5 0.5 1.5 1.0 0.5 0.5
1 1 4 1 1 1 3 2 1 1 199 h = 0.988
The variants of positions are demonstrated from rCRS [9] minus 16000 for HVS I.
among those where it was found, the maximum frequency was 2.9% in Russians from Tver [25]. The frequency haplogroup D in the studied population is 10.1% (Table 2). In Central Asia, this haplogroup is the second most prevalent after H [41]. A high frequency was registered in Oroks (68.9%) [42]. It is widely represented in populations of the Altai-Sayan highlands (from 6.4% in Khakassians to 50% in Soyots) [27, 31]. It is rare in peoples of the Volga-Ural region (from 1% in Mordovians to 3.6% in Chuvashes), except for Bashkirs (9%) and Udmurts (11.9%) [23]. Among Russians, its maximal frequency is 2.6% in Vologda, this haplogroup was not detected in most East Slav populations [25]. The frequency haplogroup G in Baraba Tatars is 6.0%. This haplogroup is most common in Koryaks (41.9–43.4%) [28, 43]. Its frequency in Todzhins is 18.8% [44]. It is rare in populations of the Altai-Sayan highlands, its highest frequency was registered in Tuvinians (5.6%) [26]. In peoples of the Volga-Ural region, it was registered in the range from 1.6% in Komi-Zyrian to 4.5% in Bashkirs. This haplogroup was not found in Chuvashes, Mordovians, Maris, and Udmurts [23]. Thus, on the basis of the data obtained, it is possible to make a conclusion about the multicomponent mitochondrial genome of the studied population, in which complex ways of ethnogenesis are reflected. The presence of Mongoloid haplogroups A, B, C, D, F, G, M, Y, Z in the genetic pool of the mtDNA of the Barabinsk Tatars with the predominance of only five is A, C, D, M and G brings this sample closer to other Siberian populations. Among West Eurasian haplogroups, we detected H, HV, V, U1, U2, U4, U5, U7, K, R, T, N1, I, and J. Haplogroups H, T, and U5 were found the most fre-
quently. The haplogroup H is the most widespread in populations that we studied (Table 1). The haplotype with CRS sequence is the most frequent haplotype; its frequency is 48% from the whole variety of this haplogroup. The haplogroup T is the next most prevalent. The presence of the haplogroup U5 (9.0%) in mitochondrial genome of Baraba Tatars brings them together with North European populations. It should be noted that the so-called Saami motif was not found in our sample [34]. Comparative Analysis of Four Studied Tatar Samples Previously, studies on Tobol-Irtysh, Belarusian, and Volga-Ural Tatars were conducted [6, 23, 45]. As well as in the population we studied, in all three samples were identified as the Eastern and Western Eurasian haplogroups (Table 2). Twenty-three haplogroups (7 East and 16 West Eurasian) were detected in the sample of Tobol-Irtysh Tatars; 23 haplogroups (6 East and 17 West Eurasian), in Tatars from the Volga-Ural region; and 11 haplogroups (3 East and 8 West Eurasian), in Belarusian Tatars [6, 23, 45]. In the sample of Baraba Tatars, nine haplogroups (H, T, U5, J, C, D, G, M, A) (80.4%) are common, in Tobol-Irtysh Tatars, four are common (C, H, T, and U4) (52.7%), in Volga-Ural Tatars, H, J, T, U4, and U5 (64.9%), in Belarusian Tatars, D, G, and H (73.9%) (Table 2) [6, 23, 45]. A high frequency haplogroup H (from 16.6% in Baraba to 46.3% in Belarusian) is typical of all four samples. The median network of haplotypes of haplogroup H in the four studied Tatar samples is presented in Fig. 2. A high frequency of two East Eurasian haplogroups in Belarusian Tatars (G (13.8%) and D (13.8%)) attracts attention, despite the fact that this sample is almost 2.5 times smaller than the rest [44]. The haplogroup G is represented by only one haplotype in the sample of
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Table 2. Frequency of haplogroups (%) in four Tatar samples Baraba
Tobol-Irtysh*
Belarusian**
Volga-Ural ***
(N = 199)
(N = 218)
(N = 80)
(N = 227)
4.5 1.5 9.5 10.1 0.0 6.0 16.6 3.5 1.5 5.5 1.5 4.5 0.5 1.5 1.5 2.0 14.6 0.0 1.5 1.0 0.0 4.0 9.0 0.5 0.0 0.0 0.0 0.0 0.0 0.5
1.8 6.9 13.3 6.9 5.0 0.5 17.4 0.0 0.5 2.8 1.8 4.6 1.8 0.9 0.0 0.0 9.2 0.5 3.7 0.5 0.5 12.8 5.0 2.8 0.0 0.5 0.5 0.0 0.0 0.0
0.0 0.0 5.0 13.8 0.0 13.8 46.3 5.0 0.0 1.3 1.3 0.0 0.0 0.0 0.0 0.0 3.8 0.0 0.0 0.0 0.0 1.3 3.8 0.0 0.0 0.0 5.0 0.0 0.0 0.0
3.1 0.0 1.8 2.6 0.0 1.8 30.7 0.9 0.9 7.5 5.7 2.2 0.0 2.2 0.9 0.4 9.2 2.2 0.9 0.9 2.2 7.0 10.5 0.0 0.0 3.9 1.8 0.0 0.0 0.4
Haplogroup A B C D F G H HV I J K M N N1 N9 R T U U1 U2 U3 U4 U5 U7 U8 V W X Y Z * [6]. ** [45]. *** [23].
