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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 133:1013–1027 (2007)

Mating Patterns Amongst Siberian Reindeer Herders:


Inferences From mtDNA and Y-Chromosomal Analyses
Brigitte Pakendorf,1* Innokentij N. Novgorodov,2 Vladimir L. Osakovskij,3 and Mark Stoneking4
1
Junior Scientists Group on Comparative Population Linguistics, Max Planck Institute for Evolutionary
Anthropology, Leipzig, Germany
2
Department of Grammar and Dialectology, Institute of Humanitarian Studies, Yakutsk, Republic Sakha (Yakutia),
Russian Federation
3
Human Genome Laboratory, FGNU, Institute of Health, Yakutsk, Republic Sakha (Yakutia), Russian Federation
4
Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany

KEY WORDS human populations; Evenks; Evens; molecular anthropology

ABSTRACT The Evenks and Evens, who speak closely bors rather than with linguistically related peoples. In
related languages belonging to the Northern Tungusic this study, we assess the correlation between linguistic
branch of the Tungusic family, are nomadic reindeer and genetic relationship in three different subgroups of
herders and hunters. They are spread over an immense Evenks and Evens, respectively, via mtDNA and Y-chro-
territory in northeastern Siberia, and consequently dif- mosomal analyses. The results show that there is some
ferent subgroups are in contact with diverse peoples evidence of a common origin based on shared mtDNA
speaking Samoyedic, Turkic, Mongolic, Chukotka-Kam- lineages and relatively similar Y-haplogroup frequencies
chatkan, and Yukaghir languages. Nevertheless, the amongst most of the Evenk and Even subgroups.
languages and culture of the Evenks and Evens are sim- However, there is little sharing of Y-chromosomal STR
ilar enough for them to have been classified as a single haplotypes, indicating that males within Evenk and
ethnic group in the past. This linguistic and cultural Even subgroups have remained relatively isolated. There
similarity indicates that they may have spread over is further evidence of some female admixture in different
their current area of habitation relatively recently, and Even subgroups with their respective geographic neigh-
thus may be closely related genetically. On the other bors. However, the Tungusic groups, and especially the
hand, the great distances that separate individual Evenks, show signs of genetic drift, making inferences
groups of Evens and Evenks from each other might about their prehistory difficult. Am J Phys Anthropol
have led to preferential mating with geographic neigh- 133:1013–1027, 2007. V 2007 Wiley-Liss, Inc.
C

The peoples of Central and Northeastern Siberia fering mainly in phonological and lexical features (Kon-
belong to different language families and practice differ- stantinova, 1964). The Even dialects, on the other hand,
ent modes of subsistence: in southern Siberia, they are are judged to be more divergent, especially the western
mainly pastoralists speaking Turkic or Mongolic lan- dialects. These are not understood by speakers of east-
guages, while the populations to the north are mainly ern dialects, nor do Western Evens understand Eastern
fully nomadic reindeer herders and hunters, such as the Evens. The central Even dialects, on the other hand,
Tungusic-speaking Evenks and Evens and the Yuka- are mutually comprehensible with the eastern dialects
ghirs, as well as a Turkic-speaking cattle- and horse- (Novikova, 1960). Both groups practice hunting and
breeding enclave, the Yakuts. Amongst all the Siberian reindeer herding, harnessing their reindeer to sleds in
peoples, the Evenks and Evens stand out through their
widely dispersed area of settlement: although according Grant sponsor: Max Planck Society; Grant sponsor: Wenner-Gren
to the 2002 census there were only 35,000 Evenks and Foundation for Anthropological Research; Grant number: 6828;
19,000 Evens in the Russian Federation (Federal’naja Grant sponsor: Russian Foundation for Basic Research (RFBR);
Sluzhba Gosudarstvennoj Statistiki, 2004), the Evenks Grant number: 03-06-96033p2003ap a_a.
are spread from the Taymyr Peninsula and Yenissey
*Correspondence to: Brigitte Pakendorf, Max Planck Institute for
river in the northwest to the Amur river and Sea of
Evolutionary Anthropology, Deutscher Platz 6, D-04103 Leipzig,
Okhotsk in the southeast (a distance of *3,200 km), and Germany. E-mail: pakendorf@eva.mpg.de
the Evens are settled in an area from the upper reaches
of the Yana river in the west to the Sea of Okhotsk
Present address of Innokentij N. Novgorodov: Department of For-
and Kamchatka in the east, a distance of *1,900 km eign Languages, Faculty of Information Technology, The Yakut State
(Evstigneev, 2003). The closely related Evenk and Even Engineering and Technical Institute, Yakutsk, Republic Sakha
languages both belong to the Northern Tungusic branch (Yakutia), Russian Federation.
of the family (Comrie, 1981; Atknine, 1997); each is split
into a large number of dialects, reflecting the wide Received 28 September 2006; accepted 24 January 2007
dispersal of the population (Novikova, 1960; Nedjalkov,
1997). Notwithstanding the enormous geographical dis- DOI 10.1002/ajpa.20590
tances separating the Evenk dialects, they are claimed Published online 9 May 2007 in Wiley InterScience
to be close enough to enable mutual comprehension, dif- (www.interscience.wiley.com).

C 2007
V WILEY-LISS, INC.
1014 B. PAKENDORF ET AL.

