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Brief Communication: Y-chromosome HaplogroupAnalysis Indicates That Chinese Tuvans ShareDistinctive Affinity With Siberian Tuvans
Zheng Chen,1 Yongke Zhang,1 An Fan,2,3 Yanan Zhang,4 Yanping Wu,5 Qianjun Zhao,5 Yong Zhou,6
Canlin Zhou,6 M. Bawudong,6 Xinmin Mao,6 Yuehui Ma,5 Lingyun Yang,1 Yuanling Ding,2
Xueqin Wang,7* and Shaoqi Rao2,3,7*
1Department of Medical Genetics, Zhongshan Medical College, Sun Yat-Sen University, Guangzhou 510080, China2Department of Medical Statistics and Epidemiology, School of Public Health, Guangdong Medical College,Dongguan 523808, China3Department of Medical Statistics and Epidemiology, School of Public Health, Sun Yat-Sen University,Guangzhou 510080, China4Department of Infertility Sterility and Sexology, the Third Affiliated Hospital of Sun Yat-Sen University,Guangzhou 510080, China5Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100094, China6Department of Biology, Xinjiang Medical University, Urumqi 830054, China7Department of Statistical Sciences, School of Mathematics and Computational Science, Sun Yat-Sen University,Guangzhou 510275, China
KEY WORDS Tuvans’ origin; Y chromosome SNPs; genetic analysis
ABSTRACT Tuvans are mainly distributed in Siberia(the Republic of Tuva), Mongolia, and China. The geneticorigin of Chinese Tuvans remains controversial. TheTuvans in China were classified as Mongolians in theearly 1950s by the National Ethnic Affairs Commissionof China, but they defined themselves as a separategroup. To resolve this dispute and determine theirgenetic relationships with the peoples in Central Asia,we randomly selected 150 male subjects from the Tuvansin the Altai region of Xinjiang Uygur AutonomousRegion in China. Fourteen Y chromosomal markers weregenotyped using the RFLP method or direct sequencing.These haplogroup data were combined with public datafor 15 populations in South Siberia and Central Asia.Tuvans in both China and the Republic of Tuva had the
highest frequencies of haplogroups K-M9 and Q-M242.Principal component analysis demonstrated that theTuvans in China were of a distinct cluster, separatedfrom their neighbors, the Mongolians and Kazakhs,which finding was consistent with the Analysis of Molec-ular Variances. Further population tree analysisrevealed that Tuvans were on a far-separated clusterfrom their neighbors. Based on these results, we proposethat the Tuvans (in both China and the Republic ofTuva) constitute a group distinct from Mongolians andfrom other Central Asia populations. However, thegenetic results might be the consequence of some evolu-tionary forces like genetic drift and founder effect, anddo not necessarily reflect their ultimate origin. Am JPhys Anthropol 144:492–497, 2011. VVC 2011 Wiley-Liss, Inc.
Tuvans were traditionally nomadic people who spreadinto Central Asia (Siberia, Mongolia and China). Themajority of Tuvans (with a population size of slightlylarger than 0.23 million according to the 2002 census,see http://en.wikipedia.org/wiki/Tuva for details) are nowliving in the Republic of Tuva (or Tyva Republic), a
federal subject of Russia which was incorporated intoRussia by Tsar Nicholas in the early twentieth century,and later became part of the former Soviet Union. Asmall population now lives in the Altai region of North-west China or in Mongolia (Ding, 2003). The geneticorigin of the Tuvans in China remains controversial.
The first two authors contributed equally to this work.Present address of Yongke Zhang: Department of Clinical Medicine
and Guangdong Key Laboratory of Male Reproductive Medicine andGenetics, Shenzhen Hospital of Peking University, Shenzhen 518036,China.
Grant sponsor: National Natural Science Foundation of China; Grantnumbers: 30640028, 30830104, 30971601, 31071166; Grant sponsor:Natural Science Foundation of Guangdong Province, China; Grant num-bers: 8251008901000007, 9151008901000089; Grant sponsor: Scienceand Technology Planning Project of Guangdong Province; Grant num-ber: 2009A030301004; Grant sponsor: Scientific Research Foundationfor the Returned Overseas Chinese Scholars, State Education Ministryof China; Grant number: to Shaoqi Rao; Grant sponsor: the GuangdongMedical College Start-up Fund; Grant number: XG1001.