Belarusian Tatars, and its frequency was 13.8%. It should be noted that the haplotype detected in Belarusian Tatars is a derived variant of the haplotype detected in Volga-Ural Tatars [6, 23, 45]. This haplogroup is represented by two haplotypes (6.0%) in Baraba Tatars, while it is represented by one haplotype (0.5%) in Tobol-Irtysh Tatars (Table 2) [6, 23, 45] (Fig. 3). The haplogroup D is the second most common after H in Central Asia; it is represented by seven haplotypes (10.1%) in Baraba Tatars, ten haplotypes (6.9%) in Tobol-Irtysh Tatars, four (2.6%) in VolgaUral Tatars, and four (13.8%) in Belarusian Tatars (Table 2) [6, 23, 45]. Only one common haplotype RUSSIAN JOURNAL OF GENETICS
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(223-362) was detected in all four samples, and its frequency varies from 0.5% in Baraba to 1.4% in TobolIrtysh Tatars [6, 23, 45] (Fig. 3). The median network of the cluster U haplotypes is presented in Fig. 4. Only two haplogroups (U4 and U5) are the most common. Only one haplotype with a single substitution in the position 16356 is common for the haplogroup U4. The haplotype 134-356 was detected in three samples; the sample of Belarusian Tatars was an exception. Despite the fact that the frequency of haplogroup U5 in three samples of Tatars (Baraba, Belarusian, and Volga-Ural) is higher than U4, but also the haplotypes found in 2 times more. It should be noted that we have not found a single hap2018
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L3
10873
1V 1Т
1V 16311
16239 2B 16145 1B 16222
N
1BL 16223 1V 16231
12705
16172 1V 16261
1V
J
16291 16290 16243 1B 1B 16145 16242 16147 16235 1B 1Т 16069 9V 16063 1B 16126 13704 2B 16092 16193 1V 16126 16149 13366 1V 1V 1B 16301 1V 1Т 1V 2V 16192 16177 16294 16172 2Т 16324 1Т 16069G 1Т 2B 11719 16269 1Т 16304 8B 16092 1B 3Т1V 3Т 1V 16186 1Т 16069 5V 16189 16263 1Т 16271 14766 16093 1Т1B 16296 16111 16261 2Т 16292 16296 4V 16324 2B 11B 00073A 4Т 1BL 1V 16078 16086A 4Т 16228 16171 16184 1V 1V 1636216209 1Т 1Т 2BL 7028 3B 1V 1V 1B1Т 1V 1Т 1Т 1V 16311 16111A 1V 1B 16111 16278 16192 16184 1V 1Т 1Т 1V 16355 1B 2Т 16294 1V 16168 1Т 16387 10BL 16356 16299 1V 1V 16162 16031 1V 16274 16304 16319 2B 16295 3B 16162 16240C 16218 25V 16209 1B 8B 18Т 16093 1V 16272 1B 16293 13BL 16311 2V 16189 16259 16169 1V 16234 3B 16354 1Т 2V 16362 16278 1V 16184 16356 7Т 8V 2B 16293 2V 16367C 6BL 16080 1V 5Т 1Т 7BL 16261 16124 1B 1B 1V 16246 16300 16189 1BL 1B 1V 16325 16344 16140 16082 2B 1V 16129 1V 16093 16265 1B 1V 1V 2B 16294
R
T
H
16092 1B
16365 1V
Fig. 2. Median network of haplogroups H, J, T in four Tatar samples: Baraba—present study, Belarusian—[45], Tobol-Irtysh— [6], Volga-Ural—[23]. For Figs. 2–4: digits and letters in circles designate the number of individuals in the population having this haplotype; restriction diagnostic sites of mtDNA coding region for each cluster are indicated in italics. B, Baraba Tatars; T, Tobol-Irtysh; V, Volga-Ural; BL, Belarusian. RUSSIAN JOURNAL OF GENETICS