winter and riding them in summer. Because of their of how closely related different Tungusic-speaking
close linguistic and cultural similarity, in the past, the groups are by studying mtDNA and Y-chromosomal vari-
two groups were often classified as one ethnic group ation in three subgroups of Evenks from the Evenk
called Tungus (Evstigneev, 2003). There are two differing National okrug, southern Yakutia, and the northern
hypotheses on the origins of the Northern Tungusic Amur oblast (both okrug and oblast are administrative
groups. The first, predominantly supported by Okladni- divisions in the Russian Federation) and in three sub-
kov (cf. references in Tugolukov, 1980) and Vasilevich groups of Evens from central and eastern Yakutia and
(1969), holds that the Evenks and Evens are the de- the Magadan oblast, and comparing them with neighbor-
scendants of neolithic populations that were settled in ing groups: Yakut-speaking Evenks from northwestern
South Siberia *3,000 to 4,000 years ago. According to Yakutia, Yakuts, Yukaghirs, Koryaks, and Tuvans. In
Okladnikov (cf. references in Tugolukov, 1980), these ne- particular, we consider to what extent Evenks and Evens
olithic ancestors of the Evenks and Evens were reindeer- intermarried with their geographic neighbors, rather
herders; the modern-day Tungusic populations of the than choosing a mate from a more distantly located, but
Amur region and Manchuria lost their reindeer-herding linguistically and culturally closely affiliated group, and
culture after migrating to the southeast. In the middle of whether there are differences with respect to female and
the first millenium AD, the arrival of Turkic groups on male admixture.
the shores of Lake Baykal is assumed to have split the
ancestors of the northern Tungus (Evenks and Evens) MATERIALS AND METHODS
into a western and eastern group; this led to their
migration to the north and initiated the formation of the Samples and DNA extraction
Evenks and Evens as separate peoples without contact In December 2003, 46 cheek swab samples were
with the Tungusic-speaking groups from the Lower collected from healthy Even men in the Eveno-Bytantay
Amur (Vasilevich, 1969). The second hypothesis takes district and the village of Topolinoe, Tompo district,
the opposite view: according to this, the Evenks and Republic Sakha (Yakutia). These were augmented by
Evens are believed to have originally been horse-herders four Even maternal lineages from the Yukaghir village
settled in Manchuria, possibly migrating to the Middle of Andryushkino (Nizhnekolyma district, Republic Sakha
Amur or Transbaykal region, where they adopted (Yakutia)), which were collected in 1995. The Even sam-
domesticated reindeer, under pressure of immigrating ples were divided into Western and Central Even sub-
Dagurs (Tugolukov, 1980; Janhunen, 1996). Their migra- groups on the basis of dialectal distinctions (Novikova,
tion further to the north is assumed to have taken place 1960); in five cases, the maternal and paternal lineages
relatively recently, in the 12th and early 13th century came from different subgroups, so that the number of
AD, while their spread over the vast area they inhabit Western and Central Evens differed for the mtDNA
today is believed to have been initiated by the Yakuts, and Y-chromosome analyses (cf. Tables 1 and 5). A fur-
who migrated to the Middle Lena from near Lake ther sample of 65 published Even sequences from the
Baykal in the 13th and 14th century (Tugolukov, 1980; Magadan oblast, who belong to the Eastern dialect
Janhunen, 1996). The Russian colonization of Siberia, group, was taken from the literature (Derenko, 1997).
which began in the 17th century, led to large-scale popu- For the Y-chromosomal analyses, we included published
lation movements in the area, and it is during this time Y-chromosomal SNP data from a mixed sample of 31
that some Evenk and Even groups spread further to Evens from the Kolyma River (Yakutia) and the Maga-
the northwest, southeast, and northeast, partly under dan oblast (Karafet et al., 2002, Karafet, personal com-
the pressure of the spreading Yakuts (Dolgikh, 1960; munication). Evens in both areas speak dialects belong-
Vasilevich, 1969). The latest migration was that of the ing to the Eastern dialectal group (Novikova, 1960). We
Evens to the Kamchatka Peninsula in the middle of the were thus able to compare three subgroups of Evens
19th century (Spevakovsky, 1994). belonging to the three major Even dialectal divisions
If the hypothesis of Vasilevich (1969) is correct, then (Western, Central, and Eastern) in both mtDNA and Y-
Evenks and Evens have constituted separate ethnic chromosomal analyses.
groups for *1,500 years, whereas the hypothesis pro- Twenty-four Evenk DNA samples collected in 2001 in
posed by Tugolukov (1980) and Janhunen (1996) suggests Iengra village in the administrative territory of Neryun-
a much more recent shared ancestry of the Northern gri, Republic Sakha (Yakutia) were obtained from the
Tungusic groups. The two hypotheses predict differing DNA sample collection of the Institute of Health,
degrees of genetic relatedness of Evenks and Evens, Yakutsk. These were augmented by one Evenk maternal
with Vasilevich’s hypothesis predicting a deeper split lineage from the Megino-Kangalas district of the Repub-
between the groups, while the recent spread hypothesis lic Sakha (Yakutia) and two Evenk paternal lineages
predicts genetic unity within and between these ethnic from the Olenëk and Verkhoyansk districts, respectively.
groups. However, since they are spread over such a vast Since the majority of these Evenk samples came from
territory, it is possible that they have admixed with their women, only nine unrelated Iengra Evenks were avail-
immediate neighbors rather than finding ethnically and able for Y-chromosomal analyses. In addition, mtDNA
linguistically related marriage partners in a distant com- and Y-chromosomal data for a sample of 40 Evenks from
munity. Although Evenk and Even samples have been several villages in the Evenk National okrug (mainly
included in previous broad areal studies of genetic diver- along the Stony Tunguska River) were included (Paken-
sity and linkage disequilibrium (Posukh et al., 1990; Tor- dorf et al., 2006). These are labeled as Stony Tunguska
roni et al., 1993; McComb et al., 1995; Kaessmann et al., Evenks (abbreviated as STE) in this article. Published
2002; Karafet et al., 2002; Starikovskaya et al., 2005; mtDNA sequence data for 47 Evenks from the northern
Derenko et al., 2006), the correlation of genetic affilia- Amur oblast (Kaessmann et al., 2002) were included in
tion with linguistic relationship within the Northern the mtDNA comparisons, and published Y-chromosomal
Tungusic groups has not yet been the focus of a molecu- SNP data from 78 ‘‘Eastern Evenks’’ (Karafet et al.,
lar anthropological study. Here, we address the question 2002) were included in the Y-chromosomal analyses.

American Journal of Physical Anthropology—DOI 10.1002/ajpa


TABLE 1. mtDNA haplogroup frequencies in Siberian populations (absolute numbers, % in parentheses)
W. Evens C. Evens E. Evens STE Iengra Nyukzha YSE Yakuts Yukaghirs Koryaks Tuvans
N 24 26 65 39 23 47 32 178 22 155 59
Linguistic Tungusic Tungusic Tungusic Tungusic Tungusic Tungusic Turkic Turkic isolate or Uralic Chukotko-Kamchatkan Turkic
affiliation
Haplogroup
A 3 (4.6) 2 (5.1) 3 (13) 5 (10.6) 1 (3.1) 6 (3.4) 8 (5.2) 1 (1.7)
B 9 (5) 1 (4.5) 3 (5.1)
C 10 (41.7) 14 (53.8) 17 (26.2) 30 (76.9) 4 (17.4) 20 (42.6) 9 (28.1) 68 (38.2) 12 (54.5) 56 (36.1) 34 (57.6)
D (excl. D5, D5a) 8 (33.3) 7 (26.9) 10 (15.4) 6 (15.4) 6 (26.1) 6 (12.8) 9 (28.1) 26 (14.6) 5 (22.7) 2 (1.3) 7 (11.9)
D5 and D5aa 1 (4.2) 1 (3.8) 7 (30.4) 3 (6.4) 4 (12.5) 28 (15.7) 1 (4.5) 2 (3.4)
F 3 (12.5) 1 (3.8) 1 (1.5) 1 (2.6) 3 (9.4) 13 (7.3) 2 (3.4)
G1 1 (3.8) 7 (10.8) 2 (8.7) 2 (9.1) 65 (41.9)
G other 1 (3.1) 8 (4.5) 3 (5.1)
Y 7 (10.8) 2 (1.1) 15 (9.7) 3 (5.1)
Z 1 (4.2) 2 (7.7) 17 (26.2) 1 (4.3) 5 (10.6) 1 (3.1) 1 (0.6) 1 (4.5) 9 (5.8)
M 1 (4.2) 1 (3.1) 2 (1.1) 1 (1.7)
H 3 (9.4) 4 (2.2)
J 1 (1.5) 2 (4.3) 1 (0.6)
K 1 (0.6)
T 2 (1.1) 1 (1.7)
U 2 (1.1) 1 (1.7)
W3 2 (1.1)
SIBERIAN mtDNA AND Y-DNA VARIATION

Not assigned 2 (3) 6 (12.8) 3 (1.7) 1 (1.7)

STE, Stony Tunguska Evenks; Iengra, Iengra Evenks; Nyukzha, Nyukzha Evenks; YSE, Yakut-speaking Evenks. Data for STE, YSE, Yakuts, Yukaghirs and Tuvans from Paken-
dorf et al. (2006); for Koryaks from Schurr et al. (1999).
a
Sequences with mutations at 16189-16223-16266-16362 were defined as belonging to subhaplogroup D5a; sequences lacking the mutation at 16266 were assigned to subha-
plogroup D5.

American Journal of Physical Anthropology—DOI 10.1002/ajpa


1015
1016 B. PAKENDORF ET AL.
TABLE 2. mtDNA diversity values in Evens and Evenks compared to neighboring groups
N n h SE MPD SE Reference
Western Evens 24 15 0.95 0.03 5.64 2.80 This study
Central Evens 26 13 0.93 0.02 5.26 2.63 This study
Eastern Evens 65 29 0.95 0.01 6.21 2.99 Derenko (1997)
Stony Tunguska Evenks 39 16 0.92 0.02 5.10 2.53 Pakendorf et al. (2006)
Iengra Evenks 23 12 0.94 0.03 5.51 2.75 This study
Nyukzha Evenks 47 16 0.91 0.02 6.00 2.91 Kaessman et al. (2002)
Yakut-speaking Evenks 32 18 0.95 0.02 6.37 3.10 Pakendorf et al. (2006)
Yakuts 178 62 0.96 0.01 6.60 3.13 Pakendorf et al. (2006)
Yukaghirs 22 13 0.94 0.03 5.62 2.80 Pakendorf et al. (2006)
Koryaks 147 37 0.92 0.01 5.76 2.77 Schurr et al. (1999)
Tuvans 59 34 0.96 0.01 5.57 2.71 Pakendorf et al. (2006)

n, number of haplotypes; h, haplotype diversity; MPD, mean number of pairwise differences.

