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Mitochondrial genome diversity in the Tubalar, Even, and Ulchi: contribution to

prehistory of native Siberians and their affinities to Native Americans

Article  in  American Journal of Physical Anthropology · May 2012

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 AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 148:123–138 (2012)
Mitochondrial Genome Diversity in the Tubalar, Even,
and Ulchi: Contribution to Prehistory of Native Siberians
and Their Affinities to Native Americans
Rem I. Sukernik,* Natalia V. Volodko, Ilya O. Mazunin, Nikolai P. Eltsov, Stanislav V. Dryomov,
and Elena B. Starikovskaya
Laboratory of Human Molecular Genetics, Institute of Molecular and Cellular Biology,
Siberian Branch of the Russian Academy of Sciences, Novosibirsk 630090
KEY WORDS mtDNA lineages; population/evolutionary history; native Siberia
ABSTRACT To fill remaining gaps in mitochondrial
DNA diversity in the least surveyed eastern and western
flanks of Siberia, 391 mtDNA samples (144 Tubalar from
Altai, 87 Even from northeastern Siberia, and 160 Ulchi
from the Russian Far East) were characterized via high-
resolution restriction fragment length polymorphism/sin-
gle nucleotide polymorphisms analysis. The subha-
plogroup structure was extended through complete
sequencing of 67 mtDNA samples selected from these
and other related native Siberians. Specifically, we have
focused on the evolutionary histories of the derivatives
of M and N haplogroups, putatively reflecting different
phases of settling Siberia by early modern humans. Pop-
ulation history and phylogeography of the resulting
mtDNA genomes, combined with those from previously
Studies on present day world populations, especially
those based on maternally inherited mitochondrial DNA
(mtDNA), suggest that modern humans expanded from
East Africa around 70 kya (1000 years ago). They dis-
persed along the Southwest-Southeast Asia shore and
reached the Siberian Pacific 38-37 kya (reviewed by
Pope and Terrel, 2007). In the other direction, archaic
cultures, including Neanderthal and previously
unknown hominin, who lived in Denisova Cave in Altai,
southwestern Siberia, around 40 kya, were replaced by
modern humans no later than 30 kya (Krause et al.,
2007, 2010b; Derevianko, 2011). During the last Ice Age
(43-12 kya), a special feature of Siberia has been its rel-
ative isolation from the rest of Eurasia and the New
World, making it a case study for understanding the
main pattern of cultural and biological adaptation and
subsequent dispersions to the New World. At the height
of last glacial maximum (LGM), the earliest Siberians
were largely confined to their strongholds, south of the
568N parallel, which were areas of continuous occupa-
tion (Finlanson and Cartion, 2007; Kuzmin, 2008; Graf,
2009).
Current distribution of maternal lineages across the
world indicates that Siberia lacks autochthonous M and
N lineages, the Eurasian descendants of African L3 that
are abundant along the proposed southern coastal
migration route (reviewed by Forster and Matsumura,
2005; Mellars, 2006). Many phylogenies across Siberia/
Beringia based on complete mtDNA sequences were
reconstructed and sequence-divergence estimates were
obtained (Derbeneva et al., 2002a; Starikovskaya et al.,
2005; Derenko et al., 2007; Perego et al., 2010; Volodko
C 2012
V WILEY PERIODICALS, INC.
published data sets, revealed a wide range of tribal- and
region-specific mtDNA haplotypes that emerged or diver-
sified in Siberia before or after the last glacial maxi-
mum, 18 kya. Spatial distribution and ages of the
‘‘east’’ and ‘‘west’’ Eurasian mtDNA haploclusters sug-
gest that anatomically modern humans that originally
colonized Altai derived from macrohaplogroup N and
came from Southwest Asia around 38,000 years ago. The
derivatives of macrohaplogroup M, which largely
emerged or diversified within the Russian Far East,
came along with subsequent migrations to West Siberia
millennia later. The last glacial maximum played a criti-
cal role in the timing and character of the settlement of
the Siberian subcontinent. Am J Phys Anthropol
148:123–138, 2012. V 2012 Wiley Periodicals, Inc.
C
et al., 2008). However, it is still not quite clear where in
the southern extent of Siberia the M and N offshoots
arose, when and how they spread over the higher lati-
tudes, setting the stage for colonization of the Americas.
As these and related studies have progressed, the Altai-
Sayan Mountain system, represented by the Tubalar,
immediate descendants of autochthonous hunters and
gatherers, emerged as a strategic area of very high rele-
vance to these issues. However, lack of entirely
sequenced mtDNA data precluded elucidation of Altaic
prehistory, potentially preserved in the intrinsic diver-
sity of mtDNA lineages. This is also true for the genetic
history of the Tungusic world (Pakendorf et al., 2007), in
East Siberia represented largely by the Evenki and
Even, the sparse groups of nomadic reindeer herders
and hunters, and the Ulchi, in recent traditional times a
Grant sponsor: Wenner-Gren Foundation for Anthropological
Research; WG Int. Res. Grant number: 65; Grant sponsor: Russian
Foundation for Basic Research; Grant number: 06-04-48182 and 09-
04-00183. Grant sponsor: Russian Foundation for Humanitarian
Research; Grant number: 08-01-0356.
*Correspondence to: Rem I. Sukernik, Prospekt Lavrentyeva 10,
Novosibirsk 630090.
E-mail: sukernik@mcb.nsc.ru, sukernik@gmail.com
Received 11 November 2011; accepted 13 February 2012
DOI 10.1002/ajpa.22050
Published online 4 April 2012 in Wiley Online Library
(wileyonlinelibrary.com).
124 R.I. SUKERNIK ET AL.
Fig. 1. Approximate location of Siberian populations analyzed for mtDNA variation.
well-defined tribe of hunters and fishermen dispersed
along the lakes and the reaches of the Lower Amur
(Starikovskaya et al., 2005).
In this study, we continued filling gaps in mtDNA
genome diversity, which remained poorly sampled in
aboriginal Siberian populations with long histories
preserved in remote ‘‘pockets’’ of the subcontinent. The
phylogeographic approach and the molecular time-
dependent clock principal have been applied to uncover
the geographic distribution of mtDNA lineages on the
tree, and antiquity of the lineages, especially those that
are restricted to a particular area (Soares et al., 2009;
2010). Newly obtained entire mtDNA sequences were
integrated with those previously published, and updated
age estimates were generated to add important details
into the prehistory of Native Siberians, and their affin-
ities to Native Americans.
MATERIALS AND METHODS
Populations and samples
Blood samples were collected from three well-defined
groups of indigenous Siberians with appropriate
informed consent during several expeditions conducted
by R.I.S., E.B.S., and N.V.V. in 2006-2009. The individu-
als who participated in this study were interviewed and
had their family histories verified by senior members of
the community for accuracy of the compiled genealogies
prior to blood being drawn only from unrelated subjects
who lacked non-native maternal ancestors. The sample
American Journal of Physical Anthropology
areas are shown in Figure 1, and a brief description of
each population follows.
Tubalar. The Tubalar are immediate descendants of
hunting-gathering bands, who for ages inhabited the co-
niferous forest (taiga) refuge in Altai-Sayan Mountains,
encompassing the northern coast of Lake Teletskoye, the
Upper Biya River and Isha River (the Upper Ob River
basin). On the northeastern border of their range, the
Tubalar were closely related to the Chelkan, similar
hunting-gathering tribe that dwindled during the last
decades. Because the Tubalar and Chelkan lived in geo-
graphic isolation in remote part of the Atai-Sayan, they
had retained their traditional way of life and tribal in-
tegrity until almost the middle of the 20th century
(Levin and Potapov, 1964; Potapov, 1972). The Tubalar
and Chelkan are grouped with northern Altaians, and
they differ from numerous southerners (Altai-kizhi or
Altai proper) in culture, language, and physical appear-
ance. Originally, northern Altaians spoke a dialect of the
Uralic language family, but later adopted a Turkic dia-
lect of the Altaic language (Radloff, 1883).
The present day Tubalar number 1,500 members and
the whole group is still subdivided into several exoga-
mous patriclans confined to their ancestral territory. Ve-
nous blood samples were drawn from elder people resid-
ing in a dozen of tiny villages: Urlu-Aspak, Paspaul,
Uimen, Kara-Koksha, Inyrga, Salganda, Tunzha, San-
kin-ail, Tuloi, Kebezen, Artybash, and Pyzha (Choisky
and Turochak districts, Altai Republic, Russian Federa-
tion). This report is based on the mtDNA genome diver-
sity of the 144 Tubalar samples. Previously published
 MITOCHONDRIAL GENOME DIVERSITY IN NATIVE SIBERIANS 125
TABLE 1. mtDNA diversity of the Tubalar, Even, and Ulchi
Lineage RFLP (SNP) HVS-I (-16000) Tubalar Even Ulchi
A4 (2/2) 663e 192 223 290 319 362 9
(2/2) 663e 179 192 223 290 319 362 1
N9a (2/2) (5231 5417) 223 248 257A 261 311 519 6
N9b (2/2) (5147 5417) 189 223 2
(2/2) (5147 5417) 223 189 519 3
(2/2) (5147 5417) 129 189 223 311 1
(2/2) (5147 5417) 180dA 188 189 223 519 1
Y1a (1/-) 7933j 28391e (5417) 126 189 231 519 5
(1/-) 7933j 28391e (5417) 126 189 266 519 2
(1/-) 7933j 28391e (5417) 126 189 231 266 519 5 47
(1/-) 7933j 28391e (5417) 126 231 266 304 519 2
(1/-) 7933j 28391e (5417) 126 189 231 266 292 519 2
(1/-) 7933j 28391e (5417) 126 189 231 266 294 519 4
(1/-) 7933j 28391e (5417) 126 140 189 231 266 399 519 1
(1/-) 7933j 28391e (5417) 093 126 189 231 266 519 1
(1/-) 7933j 28391e (5417) 126 140 189 231 266 399 519 3
(1/-) 7933j 28391e (5417) 126 169 189 231 266 519 1
(1/-) 7933j 28391e (5417) 126 189 231 292 519 1
X2e (2/2)21715c 14465s (15310) 189 223 278 519 1
B4b1a (2/2)26022a (8281d9) 086 136 189 217 519 8
(2/2)26022a (8281d9) 086 136 189 195 217 519 1
B5b2 (1/-) (8281d9) 111 140 189 234 243 244 463 519 1
F1a (2/2) -6389w 212406h (4086) 162 172 304 519 4
(2/2) -6389w 212406h (4086) 129 172 304 311 362 519 1
F1b (2/2) 4732k26389w212406h212629b 172 189 232A 249 304 519 5
(2/2) 4732k26389w212406h212629b 189 232A 249 304 311 519 3
F2 (2/2)26389w (10535 10586) 092A 291 304 4
R9b (2/2) (1541) 145 192 243 304 309 390 519 1
HV9 (2/2)214766u (8994) 249 261 311 1
H8 (2/2)27025a214766u (13101C) 288 362 4
U2e (2/2) 12308g 15907k (1811) 051 129C 189 214 258 362 519 2
U4a (2/2) 4643k 12308g (1811 8818) 129 134 356 519 1
U4b (2/2) 4643k 12308g (1811 7705) 189 356 1
(2/2) 4643k 12308g (1811 7705) 356 519 11
(2/2) 4643k 12308g (1811 7705) 287 356 519 1
(2/2) 4643k 12308g (1811 7705) 311 356 519 8
U5a1 (2/2) 12308g (15218) 192 241 256 270 287 304 325 399 9
C1a 2902291d (1/1)27598f 213259o 223 298 325 327 356 1
C4a1 (1/1)21715c 213259o (12672) 093 129 223 327 519 1
(1/1)21715c 213259o (12672) 129 223 298 327 519 1
(1/1)21715c 213259o (12672) 150 223 298 327 519 1
(1/1)21715c 213259o (12672) 093 129 223 298 327 519 1 2 1
(1/1)21715c 213259o (12672) 129 150 223 298 327 519 1 1
C4a2 (1/1)213259o (12672) 171 223 298 327 344 519 1 1
(1/1)213259o (12672) 223 298 327 344 357 519 1 1
(1/1)213259o (12672) 171 223 298 327 344 357 519 7
C4b (1/1)213259o (3816) 223 261 298 519 1
(1/1)213259o (3816) 223 298 327 519 14 10
(1/1)213259o (3816) 223 291 298 327 2 1
(1/1)213259o (3816) 223 298 311 327 3
(1/1)213259o (3816) 223 298 327 497 1
(1/1)213259o (3816) 089 223 291 298 327 1
(1/1)213259o (3816) 223 2591A 298 327 3
C5 (1/1)213259o (5911C) 223 261 288 298 11
(1/1)213259o (5911C) 223 288 298 327 390 1
(1/1)213259o (5911C) 093 189 223 261 288 298 519 2
(1/1)213259o (5911C) 093 223 288 291 298 327 518T 519 5
(1/1)213259o (5911C) 223 288 291 298 327 518T 519 1
C7 (1/1)213259o (5821) 219 223 298 327 519 1
Z1a (1/1)26749v (10325) 129 185 223 224 260 298 2
Z1a1 (1/1)26749v (9494 10325) 129 185 223 224 260 298 1
Z1a2 (1/1)26749v (10325 11590) 129 185 189 223 224 260 298 519 1
(1/1)26749v (10325 11590) 093 129 185 189dT 223 224 260 298 320 1
M8a (1/1) 14465s 184 223 298 319 4
(1/1) 14465s 184 189 223 293 298 319 1
(1/1) 14465s 086 223 298 319 1
D4a1 (1/1)25176a (10410) 129 223 362 519 1
D4b1a2a1 (1/1)25176a 21018l 13717a 14923c 15437e 093 172 173 215 223 319 362 10
D3 (1/1)2951j 25176a (1018l) 15437e 223 319 362 2 2
D4b2b (1/1)25176a (1382C 8964 9296) 223 362 1