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С4а2а1
2B
2B
С
16357
С5b1
4BL
16344
16129 1T
5B 15T
1T
10B
1T
12B 6Т 4V
16311
16288
16309
M7
6T 16390
1T
16295
16254
13263 16192
M
16311
16093
16086 16092
L3
6B
1B3T 2V6BL
16209
D
16234
1T 16245 1V
16316 16192 16278 16227
3T 16358
1T
16129
16339 1T
1V
16147
16126 16391
M*
1V
16066
M10а2
3T
16298 16297
16357 16266 16172 16129
16153
1V
16129
16093
1B
2B
1T 16368
16262 16368 1T 5178 16254 16092 16294 16192 3BL 16295 1T 16362 16111 3B 16332 16213 16274
1B
1BL
16174 16311
16261
16327
16278 16311
16111 16171
16319
16093 1B
1B
16176 16173 16108
16180
16148 16288 16329
16203
1B 1T
2T
2T
M7b1а1
16171 16086
1BL
2V 2T 16129 16172 16215 1V
16342 16290 16274 16183
725
1T
10400 1B 16356 16189
10873
12327
N
16290
00663
16242 16187
16261 16129
16111
16319
16129
16362
16140
16192
16257A
N9a 3B
5417
A
1V
16311
16293С 16266 16227
F1b
4B
16220 4B
1T
1T
1Т
1Т 16227С
16298 3Т
16230
1V
16293 16203T
2Т
5Т
16172
16182C 5Т
F1a
1Т
16274
B4
16213
16183C
223
16388С
1Т
16249
6Т
16188
1B 16182С
16183d
16162 16309
12705
1Т 16261
16166 16051
1Т
16234
16140 16129
16189
16150 16304
16217
1 16234 6140
1Т
16399
16311
16186
16183С
16335
16172
3B
16232A
16111
16189
12406 249del 9bpdel
16243
R
B5 Fig. 3. Median network of East Eurasian haplogroups in four Tatar samples: Baraba—present study, Belarusian—[45], TobolIrtysh—[6], Volga-Ural—[23].
lotype haplogroup the U4, which have been identified in all four samples. The presence of haplogroups B and U7 is a distinctive feature of Siberian Tatars (Table 2) [6]. Previously, the haplogroup B was detected in the south of Siberia RUSSIAN JOURNAL OF GENETICS
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and with a high frequency in Mongolia (48%) [46, 47]. It was considered that ancestral population of all these peoples gave rise to the spread of the haplogroup B in indigenous inhabitants of the American continent. The presence of this haplogroup in the samples of 2018
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L3 10400
1V
M 1V
10873
3В 3V
U5a2а
1Т
N U5a1
16284 1Т
16278 16093
12705
1Т
R
1B
16368
2V
16223
1Т
3Т, 6V 1BL
U7
16179
16318T
16311
16256
1Т
1Т 2V
1Т 1Т 5B 1V
1V
16311 16294
16390
11467
2Т 1V
11299
1V 16234
1V
1B,4Т
12308
16325 1BL
14798
16189
14167
16287
16278
16309
3480
12372 1189
16318T
6V 16294 16304 16192 16362 2Т 16239 2B 3V 16291 2Т
1V
U
10398
10084 9056
3197
U5a
1811 9696
16256
U5b1b
16209
U5
14182
5656
16144
12618 10927 16189 1V 16183С
16145
16362 16294 1Т 1B 1V 16092 3B
2V 16390 1Т
16173
16260 16365
16086
16234 16217
2BL 2V
U5b1a
1V
16232