TABLE 3. Shared mtDNA haplotypes and pairwise Fst values between Tungusic-speaking groups and their neighbors
Iengra Nyukzha
W. Evens C. Evens E. Evens STE Evenks Evenks YSE Yakuts Yukaghirs Koryaks Tuvans
W. Evens 15 0.02 0.06 0.08 0.07 0.05 0.00 0.00 0.03 0.07 0.02
C. Evens 6 13 0.05 0.02 0.11 0.01 0.04 0.03 0.02 0.06 0.00
E. Evens 6 7 29 0.13 0.12 0.07 0.07 0.06 0.05 0.03 0.06
STE 4 5 3 16 0.21 0.06 0.12 0.08 0.04 0.12 0.02
Iengra Evenks 5 3 3 3 12 0.08 0.01 0.03 0.11 0.15 0.12
Nyukzha Evenks 4 4 4 4 8 16 0.04 0.04 0.04 0.10 0.03
YSE 5 6 4 5 4 5 18 0.00 0.04 0.08 0.05
Yakuts 13 8 11 9 7 8 12 62 0.03 0.06 0.03
Yukaghirs 5 6 4 4 4 5 6 8 13 0.04 0.01
Koryaks 3 2 14 1 2 2 1 3 6 37 0.06
Tuvans 4 6 5 6 4 5 5 12 5 3 34

Diagonal values (indicated by bold values) show the number of haplotypes within populations.
Values above the diagonal values are the pairwise Fst values between populations; bold italic values are values that are not signifi-
cantly different (5% level) without Bonferroni correction.
Values below the diagonal values are the number of shared haplotypes between populations.

TABLE 4. AMOVA analyses based on mtDNA sequences


%Variance
Grouping Between groups Within groups Within populations
All together 5.62b 94.38
Linguistic affiliation 1.52a 4.53b 93.94b
Linguistics, Tungusic subgroups 1.75a 4.34b 93.9b
Geography 2.57b 3.37b 94.06b
MDS Tungusic 5.27b 1.11a 93.62b
Evens and Evenks grouped 1.05c 5.15b 93.8b

Linguistic affiliation: Turkic ¼ Yakuts, YSE, Tuvans, Tofa, Todzha, Soyots, Khakas, Altai, Kazakh, Kirghiz; Tungusic ¼ STE, Iengra,
Nyukzha, C. Evens, W. Evens, E. Evens (subgroups ¼ Evens vs. Evenks); Mongolic ¼ Buryats, Mongols; isolates ¼ (1) Koryaks. (2) Yukaghirs.
Geography: N/NE ¼ Yakuts, YSE, Yukaghirs, STE, C. Evens, W. Evens; E ¼ Koryaks, E. Evens; SE ¼ Iengra, Nyukzha; S ¼ Bury-
ats, Mongols, Soyots; SW ¼ Tuvans, Khakas, Tofa, Todzha, Altai; Central Asia ¼ Kazakh, Kirghiz.
MDS Tungusic: Group 1 ¼ W. Evens, Yakuts, YSE; Group 2 ¼ Koryaks, E. Evens; Group 3 ¼ Yukaghirs, C. Evens, Tuvans; Group 4
¼ STE; Group 5 ¼ Iengra; Group 6 ¼ Nyukzha.
Evens and Evenks grouped: Group 1 ¼ W. Evens, E. Evens, C. Evens; Group 2 ¼ STE, Iengra, Nyukzha; Group 3 ¼ Yakuts, YSE;
Group 4 ¼ Koryaks; Group 5 ¼ Yukaghirs.
a
P < 0.05.
b
P < 0.01.
c
P > 0.2.

Since these samples all came from villages along the They were unrelated up to the grandparental generation
Nyukzha River or nearby (Wiebe, personal communica- as far as could be established, and were asked to name
tion, Karafet, personal communication), they are labeled the birthplace and ethnicity of their parents and grand-
as Nyukzha Evenks in this article. We were thus able to parents to exclude known admixture from other ethnic-
compare three geographical subgroups of Evenks belong- ities.
ing to two different dialectal groups: southern (Stony DNA was extracted from the blood samples collected
Tunguska Evenks) and eastern (Iengra and Nyukzha from the Iengra Evenks following a standard phenol-chlo-
Evenks). roform protocol (Maniatis et al., 1982), while DNA from
All donors were healthy individuals who voluntarily the cheek swab samples collected from the Evens was
gave their sample after informed consent was obtained. extracted using a salting-out method (Miller et al., 1988).

American Journal of Physical Anthropology—DOI 10.1002/ajpa


SIBERIAN mtDNA AND Y-DNA VARIATION 1017
The Evenk and Even groups were compared to a num-

Referencesd
ber of populations from Siberia and Central Asia, the

1
1
2
3
1
2
3
3
3
2
3
data for which were taken from the literature: for both

1 ¼ This study; 2 ¼ Karafet et al. (2002), the Eastern Evens are there called ‘‘Evens,’’ the Nyukzha Evenks are there called ‘‘Eastern Evenks’’; 3 ¼ Pakendorf et al. (2006).
the mtDNA analyses and Y-chromosomal SNP and STR
analyses, they were compared to northeastern Siberian
Yakuts, Yakut-speaking Evenks, Yukaghirs, and South
4 (12.9)
Other

5 (6.4)

1 (8.3)
Siberian Tuvans (Pakendorf et al., 2006). In addition, for
the mtDNA analyses, they were compared with north-
eastern Siberian Koryaks (Schurr et al., 1999), with

12 (21.8)
R-M17

2 (6.1) South Siberian Buryats (Pakendorf et al., 2003) and


4 (2.2)
NA

NA

NA
South Siberian Turkic Khakas, Tofalar, Todzhins, Soyots,
and Altaians (Derenko et al., 2003), as well as with
TABLE 5. Y-chromosomal haplogroup frequencies in several Siberian populations (absolute numbers, % in parentheses)

Central Asian Mongols (Kolman et al., 1996), Kazakhs,


R-M173

4 (7.3) and Kirghiz (Comas et al., 1998). For comparisons on


the basis of Y-chromosomal SNP data, they were com-

Karafet et al. (2002) analyzed M178 in addition TatC and gave only numbers for M178, however, all individuals with TatC also had M178.
pared with the populations analyzed by Karafet et al.
(2002), since these offered the highest resolution. Figure 1
(30.8)
(16.7)
(16.4)
Q-P36

(0.5)

shows the approximate location of the eleven northeast-


ern Siberian populations analyzed here and used for
1
4
2
9

comparison in all of the analyses.


O-M122

1 (8.3)
1 (1.8)

Karafet et al. (2002) analyzed P14, not M89, this appears to be a parallel mutation to M89 (Jobling and Tyler-Smith, 2003).

mtDNA analyses
Both strands of the mtDNA HVR1 were sequenced
9 (37.5)

11 (27.5)

(9.1) 15 (27.3)

in all samples, using previously-described methods


1 (4.5)

(72.7) 2 (6.1)
1 (0.5)
N-P43

(Pakendorf et al., 2006). Samples that broke off after the


stretch of cytosines resulting from the T-C transition at
nucleotide position (np) 16189 were sequenced twice in
20 (90.9)

4 (12.9)

(22.2)
(20.5)

(30.8)
(33.3)
N-TatCc

each direction to ensure double coverage of each np.


2 (8.3)

(94)

Samples were assigned to mtDNA haplogroups on


16
24
173
2

4
4
5

the basis of their sequence motifs as well as by RFLP-


assays, as described elsewhere (Pakendorf et al., 2006).
N-LLY22g

Haplogroup Z was not confirmed by RFLP-assay, since


1 (1.8)

the sequence motif is unambiguous (16185-16223-16260-


16298). The Western and Central Even and Iengra Evenk
sequences will be available online after publication
(http://www.eva.mpg.de/genetics/files/pubs_stoneking.html)
1 (11.1)
K-M9

and will also be submitted to HvrBaseþþ (http://www.


NA: not applicable; STE: Stony Tunguska Evenks; YSE: Yakut-speaking Evenks.

hvrbase.org/).
F-M89b J-M172

Y-chromosomal analyses
1 (1.3)

1 (0.5)

Fourteen Y-chromosomal single nucleotide polymor-


phisms known to be of relevance in Siberian populations
1 (2.5)

1 (1.3)

1 (7.7)

(M9, RPS4Y, M217, M48, M86, M172, Tat, LLY22g, P43,


M122, P36, M207, M173, and M17) were typed in the
Western and Central Evens and Iengra Evenks. Initially,
M9 and RPS4Y were screened in all samples following
4 (44.44)
C-M86a

19 (61.3)

42 (53.8)
4 (12.1)

2 (15.4)

the method by Kayser et al. (2006). Further SNPs were


1(4.5)

1 (0.5)

5 (9.1)

Karafet et al. (2002) analyzed only M86, not M48.