American Journal of Physical Anthropology

126 R.I. SUKERNIK ET AL.
TABLE 1. (Continued)
Lineage RFLP (SNP) HVS-I (-16000) Tubalar Even Ulchi
D4c2 (1/1)25176a (8383 9431) 223 245 362 1
(1/1)25176a (8383 9431) 223 245 311 362 368 2
D4e4 (1/1)25176a (1935 8683 11215 14905) 189 223 362 1
(1/1)25176a (1935 8683 11215 14905) 223 291 362 1 3
(1/1)25176a (1935 8683 11215 14905) 129 189 223 362 1
D4e5 (1/1)25176a (5021 11215 15106 15184) 129 223 274 291 311 362 1
D4g2b (1/1)25176a (4131) 086 223 362 1
D4h (1/1)25176a (3336 3644 5048) 223 325 362 4
D4i2 (1/1) 4830n -5176a 223 294 362 3
D4j (1/1)25176a (11696) 223 362 6 6
(1/1)25176a (11696) 184 223 311 362 2
(1/1)25176a (11696) 223 263 362 10 1
(1/1)25176a (11696) 148 223 263 362 1
(1/1)25176a (11696) 082 147A 223 362 4
D4l (1/1)25176a (10427) 223 362 368 2
(1/1)25176a (10427) 223 274 362 368 2
(1/1)25176a (10427) 223 362 368 2
D4m2 (1/1)21715c 25176a (8762 12651C) 042 214 223 362 3 1
(1/1)21715c 25176a (8762 12651C) 042 093 214 223 362 2
D4o1 (1/1)25176a 10646k 183 223 274 290 319 362 1
(1/1)25176a 10646k 176 223 274 290 319 342 362 4
(1/1)25176a 10646k 129 176 223 274 290 319 342 362 1
D4o2 (1/1)25176a 10646k 093 223 232 290 362 1 6
(1/1)25176a 10646k 093 223 232 261 290 362 1 4
(1/1) -5176a 10646k 093 223 232 261 294 362 2
D5a (2/2)25176a 12026h (10397 12705) 172 189 223 266 362 1
(2/2)25176a 12026h (10397 12705) 092 172 189 223 266 362 2
(2/2)25176a 12026h (10397 12705) 092 126 164 189 223 266 362 3 1
D5c (2/2)25176a (4200T 4216 10397 12705) 129 1881C 1931C 311 362 390 1
(2/2) (4200T 4216 10397 12705) 129 1881C 1931C 311 362 390 1
(2/2)25176a (4200T 4216 10397 12705) 129 1881C 1931C 362 390 519 2
G1b (1/1) 4830n 8198a 017 129 223 519 2 2
(1/1) 4830n 8198a 017 093 129 223 519 4 3
(1/1) 4830n 8198a 017 093 129 153 223 519 2
(1/1) 4830n 8198a 017 093 129 207 223 519 2
(1/1) 4830n 8198a 017 093 129 223 303 519 1 1
(1/1) 4830n 8198a 017 093 129 223 311 519 1
(1/1) 4830n 8198a 017 093 207 223 325 519 1
(1/1) 4830n 8198a 017 051 093 207 223 399 519 2
G2a1 (1/1) 4830n 27598f 223 227 278 362 1
(1/1) 4830n 27598f 223 227 278 362 519 1 1
(1/1) 4830n 27598f 223 227 234 278 362 456 1
(1/1) 4830n 27598f 093 129 223 271 278 362 399 1
M7 (1/1) 9820g 223 245 311 362 368 1
(1/1) 9820g 140 187 209 223 519 1
(1/1) 9820g 129 152 179 189 223 362 2
M9a1 (1/1) 3391e 223 234 316 362 1
144 87 160