6047 16249 1B, 2V 14620 16270 16129 16214А 16327 16129C 16111 15693 16327 16183C 1Т 16260 16311 16287 16234 1V 4990 16355G 3Т 16134 1B 16294 16356 16356 16189 16304 1V 1Т 16051 3Т 4B, 7Т 2B 1Т 2V 7V, 1BL 16108 16259А 1Т 16261 16129 16189 2B, 11Т 16311 16162 2V 16387С 16239 1B 16261 16111 16172 2Т 16093 16362 1Т 16187 16288 16209 2B, 1Т 16362 16264 16228 1V 16163 16169 1B 16248 1Т 1Т 1Т 16113С 1Т 16248
U2e
16192 1B
16168 1V
16189
U2
U5b1
2Т
U3
U1b
U1
U5b
2BL
16343 13104 4646 14070 5999
16051
1B 7768
1V
9477
14793 13617 16270
3B
16224
16241
2Т
16261
16093
3B
16257
16114А 16291
K
16189 16086
U1a
U2d
U4с2
1Т
U4
U4a1
U1a2
16288 4V
Fig. 4. Median network of cluster U in four Tatar samples: Baraba—present study, Belarusian—[45], Tobol-Irtysh—[6], VolgaUral—[23].
Tatars from the Barabinsk forest steppe and TobolIrtysh Tatars brings them closer to the Turkic groups of Siberia and Central Asia. The haplogroup U7 was found in studied groups with a low frequency: 0.5% in Baraba Tatars and 2.8% in Tobol-Irtysh Tatars (Table 2). This haplogroup is typical of the populations of Jordan, Kuwait, Iran, and Saudi Arabia [33, 48].
Data on the index of intrapopulation genetic diversity are given in Table 3. As can be seen there, the lowest intrapopulation differences were detected in the populations of Tofalars and Yukagirs, while the highest differences were found in Tatars from the Barabinsk forest steppe, Tobol-Irtysh Tatars, Kazakhs, and Bashkirs.
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Table 3. Index of intrapopulation genetic diversity in studied populations Population Belarusian Tatars Baraba Tatars Tobol-Irtysh Tatars Volga-Ural Tatars Tuvinians Altaians Russians from Novosibirsk Nivkhs Komi Chukchi Koryaks Kazakhs Shorians Chuvashes Nanais Mansi Mordovians Yakuts Tofalars Bashkirs Maris Buryats Udmurts Kets Khakassians Nganasans Todzhins Yukagirs Evenks
Genetic diversity of sample*
Average number of pairwise differences**
Average genetic diversity of loci**
0.7468 ± 0.0427 0.9141 ± 0.0075 0.9104 ± 0.0075 0.8686 ± 0.0159 0.7064 ± 0.0443 0.8697 ± 0.0135 0.7850 ± 0.0211 0.7426 ± 0.0859 0.8362 ± 0.0212 0.7236 ± 0.0193 0.7222 ± 0.0330 0.9108 ± 0.0125 0.8120 ± 0.0247 0.8747 ± 0.0268 0.8558 ± 0.0202 0.8950 ± 0.0114 0.7810 ± 0.0341 0.7120 ± 0.0434 0.5890 ± 0.0734 0.9165 ± 0.0063 0.7898 ± 0.0275 0.7799 ± 0.0262 0.8622 ± 0.0164 0.8350 ± 0.0328 0.8042 ± 0.0213 0.7628 ± 0.0463 0.7010 ± 0.0630 0.5984 ± 0.0626 0.6486 ± 0.0623
1.493671 ± 0.910985 1.828131 ± 1.056118 1.820826 ± 1.052470 1.737242 ± 1.014857 1.412859 ± 0.873327 1.739394 ± 1.020514 1.569930 ± 0.938947 1.485294 ± 0.943075 1.672331 ± 0.988076 1.447178 ± 0.885162 1.444306 ± 0.889699 1.821541 ± 1.054516 1.624023 ± 0.966131 1.749495 ± 1.032041 1.711628 ± 1.009344 1.790027 ± 1.043498 1.562027 ± 0.940081 1.424077 ± 0.882561 1.177945 ± 0.768327 1.832935 ± 1.057869 1.579521 ± 0.946114 1.559755 ± 0.940158 1.724356 ± 1.013649 1.669986 ± 1.002673 1.608343 ± 0.957630 1.525692 ± 0.949867 1.402020 ± 0.876000 1.196744 ± 0.775470 1.297297 ± 0.830110