12 (50)

28 (70)

then typed in a hierarchical manner on the background


of these two SNPs, using previously-described methods
(Pakendorf et al., 2006).
2 (22.2)
C-M48

1 (7.7)

Nine short tandem repeat (Y-STR) loci (DYS19,


1 (3)
NA

NA

NA

DYS385I, DYS385II, DYS389I, DYS389II, DYS390,


DYS391, DYS392, and DYS393) were typed in these
three groups using previously-described methods (Kayser
31 4 (12.9)

Nyukzha Evenks 78 13 (16.7)

12 4 (33.3)
C-M217

24 1 (4.2)

184 3 (1.6)
13 1 (7.7)

55 3 (5.5)

et al., 1997, 2003; Redd et al., 1997). The STR haplo-


types will be available online (http://www.eva.mpg.de/
genetics/files/pubs_stoneking.html) after publication and
will also be submitted to the Y Chromosome Haplotype
9
22

40

33
N

Reference Database (http://www.yhrd.org/index.html).


Iengra Evenks

Statistical analyses
Yukaghirs

The software MEGA ver. 2.1 (Kumar et al., 2001) was


W. Evens
C. Evens
E. Evens

Koryaks
Tuvans

used to infer the haplogroup affiliation of mtDNA


Yakuts
YSE

sequences by visualizing the segregating sites. Parame-


STE

ters of molecular diversity of the mtDNA sequences and


d
a
b
c

American Journal of Physical Anthropology—DOI 10.1002/ajpa


1018 B. PAKENDORF ET AL.

Fig. 1. Map showing the approximate location of the Tungusic-speaking populations and their closest neighbors.

Y-chromosomal SNPs and STRs, as well as pairwise and D in the Tungusic-speaking groups and their neigh-
Fst values between populations and analyses of molecu- bors were constructed using the program Network ver.
lar variance (AMOVA) from the mtDNA sequence data 4.1 (www.fluxus-engineering.com) with the following
were calculated using the program Arlequin ver. 2.000 sites downweighted to 2: 16093, 16129, 16172, 16187,
(Schneider et al., 2000). The significance of Fst values 16189, 16209, 16223, 16234, 16256, 16278, 16290, 16291,
was tested with 10,000 permutations. The program pack- 16293, 16294, 16304, 16311, 16320, 16355, 16362. In the
age Statistica ver. 7.1 (StatSoft, Inc.) was used to per- network consisting of haplogroup D sequences, np 16093
form multidimensional scaling analyses (MDS) of the was downweighted to 1, to reduce excessive reticulation.
pairwise Fst values for both the mtDNA and Y-chromo- The Network program was also used to assess the qual-
somal data. Mantel tests to assess the correlation ity of the sequences generated for this study as described
between mtDNA and Y-chromosomal variation, as well by Bandelt et al. (2002). Furthermore, MJ-networks
as between mtDNA variation and geography, and Y-chro- were constructed from Y-STR haplotypes with individual
mosomal variation and geography, were performed in STRs weighted relative to their mutation rate (Kayser
Arlequin ver. 3.01 (Excoffier et al., 2005). For this, we et al., 2000) as described elsewhere (Kasperaviciute
analyzed the correlation between Fst matrices calculated et al., 2004). For the network consisting of Y-haplogroup
from mtDNA sequences and Y-SNP frequency (in 11 pop- C3 haplotypes, DYS389II was downweighted to 1 and
ulations), from mtDNA sequences and Y-STRs (in eight DYS385II was downweighted to 2, to resolve excess
populations), from mtDNA haplogroup frequency and Y- reticulation.
SNP frequency (in 11 populations), from mtDNA sequen-
ces and mtDNA haplogroup frequency and geographical
great circle distances, respectively, as well as from Y- RESULTS
SNP frequency and Y-STRs and geographical distances, mtDNA analyses
respectively. A SAMOVA (Spatial Analysis of Molecular
Variance; Dupanloup et al., 2002) analysis with the HVR The accuracy of the sequences was evaluated following
1 sequence data was performed with the program the method of Bandelt et al. (2002), in which the sites
SAMOVA 1.0 (http://web.unife.it/progetti/genetica/Isabelle/ they determined as ‘‘speedy’’ were removed from the
samova.html). Median-joining networks (Bandelt et al., data and a RM-network (Bandelt et al., 1995) was con-
1999) of HVR1 sequences belonging to haplogroups C structed from the remaining slowly-evolving sites and

American Journal of Physical Anthropology—DOI 10.1002/ajpa


SIBERIAN mtDNA AND Y-DNA VARIATION 1019
checked for excessive reticulations. The resulting net-
work contained no reticulations, indicating that the
sequences are free of artefacts at these sites (data not
shown).
There were three heteroplasmic sites in three of the
73 sequences generated for this study: nucleotide posi-
tion (np) 16189 was heteroplasmic for T and C in one
Western Even sample (ht11a in Online Supplement 1),
16258 was heteroplasmic for A and G in another
Western Even sample (ht26a in Online Supplement 1),
and 16311 was heteroplasmic for T and C in an Iengra
Evenk sample (ht12a in Online Supplement 1). The
heteroplasmic sites were treated as missing data in all of
the analyses.
Table 1 presents the frequency of haplogroups found
in the Tungusic-speaking groups in comparison with
their neighbors. The Western and Central Evens are
characterized by high frequencies of haplogroups C and
D and low frequencies of the northeastern Siberian hap- Fig. 2. MDS plot based on pairwise Fst values from mtDNA
logroups G1 and Z (Schurr et al., 1999; Starikovskaya sequences between Tungusic-speaking populations and their im-
et al., 2005). However, they are also characterized by low mediate neighbors.
frequencies of subhaplogroups F1b and D5a, which are
more common in Southern Siberia and Central Asia
than in Northern Siberia (Yao et al., 2004; Starikovskaya same number of haplotypes with other Even subgroups
et al., 2005). The Eastern Evens differ from the Western as with Yakuts, Yukaghirs, and Tuvans, and do not differ
and Central Evens in having a lower frequency of significantly from Western Evens, Yukaghirs, Stony
haplogroups C and D, and a much higher frequency of Tunguska Evenks, Nyukzha Evenks, and Tuvans. The
haplogroups G1, Z, and Y. Haplogroup G1 is found at Eastern Evens share nearly half of their haplotypes (14/
high frequency in Kamchatkan Koryaks and Itelmen 29) with Koryaks, twice as much as with the other Even
(Schurr et al., 1999), and haplogroup Y is found predomi- subgroups. The Stony Tunguska Evenks share only a
nantly in populations of the Lower Amur/Sakhalin region quarter of their haplotypes (3 and 4/16, respectively)
as well as on Kamchatka (Starikovskaya et al., 2005). with the Iengra and Nyukzha Evenks, while the Iengra
The Iengra Evenks have a low frequency of hap- Evenks have three quarters of their haplotypes (8/12) in
logroup C (17.4%) compared to nearly 77% found in the common with Nyukzha Evenks (Table 3). The Iengra
sample of Stony Tunguska Evenks (cf. Table 1). They Evenks do not differ significantly from Yakut-speaking
have a relatively high frequency of haplogroup D, and a Evenks, and neither the Stony Tunguska Evenks nor the
very high frequency (30%) of subhaplogroup D5a; this is Nyukzha Evenks differ significantly from the Central Evens.
higher than the frequency of this subhaplogroup in The MDS plot based on pairwise Fst values between
Yakuts (15.7%) and a much higher frequency than that the various subgroups of Evens and Evenks and their clos-
recorded in South Siberian and Central Asian popula- est neighbors (Yakuts, Yakut-speaking Evenks, Yukaghirs,
tions (Yao et al., 2002, 2004; Derenko et al., 2003; Koryaks and Tuvans) shows that neither the subgroups of
Starikovskaya et al., 2005; Pakendorf et al., 2006). This Evens nor the subgroups of Evenks group together.
is in striking contrast to the sample of Stony Tunguska Instead, the Western Evens are closest to the Yakuts
Evenks who have only 15% of haplogroup D, with no and Yakut-speaking Evenks, the Central Evens are clos-
individuals belonging to haplogroup D5a. Like the est to Yukaghirs and Tuvans, and the Eastern Evens are
Evens, the Iengra Evenks have low frequencies of the closest to Koryaks (Fig. 2). However, in the third dimen-
Siberian haplogroups G1 and Z (Table 1). The Nyukzha sion, the Western Evens are separated from the Yakuts
Evenks have a high frequency of haplogroup C, and a and Yakut-speaking Evenks, and the Eastern Evens are
low frequency of haplogroup D5a. In addition, they have separated from the Koryaks, while the Central Evens,
a relatively high frequency of haplogroup Z (Table 1). Yukaghirs, and Tuvans continue to cluster together
Haplogroups characteristic of European populations were (data not shown). This cluster is not resolved even when
not found in the Tungusic-speaking groups (Table 1), with including other South Siberian Turkic populations in the
the exception of one individual in the Eastern Evens and analysis (data not shown). The Evenk populations do not
two individuals in the Nyukzha Evenks belonging to hap- cluster either with each other or with the Evens. In fact,
logroup J. As shown by Table 2, the diversity values found the Stony Tunguska Evenks are most distant from the
in the Evens and Evenks fall within the range of their Iengra Evenks, with a Fst value of 0.21 separating the
neighboring populations, although the Nyukzha and two.
Stony Tunguska Evenks are at the lower end of the scale A MJ-network based on mtDNA sequences belonging
(as are the Kamchatkan Koryaks). to haplogroup C from the Tungusic-speaking groups and
Table 3 shows the number of haplotypes shared be- their neighbors (Fig. 3) shows that the three major hap-
tween pairs of populations as well as pairwise Fst values lotypes (indicated by asterisks in Fig. 3) are shared
between them. The Western Evens share nearly all of widely in practically all populations compared; these are
their haplotypes with Yakuts (13/15), more than with also shared by South Siberian Turkic populations and
other Even subgroups, and the Fst values between them Mongolic-speaking Mongols and Buryats (Pakendorf
and Yakuts, Yakut-speaking Evenks, Central Evens, et al., 2006). Furthermore, the Eastern Evens share
Yukaghirs, and Tuvans are not significantly different some haplotypes with Koryaks, three exclusively (Types
from zero. The Central Evens share approximately the 1, 2, and 3 in Fig. 3), one is also shared with Buryats,