Mutations were scored relative to the revised Cambridge Reference Sequence, rCRS (Andrews et al.,1999). RFLP sites are num-
bered from the first nucleotide of the enzyme recognition sequence. The restriction enzymes are given using the following single–let-
ter code: a 5 AluI; c 5 DdeI; e 5 HaeIII; f 5 HhaI; g 5 HinfI; h 5 HpaI; j5MboI; k 5 RsaI; l 5 TaqI; n 5 HaeII; o 5HincII; s 5
AccI; u 5 MseI; v 5 AvrII; w 5 Tsp509I. Three different mutations 1715, 1719 or 17181A create the same site loss -1715DdeI (veri-
fied through sequencing). The presence/absence of the associated 10394DdeI/10397AluI sites is denoted through slash brackets (1/1),
(–/–), or (1/–). 8281d9 5 9bp COII/tRNALys deletion. ‘‘2’’ indicates the absence of restriction site. Mutations are transitions, unless
the base change is specified explicitly. Insertions are specified by ‘‘1’’ with the inserted nucleotide. Single Nucleotide Polymorphisms
(SNP) in the coding region verified through sequencing are shown in brackets. Only those nucleotide positions between 16,013 and
16,520 that differ from the rCRS are shown. Founding RFLP/SNP/HVS-I haplotypes are shown in boldface. Additional mutations in
the coding region are shown in parenthesis and were identified by or confirmed by sequencing.

mtDNA data from 72 Tubalar admixed with Chelkan
(Starikovskya et al., 2005) were revised and supple-
mented by new Tubalar samples. As a result, each of the
communities sharing the river or lake was represented
more or less equally in the total sample.
Even. In recent traditional times, the Even, formerly
called Lamut, were a large group of reindeer herders
and hunters of thousands individuals who spoke a
language in the northern Tungusic branch of the Altaic
linguistic family. They spread over a vast territory
stretching from the Upper Yana River in the west to the
Sea of Okhotsk in the east. The Even share a common
genetic heritage with the Evenki, formed through the
mixing of northern aboriginal Siberians and southern
populations from former Manchuria (Levin and Potapov,
1964; Janhunen, 1996).
This study includes 87 mtDNA samples. Previously
published mtDNA data on 18 Even-Evenki from the Sea
of Okhotsk coast (Starikovskaya et al., 2005) were re-

American Journal of Physical Anthropology

 TABLE 2. mtDNA haplogroup frequencies in 19 populations
Eskimos
Tubalar Mansi Ket Nganasan Tuvan Tofalar Evenki Yukaghir Even Ulchi Udegey Negidal Nivkhi Itelmen Koryak Chukchi Sireniki Chaplin Naukan
Lineage (144) (98) (38) (39) (95) (46) (53) (82) (87) (160) (46) (33) (56) (47) (147) (182) (37) (50) (39)
A2a - - - - - - - - - - - - - - 2.7 33.7 43.3 72.0 33.3
A2b - - - - - - - - - - - - - - - 13.9 27.0 18.0 41.0
A4 6.9 3.1 2.6 - 1.1 - 7.5 - - - - - - - - - - - -
A8 - - 5.3 - 1.1 - - - - - - - - 6.5 2.7 - - - -
N2a - - 2.6 - - - - - - - - - - - - - - - -
W - - - - 2.1 - - - - - - - - - - - - - -
N9a 4.2 - - - 3.2 - - - - - - - - - - - - - -
N9b - - - - - - - - - 4.3 30.4 - - - - - - - -
Y1 - - - - - - - - 5.8 42.9 8.7 21.2 66.1 4.4 8.8 - - - -
X2e 0.7 - - - - - - - - - - - - - - - - - -
B4a - - - - 5.1 4.3 - - - - - - - - - - - - -
B4b1a 6.3 - - - 1.1 - - - - - - - - - - - - - -
B5 - - - - 2.1 - - - - 0.6 - 12.1 - - - - - - -
F1 1.4 1.0 23.7 - 4.1 8.7 1.9 - 5.8 3.1 - - - - - - - - -
F2 2.8 - - - - - - - - - - - - - - - - - -
R9b 0.7 - - - - - - - - - - - - - - - - - -
HV 0.7 - - - - - - - - - - - - - - - - - -
H 2.8 14.3 10.5 - 4.1 - - - - - - - - - - - - - -
V - 1.0 - - - - - - - - - - - - - - - - -
J - 12.3 - - 2.1 - - - - - - - - - - - - - -
T - 7.2 - - - - - - - - - - - - - - - - -
U2e 1.4 - - - - - - - - - - - - - - - - - -
U4a 0.7 5.1 21.1 12.8 - - - - - - - - - - - - - - -
U4b 14.7 8.1 2.6 - 1.1 - - - - - - - - - - - - - -
U4c - 3.1 5.3 7.7 - - - - - - - - - - - - - - -
U5a 6.3 4.1 5.3 - 2.1 - - - - - - - - - - - - - -
U7a - 5.1 - - - - - - - - - - - - - - - - -
K - 3.1 - - - - - - - - - - - - - - - - -
C1a - - - - - - - - - 0.6 - - - - - - - - -
C4a 2.1 6.1 13.2 10.3 19.7 39.1 43.4 12.2 15.9 1.9 2.2 3.0 - - 0.7 - - - -
C4b 13.9 10.2 2.6 20.5 15.6 10.9 20.7 41.6 12.5 3.1 15.2 6.1 - - 21.8 6.9 - - -
C5 4.2 1.0 - 20.5 7.2 10.9 17.0 12.2 3.5 6.8 - 6.1 - 13.0 13.6 11.9 - - -
C7 - - - - - - - - 1.2 - - - - - - - - - -
Z1 1.4 - 2.6 2.6 1.1 10.9 - 2.4 2.3 0.6 - - - 6.5 5.4 - - - -
M8a - - - - - 15.2 - - - 3.7 15.2 - - - - - - - -
D4a - - - - - - - - - 0.6 - 6.1 - - - - - - -
D4b1 7.0 - - - 2.1 - 1.9 3.6 - - - - - - 1.4 5.0 - - 25.7
D4b2 - - - - 4.1 - - - - 0.6 - - - - - - - - -
MITOCHONDRIAL GENOME DIVERSITY IN NATIVE SIBERIANS

D3 - 1.0 - 17.9 1.1 - - 1.2 2.3 1.2 - - - - - - - -

D4c - - - - 1.1 - - - 1.2 1.2 - - - - - - - - -
D4e4 - - - - - - 1.9 - 3.5 1.9 - - - - - - - - -
D4e5 - - - - - - - - 1.2 - - - - - - - - - -
D2a - - - - - - - - - - - - - - - 2.0 29.7 10.0 -
D4g - - - - - - - - - 0.6 - - - - - - - - -
D4h - - - - - - - - - 2.5 - - - - - - - - -
D4i - - - - - - - 4.9 3.5 - - - - - - - - - -
D4j 7.0 1.0 2.6 5.1 3.2 - 1.9 - 19.4 1.9 - 6.1 - - - - - - -
D4l 1.4 3.1 - - - - 1.9 2.4 4.5 - - 3.0 - - - - - - -

American Journal of Physical Anthropology

127
128 R.I. SUKERNIK ET AL.