0.046677 ± 0.031547 0.057129 ± 0.036521 0.056901 ± 0.036392 0.054289 ± 0.035090 0.044152 ± 0.030237 0.054356 ± 0.035323 0.049060 ± 0.032461 0.046415 ± 0.032982 0.052260 ± 0.034183 0.045224 ± 0.030616 0.045135 ± 0.030820 0.056923 ± 0.036476 0.050751 ± 0.033422 0.054672 ± 0.035778 0.053488 ± 0.034947 0.055938 ± 0.036119 0.048813 ± 0.032537 0.044502 ± 0.030590 0.036811 ± 0.026633 0.057279 ± 0.036578 0.049360 ± 0.032731 0.048742 ± 0.032549 0.053886 ± 0.035084 0.052187 ± 0.034817 0.050261 ± 0.033117 0.047678 ± 0.033104 0.043813 ± 0.030393 0.037398 ± 0.026866 0.040541 ± 0.028825
Belarusian Tatars—[45]; Tobol-Irtysh Tatars—[6]; Volga-Ural Tatars, Bashkirs, Chuvashes, Mordovians, Maris, Udmurts, Komi— [23]; Russians from Novosibirsk—[30]; Koryaks, Chukchi, Nanais, Nivkhs, Yukagirs, Evenks—[28]; Tuvinians, Khakassians, Altaians, Kazakhs, Shorians—[27]; Tofalars, Todzhins, Buryats, Yakuts—[31]; Kets, Nganasans—[32]; Mansi—[50]. * [19]. ** [18].
Statistically significant interpopulation differences (FST) given in Table 4 demonstrate that the greatest differences were detected between all studied samples. The smallest interpopulation differences were detected between all Tatar samples, as well as between Tatars and Komi, Mansi, Udmurts, Kazakhs, Chuvashes, and Bashkirs (Table 4). The results of multidimensional scaling of pairwise genetic differences of East and West Eurasian mtDNA haplotypes in some populations (Fig. 2) are presented in Fig. 5. On the basis of the results of the analysis, Baraba Tatars are closest to Tobol-Irtysh Tatars, Bashkirs, and Mansi; this corresponds to data given in Table 4. RUSSIAN JOURNAL OF GENETICS
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Thus, our data confirm complex ways of historical development of not only Siberian Tatars from the Barabinsk forest steppe but also Tobol-Irtysh Tatars. The presence of the haplogroup B in the mitochondrial DNA genetic pool of Siberian Tatars brings them together with Turks that came from regions of Altai and Central Kazakhstan and inhabited the Western Siberian forest steppe in the 6th–9th centuries [49]. The haplogroup U7, which is typical of populations of Jordan, Kuwait, Iran, and Saudi Arabia [33, 48], could also have entered the territory of residence of Siberian Tatars in the middle of the second millennium BC, when Iranian-speaking tribes entered Siberia [49]. The high frequency of haplogroups U4, U5, and H 2018
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0 0.06 0.23 0.24 0.19 0.22 0.11 0.18 0.15 0.11 0.02 0.19 0.12 0.09 0.23 0.00 0.03 0.10 0.23 0.03 0.10 0.17 0.15 0.12 0.04 0.01 0.00 0.01 0.18