American Journal of Physical Anthropology—DOI 10.1002/ajpa


1020 B. PAKENDORF ET AL.

Fig. 3. MJ-network based on mtDNA haplogroup C sequen-


ces in Tungusic-speaking populations and their immediate
neighbors. For the significance of the labelled haplotypes, see
text. Nodes are drawn proportional to number of individuals
carrying a specific haplotype (between 1 and 42), and branch Fig. 4. MJ-network based on mtDNA haplogroup D sequen-
lengths are proportional to number of mutational steps. a ¼ ces in Tungusic-speaking populations and their immediate
Stony Tunguska Evenks, b ¼ Iengra Evenks, c ¼ Nyukzha neighbors. For the significance of the labeled haplotypes, see
Evenks, d ¼ Western Evens, e ¼ Central Evens, f ¼ Eastern text. Nodes are drawn proportional to number of individuals
Evens, g ¼ Yukaghirs, h ¼ Koryaks, i ¼ Yakuts, k ¼ Yakut- carrying a specific haplotype (between 1 and 32), and branch
speaking Evenks. lengths are proportional to number of mutational steps. a ¼
Stony Tunguska Evenks, b ¼ Iengra Evenks, c ¼ Nyukzha
Evenks, d ¼ Western Evens, e ¼ Central Evens, f ¼ Eastern
Evens, g ¼ Yukaghirs, h ¼ Koryaks, i ¼ Yakuts, k ¼ Yakut-
Todzha, and Tuvans (Type 4 in Fig. 3; Buryat, Tuvan
speaking Evenks.
and Todzha types are not shown in the figure). Addi-
tional sharing of haplotypes between Eastern Evens and
Koryaks also occurs for haplogroups G1, Y, and Z (data
not shown). Haplogroup C sequences shared between (Fig. 2). This is further confirmed by the SAMOVA anal-
Western Evens and Yakuts are also shared with other yses, in which the Western Evens persistently group
groups; either they are shared with most populations with Yakuts and Yakut-speaking Evenks, the Central
(the asterisked haplotypes), or they are shared with Cen- Evens persistently group with Yukaghirs, and the East-
tral and/or Eastern Evens (Types 5 and 6 in Fig. 3) and ern Evens and Koryaks form a separate group when
Yukaghirs (Type 7 in Fig. 3). defining K ¼ 3 and K ¼ 4, although they are separated
A MJ-network consisting of haplogroup D sequences from each other after that (data not shown).
in the Tungusic-speaking groups and their neighbors
(Fig. 4) shows that there is very little haplotype sharing Y-chromosomal analyses
amongst the different Even subgroups, with only one
haplotype found in all three groups (arrow in Fig. 4). The evolutionary tree of the Y-chromosomal SNPs ana-
Some sequences are shared between Western Evens and lyzed here is shown in Figure 5; markers M48 and M86,
Yakuts that are not shared with other Evens (Types 1, 2, which previously were thought to be parallel mutations
and 3 in Fig. 4), while two are shared between Eastern that defined the C3c haplogroup (Jobling and Tyler-
Evens and Yakuts (Types 4 and 5 in Fig. 4). None of the Smith, 2003), are here separated. Two Iengra Evenks, as
sequences are shared between all three Evenk sub- well as one Yakut-speaking Evenk and one Yukaghir
groups, nor are any types shared between Stony Tung- have the derived state at M48, but the ancestral state at
uska and Iengra Evenks. Some types (1, 4, and 6 in Fig. M86. Thus, the derived state at M48 and the ancestral
4) are shared between Iengra and Nyukzha Evenks; state at M86 defines subhaplogroup C3c*, while the
these are also shared with Yakuts. derived state at M86 further defines subhaplogroup
The AMOVA analyses (Table 4) show that neither lin- C3c1. Since in general only one or the other marker is
guistic affiliation nor geography is a good predictor of analyzed in studies of Eurasian population prehistory
genetic relationship amongst 20 North and Central (e.g. M48 in Zerjal et al., 2002; M86 in Karafet et al.,
Asian populations, with the between-group variance 2002), the geographic distribution of subhaplogroup C3c*
being smaller than the within-group variance. However, is not known.
geography provides a slightly better fit than language. Table 5 presents the Y-haplogroup frequencies in the
The analyses further confirm the genetic heterogeneity Even and Evenk subgroups in comparison to those found
of the Tungusic groups: grouping the three Even sub- in several neighboring groups. The Western Evens differ
groups, on the one hand, and the three Evenki-speaking radically in their haplogroup frequencies from the
groups on the other, results in a poor and nonsignificant Central and Eastern Evens: the Western Evens are char-
fit to the genetic data. The analyses provide further con- acterized by very high numbers of haplogroup N-TatC,
firmation that the Even subgroups are closer to their ge- comparable to those found in their Yakut neighbors. In
ographic neighbors than to their linguistic neighbors, as contrast, both the Central Evens and the Eastern Evens
is also apparent in the MDS plot based on pairwise have high frequencies of haplogroups C-M86 (as do all of
Fst values between the Northern Siberian populations the Evenk groups), although the Central Evens also