Tubalar Mansi Ket Nganasan Tuvan Tofalar Evenki Yukaghir Even Ulchi Udegey Negidal Nivkhi Itelmen Koryak Chukchi Sireniki Chaplin Naukan
vised and supplemented by 69 new Even samples drawn

MtDNA haplogroup composition and percentages from populations other than the Tubalar, Even, and Ulchi are adapted from data of Schurr et al., (1999), Derbeneva et al.,
(39)
from elder persons currently residing in the villages of

-
-
-
-
-
-
-
-
-
-
Chokurdakh (Allaikh district, Sakha-Yakut Republic),
and Nelkan and Djigda (Ayan-Maysky District, Khabar-
Eskimos
ovsk Region). While Chokurdakh is located on the left
(50)
bank of Indigirka River in its low course, Nelkan and

-
-
-
-
-
-
-
-
-
-
Djigda are far apart to the southeast, in the Maya-Aldan
River area. The majority of samples come from individu-
als who reported their Even maternal ancestry, but quite
(37)
-
-
-
-
-
-
-
-
-
-
a few blood donors from Chokurdakh were uncertain
about their Even or Yukaghir ancestral continuity. Like-
wise, a few individuals from Maya River reported their
(182)

26.6
mixed Even-Evenki origin. Efforts were made to avoid
-
-
-
-
-

-
-
-
-
taking blood from individuals who had the Turkic-speak-
ing Yakut on their maternal side. Taking into account
the family history of each participant, including the
(147)

42.9
-
-
-
-
-

-
-
-
-
birthplace of the maternal grandmother and the lan-
guage she spoke, the entire sample represented a subset
of the Tungusic-speakers, who a century ago were wan-
69.6
(47)

dering in small aggregates within the vast area between

-
-
-
-
-

-
-
-
-

the Yana, Indigirka and Kolyma River upper reaches in

the west and the Sea of Okhotsk Coast in the east.
23.2
(56)

Ulchi. Historically, the Ulchi are a well-defined tribe of

5.4

5.4
-
-
-

-
-
-
-

hunters and fishermen dispersed along the lakes and the

reaches of the Lower Amur. They speak a language of the
27.3

Tungusic-Manchu group (Levin and Potapov, 1964; Black,

(33)

9.1
-

-
-
-

-
-
-
-

1988; Krauss, 1988). Previously published mtDNA data

obtained from 87 elderly Ulchi residing in Old and New
Bulava, two neighboring villages (Starikovskaya et al.,
19.5
(46)
TABLE 2. (Continued)

8.7

2005), were revised and supplemented by 73 new samples

-
-
-
-
-
-
-
-

collected in Bogorodskoe and Nizhniy Gavan villages (Ulchi

district, Khabarovsk Region) in September 2009. Hence,
(87) (160)
0.6
8.1

0.6

7.5
1.2

2.5
0.6

the total Ulchi sample consisted of 160 individuals, with lit-

-

tle admixture with the Nivkhi, Negidal, and Udegey.

10.3
2.3
1.2

3.5
-

-
-
-
-

mtDNA analysis
Genomic DNAs were extracted from buffy coats by using
14.7
(82)
2.4

1.2
1.2

standard procedures. The first step consisted in mtDNA

-
-

-
-
-
-

variation surveyed by digestion with a battery of restric-

tion enzymes, sequencing HVS-I of the control region and
diagnostic single nucleotide polymorphisms (SNPs) in the
(53)

(2002a,b,c), Starikovskaya et al., (2005), and Volodko et al., (2008).

1.9

coding region. Founding restriction fragment length poly-

-
-
-

-
-
-
-
-
-

morphism (RFLP)/SNP/HVS-I haplotypes are in boldface,

as shown in Table 1. Complete sequencing procedure
(46)

entailed polymerase chain reaction amplification of the

-
-
-
-
-
-
-
-
-
-

eleven overlapping mtDNA templates, which were

sequenced in both directions with BigDye terminator
(95)

chemistry (PE Applied Biosystems) and ABI Prism 3130

1.1

1.1

6.3
4.1
3.2
-
-

-
-

DNA Analyzer. Trace files were analyzed with the

Sequencher (version 4.5 GeneCode Corporation) software.
Mutations were scored relative to the revised Cambridge
(39)

2.6

Reference Sequence, (rCRS) (Andrews et al., 1999).

-

-
-
-
-
-
-
-
-

Phylogenetic and statistical analyses

(98) (38)

Network analysis. mtDNA complete sequences gener-

-
-
-
-
-
-
-
-
-
-

ated through the course of this study, revealing shared

lineages or sublineages within and among related Sibe-
2.0
1.0

6.1

1.0
-
-

-
-

rian sources, were assembled into phylogenetic trees by

using the median-joining algorithm of the Network
4.5.1.0 (Bandelt et al., 1999) and mtPhyl software
Lineage (144)
2.1
4.2

2.1
2.8

2.1
-

-
-
-

(http://eltsov.org).
Classification of mtDNA types. To reconcile discrepan-
cies in definition of haplogroup composition (Volodko
D4m
D4o

D5a
D5c

et al., 2008), we now used updated nomenclature of

D4*

M7
M9
G1
G2
G3

van Oven and Kayser (2009; http://www.phylotree.org/).

American Journal of Physical Anthropology

 MITOCHONDRIAL GENOME DIVERSITY IN NATIVE SIBERIANS 129
TABLE 3. Siberian mtDNA complete sequences generated through this investigation
No. Haplo-group Ethnicity and sampling location GenBank accession number
1 A4 Tubalar, North Altai FJ493500
2 X2e Tubalar, North Altai FJ147306
3 X2c Russian, Upper Volga R. FJ147321
4 N9a Tubalar, North Altai FJ147307
5 N9a1 Tuvan, South Siberia HM776708
6 N9b Udegey, Sikhote-Alin FJ493503
7 N9b Ulchi, Lower Amur R. HM776709
8 Y1a Ulchi, Lower Amur R. HM776710
9 Y1a Ulchi, Lower Amur R. HM776711
10 Y1a Ulchi, Lower Amur R. HM776712
11 Y1a Ulchi, Lower Amur R. HM776713
12 Y1a Ulchi, Lower Amur R. HM776714
13 Y1a Even, NE Siberia HM776715
14 N1b2 Russian, SW Siberia FJ493516
15 R9b Chelkan, North Altai FJ147308
16 HV9 Chelkan, North Altai FJ147309
17 H8 Tubalar, North Altai FJ147310
18 U2e1 Tubalar, North Altai FJ147311
19 U2e1 Russian, SW Siberia FJ493504
20 U4a Tubalar, SW Siberia FJ147312
21 U4a Russian, SW Siberia FJ493505
22 U4a Nganasan, Taimyr FJ493506
23 U4a Mansi, Lower Ob R. FJ493507
24 U4b Tubalar, North Altai FJ147313
25 U4b Tubalar, North Altai FJ147314
26 U4b Tubalar, North Altai FJ147315
27 U4b Tubalar, North Altai FJ147316
28 U4b Mansi, Lower Ob R. FJ858877
29 U4b Mansi, Lower Ob R. FJ147322
30 U5a1 Russian, SW Siberia FJ493508
31 U5a1 Tubalar, North Altai FJ147317
32 U5b Russian, SW Siberia FJ493517
33 U7a Mansi, Lower Ob R. FJ858878
34 Z1a Tubalar, North Altai FJ147318
35 Z1a Even, NE Siberia FJ493514
36 Z1a Even, NE Siberia FJ493515
37 Z1a Yukaghir, NE Siberia FJ493509
38 Z1a Yukaghir, NE Siberia FJ493510
39 Z1a Yukaghir, NE Siberia FJ493511
40 Z1a-740-12930 Ket, Lower Yenisei R, FJ493512
41 Z1a Nganasan, Taimyr FJ493513
42 Z1a Ulchi, Lower Amur R. HM044854
43 D4* Mansi, Lower Ob R. JN375993
44 D4e4 Even, NE Siberia FJ858879
45 D4e4 Even, NE Siberia FJ858880
46 D4e4 Even, NE Siberia FJ858881
47 D4e5 Even, NE Siberia FJ858882
48 D4b1a2a Tubalar, North Altai FJ493501
49 D4b1a2a Chukchi, Chukotka GQ376202
50 D3 Even, NE Siberia FJ858883
51 D3 Mansi, Lower Ob R. FJ858884
52 D3 Yukaghir, NE Siberia FJ858885
53 D4b1 Tuvan, South Siberia FJ858886
54 D4b2b Tuvan, South Siberia FJ493502
55 D4b2b Tuvan, South Siberia HM153529
56 D4b2b Tuvan, South Siberia HM153530
57 D4o Tubalar, North Altai FJ147319
58 D5c Tubalar, North Altai FJ147320
59 D4j Even,NE Siberia FJ858887
60 D4j Even, NE Siberia FJ858888
61 D4j Ulchi, Lower Amur R. HM044855
62 D4j Ulchi, Lower Amur R. HM044856
63 D4j Tuvan, South Siberia HM153527
64 D4j Tuvan, South Siberia HM153528
65 D4c2 Even, NE Siberia FJ858889
66 D4c2 Ulchi, Lower Amur R. HM776716
67 D4g2b Ulchi, Lower Amur R. HM776717