0 0.15 0.15 0.11 0.13 0.05 0.15 0.15 0.04 0.04 0.09 0.05 0.05 0.14 0.06 0.14 0.05 0.14 0.05 0.05 0.09 0.09 0.07 0.06 0.08 0.12 0.08 0.09
2
0 0.18 0.01 0.03 0.05 0.24 0.23 0.09 0.15 0.02 0.13 0.07 0.01 0.21 0.26 0.07 0.01 0.20 0.06 0.05 0.13 0.18 0.18 0.24 0.28 0.25 0.01
3
0 0.16 0.17 0.11 0.21 0.20 0.10 0.19 0.14 0.05 0.13 0.19 0.23 0.34 0.11 0.18 0.16 0.13 0.14 0.19 0.21 0.19 0.25 0.33 0.27 0.14
4
0 0.04 0.03 0.20 0.19 0.06 0.12 0.01 0.11 0.03 0.02 0.17 0.22 0.03 0.02 0.16 0.02 0.03 0.08 0.15 0.12 0.19 0.24 0.21 0.01
5
0 0.06 0.21 0.20 0.08 0.14 0.06 0.10 0.08 0.04 0.19 0.28 0.08 0.04 0.16 0.07 0.07 0.16 0.19 0.16 0.22 0.28 0.24 0.04
6
0 0.12 0.12 0.02 0.06 0.02 0.05 0.01 0.05 0.10 0.15 0.01 0.05 0.08 0.01 0.02 0.07 0.09 0.08 0.12 0.16 0.13 0.01
7
0 0.16 0.11 0.17 0.19 0.13 0.14 0.24 0.18 0.25 0.12 0.23 0.12 0.14 0.18 0.18 0.19 0.17 0.17 0.25 0.21 0.18
8
0 0.14 0.14 0.19 0.16 0.12 0.23 0.19 0.22 0.12 0.23 0.13 0.14 0.18 0.19 0.18 0.19 0.11 0.22 0.20 0.18
9
0 0.08 0.05 0.02 0.04 0.09 0.09 0.19 0.02 0.09 0.05 0.03 0.04 0.08 0.09 0.06 0.14 0.17 0.12 0.05
10
0 0.12 0.09 0.05 0.15 0.03 0.06 0.06 0.15 0.06 0.05 0.11 0.07 0.05 0.05 0.04 0.04 0.05 0.11
11
0 0.09 0.03 0.02 0.17 0.24 0.02 0.01 0.15 0.02 0.04 0.06 0.14 0.11 0.19 0.25 0.21 0.01
12
0 0.07 0.13 0.09 0.21 0.05 0.13 0.05 0.06 0.08 0.11 0.12 0.07 0.15 0.19 0.12 0.09
13
0 0.08 0.08 0.13 0.01 0.07 0.07 0.01 0.05 0.04 0.09 0.04 0.09 0.14 0.11 0.04
14
0 0.21 0.27 0.07 0.01 0.20 0.06 0.05 0.14 0.18 0.18 0.24 0.28 0.25 0.01
15
0 0.07 0.09 0.21 0.02 0.09 0.15 0.15 0.13 0.02 0.06 0.04 0.01 0.17
16
0 0.15 0.27 0.14 0.14 0.23 0.21 0.17 0.14 0.03 0.02 0.06 0.21
17
0 0.06 0.08 0.01 0.04 0.03 0.07 0.05 0.11 0.15 0.12 0.03
18
0 0.19 0.05 0.06 0.12 0.17 0.17 0.24 0.28 0.25 0.01
19
0 0.08 0.13 0.14 0.12 0.03 0.07 0.10 0.04 0.15
20
0 0.03 0.03 0.08 0.05 0.11 0.14 0.12 0.03
21
0 0.11 0.13 0.11 0.19 0.23 0.19 0.03
22
0 0.05 0.07 0.15 0.19 0.18 0.09
23
0 0.12 0.13 0.15 0.15 0.14
24
0 0.09 0.09 0.03 0.13
25
27
28
29
0 0.04 0 0.06 0.03 0 0.18 0.23 0.201 0
26
Belarusian Tatars—[45]; Tobol-Irtysh Tatars—[6]; Volga-Ural Tatars, Bashkirs, Chuvashes, Mordovians, Maris, Udmurts, Komi—[23]; Russians from Novosibirsk—[30]; Koryaks, Chukchi, Nanais, Nivkhs, Yukagirs, Evenks—[28]; Tuvinians, Khakassians, Altaians, Kazakhs, Shorians—[27]; Tofalars, Todzhins, Buryats, Yakuts—[31]; Kets, Nganasans—[32]; Mansi—[50]. 1—Tuvinians, 2—Altaians, 3—Russians from Novosibirsk, 4—Nivkhs, 5—Komi, 6—Belarusian Tatars, 7—Baraba Tatars, 8—Chukchi, 9—Koryaks, 10—Kazakhs, 11— Shorians, 12—Chuvashes, 13—Nanais, 14—Mansi, 15—Mordovians, 16—Yakuts, 17—Tofalars, 18—Bashkirs, 19—Maris, 20—Buryats, 21—Tobol-Irtysh Tatars, 22—Udmurts, 23— Kets, 24—Khakassians, 25—Nganasans, 26—Todzhins, 27—Yukagirs, 28—Evenks, 29—Volga-Ural Tatars.