American Journal of Physical Anthropology—DOI 10.1002/ajpa


SIBERIAN mtDNA AND Y-DNA VARIATION 1021
have a high frequency of haplogroup N-P43 (as do the individuals from this sample who were classified by Kar-
Stony Tunguska Evenks and Tuvans), while the Eastern afet et al. (2002) as belonging to haplogroup C-M217 in
Evens lack N-P43. All three Evenk subgroups are char- actual fact belong to haplogroup C-M48*, which is found
acterized by high frequencies of haplogroup C-M86 in two out of nine Iengra Evenks, since M48 was not
(Table 5); in addition, the Stony Tunguska Evenks have typed in this sample. The Nyukzha Evenks are further-
a high frequency of N-P43, which is absent in the other more characterized by intermediate frequencies of
two Evenk subgroups. The Nyukzha Evenks have a high haplogroup N-TatC (*20%), which is completely absent
frequency of C-M217, which contrasts them with the in the Stony Tunguska Evenks. The sample size of the
other Evenk subgroups; it might be that some of the Iengra Evenks is too low to allow much inference about
population history, although in general, haplogroup fre-
quencies are more similar to those in their geographic
neighbors, Nyukzha Evenks, than to those in the more
geographically-distant Stony Tunguska Evenks.
Pairwise Fst values between the Tungusic-speaking
groups and their neighbors confirm the large difference
between the Western Evens and the other Even sub-
groups as well as the Evenks (Table 6): the Western
Evens are separated from the other Evens by highly sig-
nificant Fst values of 0.54 and 0.52, respectively. The
Western Evens do not differ significantly from the
Yakuts and Yakut-speaking Evenks, populations which
are likewise characterized by high frequencies of hap-
logroup N-TatC (Tables 5 and 6). The Central Evens are
closer to the Stony Tunguska Evenks than to the East-
ern Evens and do not differ significantly from the for-
mer, while the Eastern Evens are not significantly differ-
ent from the Nyukzha Evenks. (Both Even subgroups
also do not differ significantly from the Iengra Evenks;
however, this might be due to the small sample size of
the latter.) The differences between the Central and
Eastern Even subgroups and the Western Even sub-
group are clearly apparent in a MDS plot based on pair-
wise Fst values between the Tungusic groups and their
closest neighbors (Fig. 6); here, the Western Evens are
outliers who fall close to the Yakuts, while the other
Tungusic-speaking groups cluster at the other end of the
plot. The Iengra and Nyukzha Evenks group quite
closely with the Central and Eastern Evens, while the
Stony Tunguska Evenks are somewhat separate. When
comparing the populations analyzed here with those an-
alyzed by Karafet et al. (2002), all the different Evenk
groups from Russia and China cluster together, as do
the Oroqen (a population living in northern China who
speak a closely related language). The Manchu, on the
other hand, who speak a language more distantly related
to the Northern Tungusic Evenk and Even languages,
are at some distance from the Northern Tungusic groups.
The Western Evens, however, are distinctly separate
from this general Tungusic cluster (data not shown).
AMOVA analyses based on Y-chromosomal SNP fre-
Fig. 5. Tree showing the evolutionary relationship of the Y-
quencies confirm that neither shared linguistic affiliation
chromosomal SNP markers analyzed in this study.

TABLE 6. Pairwise Fst values based on Y-chromosomal haplogroup frequencies


Iengra Nyukzha
W. Evens C. Evens E. Evens STE Evenks Evenks YSE Yakuts Yukaghirs Koryaks
C. Evens 0.54
E. Evens 0.52 0.09
STE 0.65 0.02 0.08
Iengra Evenks 0.48 0.09 0.02 0.16
Nyukzha Evenks 0.40 0.10 0.01 0.12 0.02
YSE 0.02 0.37 0.36 0.50 0.25 0.28
Yakuts 0.01 0.76 0.74 0.81 0.72 0.61 0.15
Yukaghirs 0.34 0.19 0.18 0.33 0.05 0.14 0.17 0.62
Koryaks 0.36 0.27 0.25 0.42 0.15 0.19 0.20 0.62 0.00
Tuvans 0.37 0.12 0.21 0.24 0.13 0.20 0.25 0.61 0.07 0.11

Italic values are values that are not significant at the 5% level without Bonferroni correction.

American Journal of Physical Anthropology—DOI 10.1002/ajpa


1022 B. PAKENDORF ET AL.

nor geographic proximity are good predictors of genetic C-M86 also had 13 and 14 repeats at this locus. Duplica-
relationships (Table 7). The analyses further confirm tions at DYS393 have been found in four individuals
the close affinities of the Western Evens with Yakut- from the Czech Republic, Turkey, and Poland, however
speaking Evenks and Yakuts, and of the Dolgans (a with very different haplotypes than the ones found in
group who speak a language very closely related to the Evens (http://www.yhrd.org/index.html, release 20,
Yakut) with the remaining Evens and Evenks: in this January 10, 2007). Also, a duplication of DYS19 involv-
grouping, 45% of the variation is due to differences ing alleles 16 and 17 was found in four Tuvan individu-
between groups, and only 5% of the variation is due to als in the sample analyzed in Pakendorf et al. (2006).
differences between the populations included in the indi- These four Tuvans belong to haplogroup C-M86; this
vidual groups. In contrast, when these populations are same duplication has been reported in Kalmyks (Nasidze
grouped strictly according to their linguistic affiliation, et al., 2005).
approximately the same amount of the variation is The Western Evens show a very low haplogroup diver-
accounted for by differences between populations within sity, much lower than that found in either the other
the groups as by differences between the groups. Even subgroups or the Evenks, and almost as low as
Typing nine Y-chromosomal STRs in the Western and that of Yakuts (Table 8). In their Y-STR diversity, how-
Central Even subgroups as well as in the Stony Tung- ever, they do not differ significantly from the Central
uska and Iengra Evenks revealed a duplication of the Evens. The Stony Tunguska Evenks, too, show reduced
DYS393 locus in four Evens: two Western Evens belong- haplogroup diversity and MPD values, as well as signifi-
ing to haplogroup N-TatC had 13 and 14 repeats at this cantly lower Y-STR haplotype diversity than that found
locus, and two Central Evens belonging to haplogroup in any of the other populations compared (Table 8).
As can be seen in Table 9, there is not much sharing
of Y-STR haplotypes amongst the Siberian populations.
As shown by pairwise Rst values, the Western Evens are
closer to the Yakut-speaking Evenks from northwestern
Yakutia than they are to the Central Evens, while the
Central Evens are closer to the Stony Tunguska and
Iengra Evenks than they are to the Western Evens. The
Iengra Evenks are not significantly different from the
Central Evens, Stony Tunguska Evenks, and Yukaghirs;
however, this may be an artefact of the small sample size.
A MJ-network of Y-STRs within haplogroup N-TatC
(Fig. 7) demonstrates that the Western Evens belonging
to this haplogroup are divided into two groups. Eight of
the Western Evens share their STR haplotypes with
Yakuts and Yakut-speaking Evenks, and two have a sin-
gle haplotype that is part of the Yakut-dominated half of
the network. The two individuals with the 13/14 duplica-
tion in DYS393 are indicated by asterisks; the location
of their haplotypes (identical to the two most frequent
haplotypes in Yakuts) in the figure comes from coding
Fig. 6. MDS plot based on pairwise Fst values from Y-chro- them as having 14 repeats (which we reconstruct as hav-
mosomal SNPs between Tungusic-speaking populations and ing been the ‘‘ancestral’’ state before the duplication);
their immediate neighbors. with 13 repeats at DYS393, they would be identical to

TABLE 7. AMOVA analyses based on Y-chromosomal haplogroups


%Variance
Grouping Between groups Within groups Within populations
All together 32.96a 67.04
Linguistic affiliation 7.45b 26.43a 66.12a
Linguistics, Tungusic subgroups 8.04 26.48a 65.48a
Geography 6.84c 26.88a 66.28a
Tungusic vs. Yakut-speaking 23.33b 21.19a 55.48a
W. Evens with Yakuts 44.97a 5.04a 49.99a

Linguistic affiliation: Uralic ¼ Komi, Khanty, Selkup, Forest Nenets, Tundra Nenets, Nganasan; Turkic ¼ Yakuts, YSE, Tuvans,
Altai, Kazakh, Kirghiz, Dolgans, Uyghurs, Uzbeks; Tungusic ¼ STE, Iengra, Nyukzha, Chinese Evenks, W Evenks, Oroqen, Man-
chu, C. Evens, W. Evens, E. Evens (subgroups ¼ Evens vs. Evenks incl. Oroqen; Manchu excluded); Mongolic ¼ Buryats, Mongols;
isolates ¼ (1) Koryaks, (2) Yukaghirs, (3) Eskimos, (4) N. Han, (5) Russians, (6) Kets.
Geography: NW ¼ Komi, Khanty, Selkup, ForestNenets, TundraNenets, Ket; N/NE ¼ Nganasan, W. Evenks, Yakuts, YSE, Yukaghirs,
STE, C. Even, W. Even, Dolgans; E ¼ Koryaks, E. Evens, Eskimos; SE ¼ Iengra, Nyukzha, Buryats, Mongols, Chinese Evenks, Oroqen,
Manchu, N Han; SW ¼ Tuvans, Altai; Central Asia ¼ Kazakh, Kirghiz, Uyghur, Uzbeks; W ¼ Russians.
Tungusic vs. Yakut-speaking: Tungusic ¼ W. Evenks, STE, Iengra, Nyukzha, Chinese Evenks, E. Evens, W. Evens, C. Evens;
Yakut-speaking ¼ Yakuts, Dolgans, YSE.
W. Evens with Yakuts: Tungusic ¼ W. Evenks, STE, Iengra, Nyukzha, Chinese Evenks, E. Evens, C. Evens, Dolgans; Yakut-speak-
ing ¼ Yakuts, YSE, W. Evens.
a
P < 0.01.
b
P > 0.05.
c
P < 0.05.