American Journal of Physical Anthropology

130 R.I. SUKERNIK ET AL.

Estimates of coalescence time. Age estimates are TABLE 4. Age estimates with 95% confidence intervals for
based on q-statistics (Forster et al., 1996; Saillard et al., mtDNA haplogroups referred to in the text or figures
2000). Incidentally, q is an objective measure of a depth rho estimate
of a node within the tree and is an indicator of the age Complete Synonymous
of the mutations defining the branch leading to that Haplogroup Na genome positions
node. Converting q to time would require assumptions
A2 177 14.4 (10.6; 18.3) 15.1 (12.8; 17.4)
about the consistency of mutation rates on different
A4 224 28.8 (17.3; 40.9) 21.9 (15.3; 28.4)
branches of the phylogenetic tree, and there is some dis- A8 3 17.3 (9.8; 25.3) 11.0 (6.9; 15.2)
crepancy deriving from the differences in mutation rates B4b1a 51 20.5 (11.3; 30.0) 18.9 (12.3; 25.4)
used (briefly reviewed by Pereira et al., 2011). Here, we B2 64 15.9 (13.3; 18.5) 17.8 (15.6; 20.0)
used recently improved rates for the entire mtDNA mo- N9 130 38.7 (28.2; 49.5) 36.0 (28.2; 43.9)
lecular clock, considering one coding-region substitution N9a 69 18.7 (12.3; 25.3) 16.5 (11.8; 21.1)
every 3,624 years, while assuming 7,884 years per syn- N9b 25 16.4 (12.0; 20.9) 19.2 (14.5; 24)
Y 36 25.0 (15.0; 35.5) 30.7 (20.7; 40.6)
onymous transition (Soares et al., 2009). To define the Y1 17 12.4 (5.9; 19.1) 12.5 (6.0; 19.0)
genetic relationships between populations, the principal Y1a 13 6.0 (3.3; 8.8) 1.8 (0.8; 2.9)
component analysis (PCA) was performed using Statis- N2 118 53.0 (32.1; 75.1) 46.0 (31.4; 60.5)
tica software, version 6.0 (StatSoft). X2e2 7 6.7 (0.6; 13.1) 1.1 (0.0; 2.3)
X2e2-13327 5 1.5 (-0.7; 3.8) 0.0 (0.0; 0.0)
H8 7 11.4 (6.1; 16.8) 6.8 (3.6; 9.9)
RESULTS U2e1 26 17.5 (10.8; 24.3) 20.0 (12.5; 27.5)
mtDNA diversity U4 132 18.6 (13.8; 23.4) 21.4 (16.2; 26.6)
U4b 37 18.0 (11.5; 24.7) 20.2 (13.1; 27.3)
Table 1 delineates distinct SNP haplotypes belonging U4b1 27 17.3 (10.8; 24.1) 18.1 (12.6; 23.6)
to lineages identifiable by subhaplogroup-specific muta- U7 26 18.7 (13.2; 24.3) 16.4 (12.7; 20.0)
tions in 144 Tubalar, 87 Even and 160 Ulchi mtDNAs. U7a 2 22.0 (10.8; 33.5) 23.7 (14.0; 33.3)
Table 2 presents the distribution of these subha- D1 46 14.5 (11.4; 17.6) 17.8 (15.2; 20.4)
D4 429 28.8 (23.1; 34.6) 37.1 (31.2; 43.1)
plogroups within and between 19 populations dispersed D4b 154 29.1 (19.9; 38.6) 42.7 (33.0; 52.4)
across the whole Siberia. The ethnic origin and approxi- D4b1 55 24.8 (17.5; 32.3) 32.4 (25.5; 39.3)
mate location of 67 mtDNA complete sequences, of which D4b1a 26 23.1 (14.1; 32.5) 38.5 (27.7; 49.4)
39 were from the Tubalar, Even, and Ulchi, and 28 from D4b1a2 18 17.0 (8.8; 25.4) 22.8 (14.2; 31.3)
other Siberians, along with accession codes in GenBank, D4b1a2a 17 13.9 (7.3; 20.6) 14.8 (10.4; 19.2)
are given in Table 3. The coalescence time and variance D4b1a2a1-16093 7 12.2 (5.2; 19.5) 16.9 (9.7; 24.1)
D4b1c 9 13.4 (2.7; 24.7) 25.4 (11.7; 39.1)
computed from the root of major mtDNA lineages and of D3 9 2.6 (0.9; 4.3) 1.8 (0.5; 3.0)
their younger nodes are given in Table 4. D4b2 99 16.3 (9.8; 23) 23.9 (16.8; 30.9)
D4e 126 19.7 (12.0; 27.8) 21.2 (14.0; 28.4)
Macrohaplogroup N mtDNAs D2a1 33 5.1 (0.7; 9.7) 2.9 (1.5; 4.2)
D4h 60 39.9 (25.3; 55.2) 33.5 (22.9; 44.1)
Almost half of the mtDNA types harbored by the D4j 88 16.0 (10.8; 21.4) 17.3 (12.6; 22.0)
Tubalar were found to fall into different lineages of C4 119 21.7 (15.3; 28.4) 23.5 (16.9; 30.2)
‘‘west’’ Eurasian haplogroups. Most common of the Tuba- C4a 73 25.8 (17.8; 34.1) 20.6 (15.4; 25.8)
C4b 46 8.2 (5.1; 11.5) 7.7 (4.7; 10.7)
lar mtDNA samples are the haplogroup U mtDNAs, con- C4c 2 13.4 (5.0; 22.2) 11.8 (5.0; 18.7)
fined to subhaplogroups U2e, U4a, U4b, and U5a1. Of Z 64 24.9 (15.9; 34.4) 27.3 (21.2; 33.5)
these, the entire U4 type attains its highest frequency Z1 29 20.4 (7.4; 34.0) 21.7 (10.8; 32.7)
east of the Urals Mountains, ranging from 15.4% in the Z1a 28 9.1 (2.5; 15.8) 14.4 (6.3; 22.5)
Tubalar to 29.0% in the Ket (Tables 1 and 2). The Z1a1 21 6.9 (0.2; 13.8) 9.0 (1.8; 16.2)
uneven distribution of the two subhaplogroups, with Z1a1a 19 1.6 (0.6; 2.6) 0.8 (0.2; 1.4)
U4a predominately found in the Ket (21.1%) and U4b in a
Number of complete sequences gleaned from GenBank.
the Tubular (14.7%), could be attributed to their differ-
ent population history augmented by subsequent genetic
samples, respectively. One of the U2e and one U5a1
drift. To discern the ancestral status of U4a and U4b
mtDNAs were subjected to complete sequencing. We
types in the region, we generated 10 new sequences, of
found that the Tubalar U2e mtDNA sequence motif
which four are of U4a and six U4b (Table 3). Because of (524insAC-2626-5814-13419T-14587-16214-16258) was
the difference in the age of U4a (14.0/7.6 kya), in com- different from both European and Indian U2e counter-
parison with U4b (18.0/20.2), it seems unlikely that the parts (Palanichamy et al., 2004; Achilli et al., 2005; Met-
high frequency and extensive diversity within the Tuba- sapalu et al., 2004). Incidentally, we also sequenced the
lar U4b sequences confined to western Siberia is a result U2e mtDNA from a patient with Leber’s (Leber’s heredi-
of recent gene flow from eastern Europeans. Rather the tary optic neuropathy) disease of Russian origin. Both
remarkable concentration of the U4b mtDNAs preserved the Tubalar and Russian haplotypes assigned to U2e1
within the northern Altai-lower Ob-lower Yenisei trian- were not previously reported, and either differed from
gular could be a part of the Upper Palaeolithic expansion other derivatives of the U2e1 available through Gen-
from the Middle East or western Asia (Derbeneva et al. Bank. The entire U2e1 appears to have an age 17.5/20.0
2002b,c; Pimenoff et al. 2008; Naumova et al. 2009; this kya (Table 4). Recent identification of a complete U2
study). mtDNA sequence from 30,000-year-old early modern
Of the remaining haplogroup U samples, the mtDNAs humans from Kostenki, southwest Russia (Krause et al.,
that belonged to U2e and U5a1 were also well repre- 2010a), supported the picture with Upper Paleolithic
sented in the Tubalar and encompassed 2 and 9 mtDNA ancestry of the U2e1 lineage observed in West Siberian

American Journal of Physical Anthropology

 MITOCHONDRIAL GENOME DIVERSITY IN NATIVE SIBERIANS 131

Fig. 2. The phylogenetic tree of haplogroup N9 complete sequences revealed in Siberia. Mutation positions, relative to the re-
vised Cambridge reference sequence (Andrews et al., 1999) are transitions unless the base change is specified. Deletions are indi-
cated by a ‘‘d’’ preceding the deleted nucleotides. Insertions are indicated by a ‘‘1’’ preceding the inserted nucleotide. Reversal muta-
tions are underlined. Point mutations at 16182 and 16183 are excluded because of their dependence on the presence of C-T transi-
tion at 16189; the length variation in the poly-C stretch at nps 309-315 and point mutation at 16519 was omitted because of their
hypervariability. When two or more identical samples belong to the same group, their number is given in brackets.