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29
1
Table 4. Pairwise differentiation (FST) of interpopulation differences by haplogroup frequencies
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0.15 Tofalars Yukagirs
0.10 Evenks Tuvinians Yakuts Todzins
0.05
Kets
Nganasans Shorians Buryats
–0.15
Mansi Tatars 2 Bashkirs
Altaians
–0.10 Komi –0.05 0 Tatars 1 Chuvashes Mari Kazakhs Tatars 3 Russians* Udmurts Mordovians Nanais –0.05 Tatars 4
0.05
0.10
0.15
Khakassians
Koryaks
–0.10 Chukchi Nivkhs
–0.15
–0.20 Fig. 5. Pairwise differentiation (FST) of interpopulation differences by haplogroup frequencies. Belarusian Tatars—[45]; TobolIrtysh Tatars—[6]; Volga-Ural Tatars, Bashkirs, Chuvashes, Mordovians, Maris, Udmurts, Komi—[23]; Russians from Novosibirsk—[30]; Koryaks, Chukchi, Nanais, Nivkhs, Yukagirs, Evenks—[28]; Tuvinians, Khakassians, Altaians, Kazakhs, Shorians— [27]; Tofalars, Todzhins, Buryats, Yakuts—[31]; Kets, Nganasans—[32]; Mansi—[50]. Tatars 1, Baraba; Tatars 2, Tobol-Irtysh; Tatars 3, Volga-Ural; Tatars 4, Belarusian; Russians, Novosibirsk.
brings them together not only with Samoyeds but also with Finno-Ugric populations that inhabited the territory of Western Siberia in the Neolithic period [49]. ACKNOWLEDGMENTS This work was supported by the Russian Foundation for Basic Research (grant no. 14-06-00180a) and basic budgetary project no. 0324-2016-0002. REFERENCES 1. Chikisheva, T.A., Gubina, M.A., Kulikov, I.V., et al., Paleogenetic study of the ancient population of the mountainous Altai, Archeol., Ethnogr., Anthropol. Eurasia, 2007, vol. 4, pp. 130—142. 2. Genofond i genogeografiya narodonaseleniya (Gene Pool and Gene Geography of Population), vol. 2: Genogeograficheskii atlas naseleniya Rossii i sopredel’nykh stran (Gene Geographical Atlas of Population of Russia and Contiguous Countries), Rychkov, Yu.G., Ed., St. Petersburg: Nauka, 2003. RUSSIAN JOURNAL OF GENETICS
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3. Tomilov, N.A., Etnokul’turnye protsessy u tatar Zapadnoi Sibiri XVIII—XIX vv (Ethnocultural Processes among the Tatars of Western Siberia in the 18th— 19th Centuries), Omsk, 2011. 4. Rudenko, I.N., Dolinina, D.O., and Padyukova, A.D., Investigation of the genetic structure of the Tobol— Irtysh Siberian Tatar subpopulations, Materialy XXI Mezhdunarodnoi nauchnoi konferentsii studentov, aspirantov i molodykh uchenykh (Proceedings of the 21th International Scientific Conference of Students, Graduate Students and Young Scientists), Moscow: Moscow University, 2014. 5. Shneider, Yu.V., Grosheva, A.N., Evsyukov, A.N., and Zhukova, O.V., Polymorphism of immunogenetic and biochemical markers in Siberian (Tobol—Irtysh) Tatars, Russ. J. Genet., 2011, vol. 47, no. 12, pp. 1468— 1478. https://doi.org/10.1134/S1022795411120131. 6. Naumova, O.Iu., Rychkov, S.Iu., Morozova, I.Iu., et al., Mitochondrial DNA diversity in Siberian Tatars of the Tobol—Irtysh basin, Russ. J. Genet., 2008, vol. 44, no.2, pp. 215—226. 7. Padyukova, A.D., Lavryashina, M.B., and Ulyanova, M.V., Study of the gene pool of the Yaskolbinsky Tobol— 2018
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Translated by A. Barkhash
2018