American Journal of Physical Anthropology—DOI 10.1002/ajpa


SIBERIAN mtDNA AND Y-DNA VARIATION 1023
TABLE 8. Y-chromosomal haplogroup and STR diversity
Haplogroup Haplotype
N diversity SE n diversity SE MPD SE References
Western Evens 22 0.18 0.11 8 0.74 0.08 2.60 1.45 This study
Central Evens 24 0.63 0.06 8 0.74 0.06 3.24 1.73 This study
Eastern Evens 31 0.60 0.09 NA NA NA NA Karafet et al. (2002)
STE 40 0.44 0.07 7 0.58 0.08 2.08 1.19 Pakendorf et al. (2006)
Iengra Evenks 9 0.78 0.11 6 0.92 0.07 5.06 2.71 This study
Nyukzha Evenks 78 0.65 0.04 NA NA NA NA Karafet et al. (2002)
YSE 33 0.46 0.10 13 0.90 0.03 4.16 2.12 Pakendorf et al. (2006)
Yakuts 183a 0.12 0.03 44 0.79 0.03 2.07 1.16 Pakendorf et al. (2006)
Yukaghirs 13 0.83 0.07 7 0.87 0.07 5.95 3.04 Pakendorf et al. (2006)
Koryaks 12 0.80 0.08 NA NA NA NA Karafet et al. (2006)
Tuvans 55 0.84 0.02 29 0.94 0.02 4.97 2.45 Pakendorf et al. (2006)

NA ¼ not applicable.
a
The sample size was 184 for the haplogroup diversity calculations and 183 for the STR diversity calculations.

TABLE 9. Shared number of Y-STR haplotypes (below diagonal) and pairwise Rst values (above diagonal) between
Tungusic-speaking groups and their neighbors
Western Evens* Central Evens STE Iengra Evenks YSE Yakuts Yukaghirs Tuvans
Western Evens 8 0.18 0.47 0.22 0.08 0.27 0.14 0.22
Central Evens 2 8 0.08 0.02 0.29 0.65 0.14 0.13
STE 1 1 7 0.09 0.55 0.78 0.32 0.23
Iengra Evenks 1 0 2 6 0.28 0.68 0.06 0.09
YSE 1 0 1 3 13 0.13 0.17 0.22
Yakuts 3 3 1 2 5 44 0.54 0.53
Yukaghirs 1 1 0 1 0 1 7 0.04
Tuvans 1 1 1 0 0 3 0 29

Italics ¼ not significantly different at 5% level without Bonferroni correction.


Bold on diagonal ¼ number of haplotypes within each group.
* The two Western Even haplotypes with the duplication at DYS393 belonging to haplogroup N-TatC were considered as being dif-
ferent from all other haplotypes.

the two haplotypes marked by arrows in Figure 7. The et al., 2000), this event would have taken place 4,630
remaining ten Western Evens have an identical haplo- (2,780–7,350) years ago.
type (Type 1 in Fig. 7) that is in the part of the network We performed Mantel tests to evaluate the correlation
that includes Tuvans and Yukaghirs. These haplotypes between mtDNA and Y-chromosomal variation as well as
are related to haplotypes based on 6 Y-STRs from differ- between mtDNA variation and geography and Y-chromo-
ent Finno-Ugric populations, Russians, and Buryats somal variation and geography. None of the analyses
(data not shown; taken from Zerjal et al., 1997; Lahermo showed a significant correlation (data not shown).
et al., 1999). This indicates a dual source for haplogroup
N-TatC in the Western Evens, of which about half origi- DISCUSSION
nated through admixture with Yakuts. The two Central
Evens belonging to haplogroup N-TatC are to be found By analyzing both M48 and M86, which are generally
in the Yakut half of the network, indicating an admixed assumed to be equivalent mutations defining the C3c
origin for these haplotypes as well. This also holds for haplogroup, we found that the mutations could be sepa-
the two Iengra Evenks with Tat C: their haplotypes are rated and that the M86 mutation occurred on the back-
the most common ones in Yakuts, making an admixed ground of derived M48 chromosomes. Since both M48
source very likely (types marked by an asterisk in Fig. 7). and M86 are generally not typed in the same study,
A MJ-network of Y-STRs on the background of hap- there is a lack of data on the distribution of the C-M48*
logroup C3 shows that the Evens (mainly Central Evens) subhaplogroup, making any inferences about the history
and Evenks have separate C-M86 haplotypes that differ of this subhaplogroup speculative. Judging from the
from each other by at least two mutational steps (Fig. 8). number of mutations that separate the C-M48* sub-
The two Central Evens with the 13/14 duplication at haplogroup from the C-M86 haplogroup, the separation
DYS393 are shown with 13 repeats (arrows in Fig. 8), time falls in the Neolithic, around 4,600 years ago. The
which is the most plausible ‘‘ancestral’’ state for the Evenks and Yakuts are widely assumed to have migrated
duplication. With 14 repeats, they would each be at a to Yakutia relatively late, in the first half of the second
distance of one mutational step and constitute a separate millennium AD (Tugolukov, 1980; Gogolev, 1993; Janhu-
haplotype (data not shown). Furthermore, the four indi- nen, 1996), but the Yukaghirs are believed to be the de-
viduals with the derived state at M48 and the ancestral scendants of the Neolithic inhabitants of Central and
state at M86 (C-M48* in Fig. 8) are separated from the Northeastern Siberia (Gurvich and Simchenko, 1980;
C-M86 haplotypes by at least five mutations, indicating Gurvich, 1994). It is therefore possible that the under-
a long time period since the M86 mutation arose on the ived C-M48* subhaplogroup was carried to Northeastern
background of M48. Assuming an average mutation rate Siberia by the ancestors of the Yukaghirs, where it was
of 3 3 103 (95% CI 1.89 3 103 to 4.94 3 103) (Kayser passed into the Iengra Evenks and Yakut-speaking

American Journal of Physical Anthropology—DOI 10.1002/ajpa


1024 B. PAKENDORF ET AL.

Fig. 8. MJ-network based on nine Y-chromosomal STRs in


individuals belonging to Y-chromosomal haplogroup C3. For the
Fig. 7. MJ-network based on nine Y-chromosomal STRs in significance of the labeled haplotypes, see text. Nodes are drawn
individuals belonging to Y-chromosomal haplogroup N-TatC. For proportional to number of individuals carrying a specific haplo-
the significance of the labelled haplotypes see text. Nodes are type (between 1 and 30), and branch lengths are proportional to
drawn proportional to number of individuals carrying a specific the number of mutational steps. a ¼ Stony Tunguska Evenks,
haplotype (between 1 and 89), and branch lengths are propor- b ¼ Iengra Evenks, d ¼ Western Evens, e ¼ Central Evens,
tional to the number of mutational steps. b ¼ Iengra Evenks, g ¼ Yukaghirs, i ¼ Yakuts, k ¼ Yakut-speaking Evenks, l ¼
d ¼ Western Evens, e ¼ Central Evens, g ¼ Yukaghirs, Tuvans, m ¼ Kalmyks.
i ¼ Yakuts, k ¼ Yakut-speaking Evenks, l ¼ Tuvans.