Plain (Pimenoff et al., 2008; this study). Likewise, the
U5a1 mtDNA haplotype harbored previously non-
reported coding-region motif: 3027-3552-4924C-10858-
14110-15218.
Among the five Tubalar mtDNA samples that belonged
to haplogroup H, four harbored the characteristic coding-
region 13101C transversion and control-region 16288
transition, indicating that they should be attributed to
H8 (Achilli et al., 2004). This lineage is very uncommon.
Of seven H8 mtDNA sequences available from GenBank,
that one of the Tubalar differs from their European
counterparts by three previously nonreported transi-
tions: 961, 7765, and 12490. The presence in the Tubalar
of subhaplogroup H8 dating to 11.4/6.8 kya (Table 4)
may indicate a Neolithic phase expansion towards the
Altai Mountains.
In addition, the complete genome sequencing was per-
formed in two of 10 Tubalar mtDNAs of haplogroup A4.
It resulted in the appearance of a unique A4* mtDNA
haplotype, which shared no mutation with any other A4
sequences, with only 16362 being an exception. This
finding introduces the possibility that the A4* sequence
revealed in the Tubalar is tribal-specific, and represents
a part of basic A4 dispersal originated in Altai 28.8/21.9
kya, but only 14.4/15.1 kya its particular derivative
gave rise to an ‘‘American’’ enclave of the A2 (A2a1A2b)
haplogroup in modern Chukotka (Starikovskaya et al.,
2005; Volodko et al., 2008; Qin et al., 2010; this study).
Of special interest are the Tubalar B4b1a samples
(6.2%) that have 16086 variant, resulting in the 16136-
16189-16217-16519 motives, previously described in a
few ancient and modern mtDNA samples from the Egyin
Gol Valley (south of Lake Baikal in northern Mongolia)
(Keyser-Tracqui et al., 2003; 2006). Compared at the
complete sequence level, the Tubalar B4b1a shared 6023,
6413, and 16136 with only a part of the eastern Asian