ulations. This is in good accordance with the ethno-


Evenks through admixture with local groups of Yuka- graphic data, which shows that the Evens were in close
ghirs. However, this scenario can only be substantiated cultural interaction with their neighboring groups, adop-
when more studies type both M48 and M86. ting means of transportation and details of their dwell-
As shown by the mtDNA analyses, the different Even ings from them (Spevakovsky, 1994).
subgroups are genetically very close. The Central Evens Furthermore, as is clear from the pairwise Fst analy-
furthermore show affinities to the Stony Tunguska and ses of HVR 1 sequences (Table 3), the Stony Tunguska
Nyukzha Evenks, with the pairwise Fst values being and Iengra Evenks appear not to have exchanged many
nonsignificant (Table 3). This contradicts the hypothesis women: these two subgroups share very few mtDNA
of a long-standing separation of Evenks and Evens, and haplotypes (Table 3) and differ significantly from each
supports the hypothesis of a recent spread of the North- other in their mtDNA variation. The Iengra Evenks are
ern Tungusic populations. Furthermore, this indicates closer to the Nyukzha Evenks, which can be explained
some sharing of maternal lineages between Northern by their geographic proximity. However, notwithstanding
Tungusic-speaking groups, irrespective of linguistic affin- the fact that only *200 km separate these two Evenk
ity and notwithstanding the huge geographic differences subgroups, there are still some differences in mtDNA
that separate them. However, although there does seem sequences between the two groups. This may be due in
to be a recent common mtDNA gene pool for the Tungu- part to Yakut admixture in the Iengra Evenks, as
sic-speaking groups, the individual Even subgroups ap- evinced by the high frequency of haplogroup D5a in the
pear to have undergone admixture with their geographic latter (Table 1), with one of the two D5a haplotypes in
neighbors as well, as evinced by the MDS plot based on Iengra Evenks being identical to the most frequent D5a
HVR1 sequences in the Tungusic-speaking populations haplotype in Yakuts (haplotype 1 in Fig. 4). However, it
and their neighbors (Fig. 2), the AMOVA (Table 4) and is likely that genetic drift has acted on all of the Tungu-
the SAMOVA analyses. The Western Evens are close to sic groups analyzed here, as shown by their relatively
the Yakuts, indicating admixture with the latter in the low diversity values (Tables 2 and 6) and by the outlying
maternal line, and the Central Evens are close to the positions of the Evenk subgroups in the MDS plot based
Yukaghirs and Tuvans. This clustering of the geographi- on the mtDNA Fst values (Fig. 2). The Stony Tunguska
cally very distant South Siberian Tuvans and the North- Evenks stand out amongst the Tungusic groups by their
east Siberian Yukaghirs, who speak completely unre- significantly lower Y-chromosome haplotype diversity
lated languages and have very different modes of sub- and their highly restricted haplogroup composition: they
sistence, is potentially intriguing, but may also simply have predominantly mtDNA haplogroups C (77%) and D
be a consequence of the relatively small sample size for (15%) (Table 1) and Y-chromosomal haplogroups C-M86
the Yukaghirs; larger sample sizes and further analyses (70%) and N-P43 (28%) (Table 5). The Western Evens, on
will be necessary to shed light on this matter. Although the other hand, are characterized by very low Y-chromo-
the Eastern Evens are intermediate between the Central somal haplogroup diversity. The effects of drift may
Even/Yukaghir cluster, the Western Even/Yakut cluster, have obscured original genetic affinities, making infer-
and the Koryaks in Figure 2, MJ-network analyses of ences about genetic relationships of these populations
haplogroup C (Fig. 3) and G1, Y, and Z sequences (not complicated.
shown) show that several haplotypes are shared between A correlation between genetic and linguistic affiliation
the Eastern Evens and the Koryaks, their geographic is evident in the MDS plot based on Y-chromosomal
neighbors, indicating admixture between these two pop- SNPs, with both Even and Evenk subgroups clustering

American Journal of Physical Anthropology—DOI 10.1002/ajpa


SIBERIAN mtDNA AND Y-DNA VARIATION 1025
together irrespective of their geographical location evidence of admixture with Europeans, with the excep-
(Fig. 6), as well as in the AMOVA analyses based on Y- tion of individual samples in the Eastern Even and
chromosomal SNP frequencies (Table 7). Clustering of Nyukzha Evenk mtDNA samples, which were taken
the Tungusic groups is also evident in an MDS plot that from the literature. However, since the sampling strat-
includes more Eurasian populations (figure not shown). egy of this study excluded individuals with known non-
However, this correlation disappears in the more fine- Even or non-Evenk ancestry, the effects of possible inter-
scaled STR analysis (Fig. 8). This may be a reflection of marriage during Soviet times would not be detected.
an older common origin of Evenks and Evens (excluding
the Western Even subgroup, who do not cluster with CONCLUSIONS
the other Northern Tungusic populations) followed by a
period of isolation. From the STR analysis, it becomes The Tungusic-speaking peoples show evidence of a
clear that even within haplogroup C-M86, which is wide- common origin followed by intermarriage in the mater-
spread in Tungusic-speaking groups [between 33 and nal line and genetic isolation in the paternal line, as is
78%, cf. Table 5 and Karafet et al. (2002)], the Stony expected of patrilocal groups (Oota et al., 2001). How-
Tunguska and Iengra Evenks do not share any haplo- ever, the mtDNA analyses in the Evens provide some
types with the Western or Central Evens. This indicates evidence of admixture with geographic neighbors, indi-
that the different languages spoken by Evens and cating that at times local proximity was chosen over
Evenks precluded recent gene flow in the paternal line linguistic and cultural similarity when searching for
between the ethnic groups, although paternal gene flow mates. Such admixture with geographic neighbors is not
between subgroups of the Evenks appears not to have apparent in the Y-chromosomal analyses, with the excep-
been affected. However, this latter conclusion can only tion of the Western Evens; these have clearly undergone
be tentative due to the very small sample size of the Ien- substantial admixture with neighboring Yakuts. How-
gra Evenks. Unfortunately, Y-chromosomal STR data are ever, the number of populations available here for Y-
not available for the populations analyzed by Karafet chromosomal comparisons with the Tungusic-speaking
et al. (2002), so it is impossible to evaluate whether populations is small. Moreover, detailed Y-STR analyses,
other subgroups of Tungusic-speaking populations do which are necessary for fine-grained analyses of Y-chro-
share Y-STR haplotypes with the groups analyzed here. mosomal variation, have not been carried out in many
These results indicate a large degree of substructuring populations of interest. It is therefore impossible to
of the male gene pool in Tungusic-speaking groups, with exclude admixture in the Tungusic-speaking groups with
genetic isolation of individual groups. This is most strik- neighboring populations such as Samoyedic-speaking
ing in a comparison of the Central and Western Evens, groups in the west or Koryaks in the east. In addition,
who have completely contrasting Y-chromosomal hap- the local Tungusic groups have always been very small
logroup compositions (Table 5). Although the Western (Dolgikh, 1960), facilitating the effect of genetic drift.
Evens have clearly undergone admixture with neighbor- This may have obscured the genetic affinities of the
ing Yakuts (as shown by the widespread haplotype shar- populations analyzed; analyses of autosomal markers
ing of haplogroup N-TatC STR haplotypes), this accounts would therefore be desirable to further evaluate the rela-
for only *45% of their Y-chromosomal gene pool; tionships indicated by the mtDNA and Y chromosome
another 45% of the N-TatC haplotypes in Western Evens analyses.
have a separate, unknown origin (Fig. 7). Nevertheless,
hardly any haplotypes are shared between the Western ACKNOWLEDGMENTS
and Central Evens. The Western Evens thus seem to
have been isolated from the other Even subgroups in the This study focuses on the prehistory of populations as
paternal line, as is confirmed by the fact that their reflected by mtDNA and Y-chromosomal variation. It does
dialect is not mutually comprehensible with the other not aim at ascribing ethnicity to individual groups, nor
Even dialects (Novikova, 1960). The more intense inter- does it intend to evaluate the self-identification of such
marriage with Yakuts may be due to the longer period of groups. The authors thank all sample donors for their par-
time that these groups were settled in close proximity: ticipation in this study. The support of the administrative
Yakuts were settled on the Yana river at the time of first heads of the districts and villages visited during sample
Russian contact (Dolgikh, 1960). The fact that the collection is gratefully acknowledged. Sample collection
Tungusic-speaking men were locally isolated to a greater and research was supported by the Max Planck Society,
degree than the women may be a reflection of the pre- Wenner-Gren Foundation for Anthropological Research
vious patrilocal social structure, where the bride joined and the Russian Foundation for Basic Research. The
authors thank members of the Molecular Anthropology
the groom’s clan (Fondahl, 1994). This would have led
group at the MPI for Evolutionary Anthropology for help-
to a mixing of mtDNA lineages between individual sub-
ful discussions, Patricia Heyn for mtDNA haplogroup typ-
groups of Tungusic-speaking populations, while the Y-
ing, Matti Heino for help with Y-STR typing, and Knut
chromosomal lineages would have remained relatively Finstermeier for help with the figures.
isolated. With the exception of the Western Evens, the
admixture with neighboring groups is detectable in the
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