American Journal of Physical Anthropology

132 R.I. SUKERNIK ET AL.
Fig. 3. The phylogeny of haplogroup D4b sequences. For additional information, see Figure 2 legend.
B4b1 full sequences albeit with the same ancestral
node 499-4820-13590 shared with Native American B2
(Starikovskaya et al., 2005; Hill et al., 2007; this study).
The estimated age of the B4b1a cluster is 20.5/18.9 kya,
in consistency with its pattern of geographic distribution
throughout the extreme south of Siberia and adjacent
part of Central/Eastern Asia.
A total of 16 distinct haplotypes attributable to hap-
locluster N9 (N9a-N9b-Y) were identified in the Tubalar,
Even and Ulchi (Table 1). The updated genealogy of N9
enriched by 10 new sequences, of which the Tuvan and
Udegey mtDNA samples are from our old collection, is
shown in Figure 2. The ages of principal offshoots of the
N9 lineage are 18.7/16.5 kya for N9a, 16.4/19.2 kya for
N9b, and 25.0/30.7 kya for Y, thus falling nicely within
the Ice Age, whereas the antiquity of the subhaplogroup
Y1a confined to the Even, Koryak, Ulchi, and Nivkhi is
much younger, only 6.0/1.8 kya. Spatial patterns and
coalescent dates of the N9a, N9b, and Y haplogroups
suggest that the N9 root (5417) emerged in southwest
Asia 38.7/36.0 kya, but only much later, presumably dur-
ing the LGM, its particular derivatives might have
spread through the corridor provided by southern refu-
gia that stretch from mountainous Altai to the Russian
Far East on one hand and deserted areas of Central
Asia steppe on the other (Finlanson and Cartion, 2007).
American Journal of Physical Anthropology
This conjecture is supported by absence of autochtho-
nous N in the South/Southeast Asia where only M has a
vast geographical distribution (Hill et al., 2007; Chan-
drasekar et al., 2009). The fact that N9 is present in the
Tubalar, Tuvan, Buryat, Udegey, and Ulchi (Starikov-
skaya et al., 2005), as well as ancient (Upper Paleolithic)
mtDNAs from Hokkaido (Adachi et al., 2009), implies
that relatively rare N9 mtDNAs exhibited by modern
Japanese (Tanaka et al., 2004; Nohira et al., 2010) have
Siberian rather than Southeast Asian source.
The haplogroup X sequence we revealed in a sole
Tubalar and one Russian mtDNA samples seem to be
attributed to the European X2e2 sub-branch. From the
Druze and Georgian X2e2, defined by 3948 and 12084
mutations (Reidla et al., 2003; Shlush et al., 2008), the
Tubalar differed at 13327. The age of Siberian X2e2-
13327 lineage calculated on the basis of five similar
mtDNA sequences, one Tubalar, one Teleut, two Altai-
kizhi, and one Buryat (the latter four being attested by
Derenko et al., 2007) is at most 1.5 kya (Table 4). It is
obvious that Siberian X2e2-13327 sub-cluster, separated
from the Near Eastern X2e root by three mutational
steps (3948-12084-13327), represents a portion of rela-
tively recent gene flow toward Altai-Sayan. So far, it is
impossible to say whether the bearers of the founding
sequence for X2a, distinguished by three coding region
 MITOCHONDRIAL GENOME DIVERSITY IN NATIVE SIBERIANS
Fig. 4. Schematic presentation of haplogroup D4 tree encompassing novel Mansi D* sequence.
mutations, 8913, 12397, and 14502 (Fagundes et al.,
2008; Perego et al., 2010), have reached North America
without leaving a progenitor of X2a in Siberia/Beringia.
Some haplotypes intermediate between Near Eastern
haplogroup X root and Native North American X2a are
apparently missing.
Finally, several Tubalar mtDNAs were found to fall
into various sublineages of F1, F2, and G2 haplogroups.
On the basis of what is known of the Tubalar ethnic his-
tory (Potapov, 1972), it is possible that the F1, F2, and
G2 mtDNAs have been acquired through the gene flow
from adjacent Tuvan or Altai-kizhi residing southward,
where these lineages are more common and diverse
(Starikovskaya et al., 2005; Derenko et al., 2007).
Macro-haplogroup M mtDNAs
Among the Tubalar, Even, and Ulchi mtDNAs attribut-
able to distinct haplogroup C and D lineages, representa-
tives of almost all known subhaplogroups are present
(Table 1). Specifically, among the 70 (48.6%) Tubalar
mtDNA samples that belong to traditional East Asian
haplotypes, 10 harbored characteristic mutations, indi-
cating that they belong to haplogroup D4b1a2a1 (D3a2a
in Volodko et al., 2008). Of these, two samples, each rep-
resenting geographically separated territories, were com-
pletely sequenced. Sublineage of this haplogroup marked
by 16093 unequivocally links a portion of the Tubalar
maternal gene pool to that one harbored by the Eskimos
residing on both sides of the Bering Strait. The coales-
cence time of the D4b1a2a1-16093 cluster, based on 7
mtDNA genomes, dates to 12.2/16.9 kya, in consistency
with its pattern of geographic distribution, the Tubalar
sequences included, whereas the estimated age of the
11383-14122C subcluster, calculated on the basis of only
five entire sequences (two Chukchi, two Naukan Eskimo,
and one Canadian Inuit), is significantly younger, 7.4/9.5
kya, implying a separate dispersal that ultimately con-
tributed to formation Coast Chukchi and Neo-Eskimo
mtDNA gene pool within the range of early-mid
Holocene. A wide geographic distribution of the mtDNA
lineages stemmed from either D4b1a2 (aged 17.0/22.8
kya) or the D4b1c nodes (aged 13.4/25.4 kya) encompass
133
most sequences from the Siberian interior. In contrast,
members of the D4b2 node of similar time-depth (16.3/
23.9 kya) are virtually absent from autochthonous Sibe-
rians as they are confined largely to central/eastern
Asians, thus suggesting significant discontinuity in the
northeast Asian gene pool (Fig. 3; Table 4).
New haplogroup D4j sequences (two Tuvan, two Even,
and two Ulchi) have also been subjected to complete
sequencing. This haplogroup (‘‘D6’’ in Volodko et al.,
2008) is conspicuous for its nodal mutation at 11696 and
embraces different haplotypes from Siberia, central and
eastern Asians (Starikovskaya et al., 2005; Derenko et
al., 2007; Volodko et al., 2008; Qin et al., 2010). An
exceptionally large variety of D4j haplotypes and inde-
pendent lineages have been recognized among the Tuba-
lar, Mansi, Ket, Nganasan, Even, Evenk, Yukaghir,
Ulchi, Tuvan, and Buryat mtDNA sequences. The esti-
mated age of the D4j cluster is 16.0/17.3 kya (Table 4),
in consistency with its pattern of geographic distribu-
tion, suggesting Manchuria/Mongolia region as putative
origin of the haplogroup D4j lineages.
Aside from the four Even/Yukaghir D4e mtDNAs (‘‘D2’’
in Volodko et al., 2008), we have completely sequenced
rare D4 mtDNA samples exhibited by either the Tubalar,
Even, or Ulchi, and compared them with a subset of sim-
ilar mtDNA genomes elsewhere. As a result, the D4o
(‘‘D4’’ in Volodko et al., 2008) sequence variants, distin-
guished by presence of 195-10646-16290, were found in
the Tubalar, Nganasan, Even, Ulchi, Negidal, and Niv-
khi, though in low frequency (Tables 1 and 2). Further
comparisons showed that one Even and two Ulchi
mtDNA samples share three mutations (8383, 9431, and
16245) with their East Asian counterparts, thus falling
within the lineage D4c2.
An unexpected and intriguing finding of this study
was relic D* mtDNA variant, initially noted at the HVS-
I level in two Mansi samples from northwestern Siberia
(Derbeneva et al., 2002b). The entire sequencing of one
of these Mansi mtDNA samples yielded unique, previ-
ously unreported set of mutations: 3583, 9856, 15884,
16192, 16261, and 16316. Since D* haplotype does not
share this set of mutations with those available from
GenBank, except for 3010, 8414, and 14668 characteris-
American Journal of Physical Anthropology
134 R.I. SUKERNIK ET AL.
Fig. 5. The phylogeny of haplogroup Z1 complete sequences.
Those with asterisk were gleaned from Ingman and Gyllensten
(2007).
tic for the D4 node, we have clustered D* haplotype
directly to basic D4 (Fig. 4). Because of the antiquity of
nodal D4 (28.8/37.1 kya), it is reasonable to suggest that
the Mansi D4* is the LGM-gap survivor among whatever
haplotypes expanded from the Far East, where the hap-
logroup D4 diversity is particularly high (Derbeneva et
al., 2002b; Starikovskaya et al., 2005; Volodko et al.,
2008; Nohira et al., 2009; this study). This conjecture is
consistent with archeological records of the Lower Amur,
Sakhalin and Hokkaido region (Derev’anko and Volkov,
1997; Kuzmin, 2008), suggesting a postglacial recoloniza-
tion event originated in maritime eastern Asia, with
humans spreading north and west.
We have also revealed seven Tubalar, three Even, and
one Ulchi mtDNA samples attributable to lineage D5
(Table 1). This lineage, for the first time described by
Derbeneva et al., (2002b), in contrast to other subsets of
the haplogroup D mtDNAs, has back mutated at the
10394 Dde I1 and 10397 Alu I1 sites, characterizing
macrohaplogroup M at the RFLP level.
Finally, nine new haplogroup Z1a complete mtDNA
sequences were generated. The geographic specificity
and coalescence time computed from the root of the Z
lineage (6752-9090-15784-16185-16260), assumes origin
of the Z1 founder in the vicinities of Lake Baikal 20.4/
21.7 kya. In the millennia after diversification in situ, Z1
American Journal of Physical Anthropology
Fig. 6. Phylogenetic relationships (PCA) among 19 Siberian
populations with the frequencies of the observed subha-
plogroups.
led directly to the extended Z1a node (Fig. 5). Most
likely, distinct sub-lineages of Z1, harbored by the Tuba-
lar, Tofalar, Nganasan, Yukaghir, Koryak, Even, and
Ulchi, could be a major part of Neolithic dispersals from
southeastern Siberia, whereas Z1a1a emerged in the
present-day Ket, Volga-Urals ‘‘Russians’’ and Finns-
Saami most recently, 1.6/0.8 kya. Confinement of single
Volga-Urals Russians to the Finns-Saami Z1a1a (Ingman
and Gyllensten, 2007) is not unexpected in view of
recent historical events. Finnic-speaking hunters and
gatherers from the Upper Volga basin, including those of
the Volga-Kama region to the west of the Ural moun-
tains, were partially dissolved in eastern Slavs 1,000
years ago, as the latter had spread rapidly across north-
ern Russia (Kluchevsky, 2003). Based on the distribution
of haplogroup Z1 and the number of sequence variants
encompass, we postulate that this lineage originated in
Manchuria, the putative homeland of the Altaic-speakers
(Janhunen, 1996), and was then dispersed by their geo-
graphical expansion.
Population relationships
To begin with, it is worthwhile to recall the major geo-
graphic subdivisions of Siberia, which are (1) western
Siberia, encompassing the Ob River basin, bounded by
the Ural Mountains in the west and Yenisei River in the
east; (2) eastern Siberia, which covers essentially the
Yenisei and Lena River basins, including the Taimyr
Peninsula far north, and the Trans-Baikal, east of Lake
Baikal; (3) northeastern Siberia, which stretches east of
Lena River up to Chukotka. The Russian Far East is a
separate large region of northern Asia, including the
lower Amur River basin, Sea of Okhotsk region, and
Sakhalin Island. The Kamchatka Peninsula and adjacent
part of the Bering Sea coast also may be associated with
the Russian Far East (reviewed by Kuzmin, 2008).
The distribution in Table 2 has shown that the
mtDNA variation west of the Yenisei is contributed by
substantial proportion of eastern Eurasian ancestry. Spe-
cifically, the Tubalar were found to harbor 48.2%
mtDNAs belonging to C1D lineages, whereas the Mansi
harbored 25.4%, and Ket of 21.0%, thus testifying a sep-
arate maternal makeup of the western and eastern Sibe-
rian populations. The PC analysis delineates the resem-
blances and distinctions of samples, representing 19
 MITOCHONDRIAL GENOME DIVERSITY IN NATIVE SIBERIANS
Siberian populations, based on sub-haplogroup frequen-
cies, and these are well reflected on the plot (Fig. 6). In
accord with the expectations, the Eskimos are outliers
while the Even placed near the Yukaghir because the
core of the present-day Even mtDNA pool would repre-
sent an amalgamation of the remnants of Paleo-Sibe-
rian-speaking Yukaghir and northern Tungusic-speakers
(Jochelson, 1910). Most likely, this is an implication of
recent northward expansion of the bearers of lineage G1
from the Sea of Okhotsk-Kamchatka region. This hap-
logroup is predominantly found in the Koryak and Itel-
men and also occurs at moderate frequency in the Negi-
dal and Yukaghir (Schurr et al., 1999; Starikovskaya et
al., 2005; Volodko et al., 2008; this study). On the same
reason, present day Chukchi would place an intermedi-
ate position between populations of the Russian Far
East the Eskimos. The PCA plot supports the hypothesis
that the Ulchi, Nivkhi, Negidal, and Udegey represent a
detached population cluster isolated by sufficient time to
be relatively distinct over the average genetic back-
ground of continental Siberia. This picture may reflect
prolonged interactions and, therefore, genetic inter-
change among inhabitants of the Lower Amur, Sakhalin
and Hokkaido since the early days of their common his-
tory (Adachi et al., 2009).
DISCUSSION
Traces of pre-LGM Eurasians in West Siberia
One of the most significant findings of this study is
some level of genetic continuity between small hunting-
gathering-fishing groups who for ages inhabited the
pine-birch forest area of western Siberia. Aside from the
Tubalar, they encompass the Ket, the sole living speak-
ers of Yenisseian isolate language, and Uralic-speaking
Mansi and Khanty from the Lower Ob River basin.
These populations are conspicuous for the presence of
tribal- or region-specific, previously unreported haplo-
types, clustering to west Eurasian haplogroups: H8,
U2e1, U4a, U4b, U51a, and U7a. Interestingly, the Tuba-
lar were lacking U7a mtDNA samples, which in Siberia
were confined to the Mansi and Khanty (Derbeneva et
al., 2002b; Pimenoff et al., 2008; Naumova et al., 2009).
Through this study, we found that the Mansi U7 mtDNA
subjected to complete sequencing exhibited a previously
unreported set of coding-region mutations: 4452, 4820,
5480, 10124, 12398, 14097, and 15804. This haplotype is
unique, and it should be clustered to the additional sub-
lineage of the U7a2 node distinguished by the coding
region mutation at 4502 (van Oven and Kayser, 2009).
The age of a single haplogroup may not be the age of a
population demographic event because of drift and/or
selection, to which small-sized populations adapting to
high-latitude environments are particularly sensitive.
Nevertheless, similar age estimates (18-24 kya) of the
founder clusters for several haplogroups (U2e1, U4b,
U51a, and U7a2) make it less probable to be an overesti-
mate of the colonization time, hence providing evidence
for LGM survival. Likewise, the age of a relic N2a
sequence variant, encountered in a Ket as the sister line-
age of haplogroup W (Derbeneva et al., 2002b) seems to
be much older than U7a2 as evidenced by the age of the
N2 founder (53/46 kya) (Table 4). Thus, the presence of
U7a2 and N2a lineages may be indicative of the rem-
nants of the Upper Paleolithic Europeans preserved just
east of the Urals Mountains. Their absence from the
Altai-Sayan gene pool (Starikovskaya et al., 2005;
135
Derenko et al., 2007; this study) may be explained by
extinction because of genetic drift or purifying selection
during long-term dispersals from the near East-South-
west Asia, where the U7 and N2 types present the most
widespread distribution and diversity (Richards et al.,
2000; Metsapalu et al., 2004; Quintana-Murcy et al.,
2004; Palanichami et al., 2004; Derenko et al., 2007).
Reconstructing trans-Beringian migrations into
North America
Contemporary distribution of mtDNA diversity on
both sides of the Bering Strait cannot be understood
without taking into account an array of variables and
individual events that are likely to have affected the tim-
ing and character of settlement in the now partially sub-
merged land that lies between Lena and Mackenzie Riv-
ers. Small groups of fishing and sea-mammal hunting
populations were apparently scattered throughout not
only the southern but also arctic coast of Beringia [30
kya. During the interval between the end of the LGM
cold peak (18.0 kya) and the beginning of the Holocene
(11.6 kya), Beringia may have been the repository of
remaining founding mtDNA sequences that were pulsing
into the interior and the coastal areas of Alaska and
northwest Canada at different times (Goebel et al., 2008;
Dillehay, 2009). Unceasing comparison of the complete
mtDNA sequences from Siberia and the Americas has
extended the number of founding haplotypes from Berin-
gia significantly (Volodko et al., 2008; Perego et al.,
2010; Kumar et al., 2011). In this regard, it is worth not-
ing relic C4c mtDNA sequences defined in two geograph-
ically distant Native American populations. One comes
from the Ijka-speaking tribe from Colombia (Tamm et
al., 2007), and the other from a sole Shuswap-speaker
from British Columbia, Canada (Malhi et al., 2010).
However, on the other side of the Bering Strait, an
extensive survey of Siberian/Asian samples failed to
reveal C4c, whereas its sister lineages, C4a and C4b,
were widely dispersed in Siberia (Table 2). The coales-
cence of C4c, though based only on two sequences avail-
able from GenBank, dates to 13.4/11.8 kya, depending on
whether the complete genome or synonymous substitu-
tion is used (Table 4). Assuming a low effective popula-
tion size, reduced diversity and a uniform distribution of
mtDNA lineages during the LGM, the lack of C4c in
western Beringia appears to have been a consequence of
a strong population bottleneck because of widespread
mortality from various sources since the first contact
with Europeans (Volodko et al., 2008). In other direction,
the mid-lower Amur region seems to remain the best
candidate for the ancestral homeland for a variety of
present-day American C1 and D4 sublineages, namely
C1b, C1c, C1d, and D4h3. This conjecture is based on
the presence of the D4h and C1a complete mtDNA
genomes in the Ulchi mtDNA pool (Derbeneva et al.,
2002a; Starikovskaya et al., 2005; this study). Moreover,
the D4h-16325 haplotype defined in four Ulchi samples
seems to occur in ancient mtDNAs from Hokkaido, albeit
assigned differently, as D1a (Adachi et al., 2009).
One major component of the mtDNA pool at the cross-
roads of two continents is the mutation specific to hap-
logroup D2a (11959), which must have arisen amongst
the common ancestors of Sireniki Eskimos, Aleuts, and
Na-Dene, representing the latest trans-Beringian expan-
sions into the New World. Accordingly, subhaplogroup
D2al derived through acquisition of 9667 from D2a root
American Journal of Physical Anthropology
136 R.I. SUKERNIK ET AL.
occurs in the Aleuts of the Commander Islands and Sire-
niki Eskimos of the Chukchi Peninsula (Derbeneva
et al., 2002a; Starikovskaya et al., 2005; Volodko et al.,
2008), and the Paleo-Eskimo Saqqaq mtDNA genome
from archeological remains in Greenland (Gilbert, 2008).
Importantly, a few non-Aleut D2a1 mtDNA samples
from the village of Nikolskoye on the Bering Island,
most likely of the Tlingit (Na-Dene) ancestry, missed
this mutation (Derbeneva et al., 2002a). Thus, the Paleo-
Eskimos represented by Saqqaq and Sireniki on one
hand, and Neo-Eskimos represented by Naukan on the
other hand, have distinct relationships to Siberians/
Asians as reflected in different ages for the D2a1 (5.1/
2.9 kya) and D4b1a2a1-16093 (12.2/16.9 kya), consistent
with different patterns of their geographical distribu-
tion (Volodko et al., 2008; this study). The coalescence
dates and spatial distribution of the D2a, D4b1a2, and
D4b1c/D3 haploclusters across Siberia-Beringia (Stari-
kovskaya et al., 2005; Derenko et al., 2007; Volodko
et al., 2008; Gilbert et al., 2008; this study) suggest
that their deep-rooted nodes, D4e and D4b1, emerged in
the refugia of the southern extent of Siberia prior or
during the LGM, placing part of recurrent episodic dis-
persals toward Alaska at the terminal Pleistocene to
early Holocene.
CONCLUSION
Here, we extended the survey of mitochondrial SNPs
and entire sequences across Siberia to go deeper into the
population-evolutionary history of northeastern Eurasia.
Relatively limited variation of east Eurasian lineages
(C4a, C4b, C5, D3, D4, D5, and Z1a) observed west of
Yenisei appears to be associated with admixture events
that distinguish more recently formed Eurasian popula-
tions from older ones. It resulted in a large variety of M
and N derivatives with substantial geographical separa-
tion of western and eastern Eurasian lineages. Our
results suggest that anatomically modern humans that
originally colonized the Altai-Sayan region derived from
macrohaplogroup N and came from Southwest Asia not
later than 38 kya. The derivatives of macrohaplogroup
M, which largely emerged or diversified within the Rus-
sian Far East, came along with subsequent migrations
to West Siberia area millennia later. Further insights
into the prehistory of native Siberians and their relation-
ship to Native Americans would benefit from generating
whole genome sequences, with the final goal to discern
traces of potential gene flow of archaic groups from
Altai, "Denisovans" to the ancestors of modern Siberians.
ACKNOWLEDGMENTS
We are indebted to the native people of Siberia, the
Tubalar, Even and Ulchi, in particular, for their partici-
pation in this project. The authors have greatly benefited
from conversations with Anatoly Derevianko and Andrei
Tabarev (Institute of Archaeology and Ethnography,
SBRAS, Novosibirsk). The help of Andre M. Sukernik in
editing the final draft of the manuscript is gratefully
acknowledged.
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