*Correspondence to: Dr. Shaoqi Rao, PhD, Department of MedicalStatistics and Epidemiology, School of Public Health, GuangdongMedical College, Dongguan 523808, China. E-mail: [email protected] and Xueqin Wang, Department of Statistical Sciences,School of Mathematics and Computational Science, Sun Yat-SenUniversity, Guangzhou 510275, China.E-mail: [email protected]
Received 31 May 2010; accepted 19 October 2010
DOI 10.1002/ajpa.21453Published online 4 January 2011 in Wiley Online Library
(wileyonlinelibrary.com).
VVC 2011 WILEY-LISS, INC.
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 144:492–497 (2011)
These people were classified as Mongolians in the early1950s by the National Ethnic Affairs Commission ofChina; nonetheless, they recognized/claimed themselvesto be of an independent origin.Tuvans have been termed the Dewa, Tyiva and the
Tocumen Qiake in history (Ling, 2006). They were alsoknown as Dubos, Sayan-uryankhais and Tangnu-uryan-khais (Ding, 2003). In Russian, Tuvan was translated asSoyot or Tangnutuvan (Wells et al., 2001; Ding, 2003).Tuvans were first mentioned in an ancient Chinese booktitled ‘Sui Shu Tie Le’, written in about the 7th centuryAD, saying: ‘‘Dubos and the other groups who live in thesouth of Lake Baikal are generally called Tiele, althoughthey belong to different tribes’’ (Wei, 1973). The Valley ofKanas River in the Altai region in Xinjiang UygurAutonomous Region is the only dwelling place for theTuvans in China. Today, there are about 2000 Tuvans inthis region, separated into three villages: Baihaba,Hemu and Kanasi (see Fig. 1 for their geographic loca-tions). Some anthropological scientists believed thatthese Tuvans were the descendants of some soldiers ofGenghis Khan’s army, who remained in the local placesduring their long expedition to the West during theYuan Dynasty (Ling, 2006). However, the senior peoplein the villages claimed that their ancestors migratedfrom Siberia about 500 years ago, initially affiliated withthe same country as the Tuvans in the Tuva Republic(Ling, 2006). In addition, some of the senior peopleargued that their ancestors had already been settled inthe region for more than 1000 years (Cheng, 1994; Wellset al., 2001). Overall, there are different perspectives/speculations over the origin of the Tuvans in China, andtheir genetic relationships with the neighboring peoplesare to be determined (Cheng, 1994; Ling, 2006).
The Tuvans in the Altai region have kept a distinctlanguage and their own specific religious beliefs, and arestill aggregating in tribes or clans (Cheng, 1992; Cheng,1994; He, 2001; Ling, 2006). The corresponding lan-guage, Tuvan, belongs to the Turkic branch of the Altailanguage family (Cheng, 1992), and is closest to Kazakhin linguistics. Tuvans take Tibetan Buddhism as theirbelief system, while Shamanism also plays an importantrole in their daily lives (Cheng, 1994; Ding, 2003).However, up to the present, few genetic studies havebeen done to resolve their disputed origin. In this study,we randomly selected 150 Tuvan male subjects from theAltai region in Xinjiang Uygur Autonomous Region ofChina to explore their genetic relationships with the peo-ples of Central Asia. Fourteen Y chromosomal markers(11 single nucleotide polymorphism (SNP) loci, one Aluinsertion, one 5-bp insertion, and one 1-bp deletion) weregenotyped by using the RFLP method or direct sequenc-ing. Then, these multi-loci marker data were analyzedjointly with public data for 15 populations in SouthSiberia and Central Asia. The purpose of this study wasto test whether the Tuvans living in an isolated mannerin the Altai region of northwest China were geneticallydistinct from their neighbors, specifically the Mongoliansand Kazakhs, and whether they were a small number ofmigrants who originated from the Republic of Tuva.
MATERIALS AND METHODS
One hundred and fifty male subjects for Tuvans wererandomly collected from three villages [Baihaba (51),Hemu (51) and Kanasi (48)] in the suburb of Aletai cityof Xinjiang Uygur Autonomous Region, China. An effortwas made to collect blood samples from healthy andunrelated individuals based on the information providedby the participants or their parents/guardians. The ageof the participants varied, including children and elderlyseniors. This study was approved by the local institu-tional review boards on human subject research. Writteninformed consents were obtained from all participants.DNA was extracted from the whole blood by the stand-ard phenol-chloroform method.Each sample was typed for a total of 13 Y-chromosome
markers, including 10 single nucleotide polymorphismsloci (M130, C to T; M48, A to G; M89, T to C; M9, G toC; M45, A to G; M46, T to C; M119, T to G; M122, C toT; M173, A to C; M242, C to T), an Alu insertion (YAP,M1), a 5-bps deletion (M175, Del TTCTC) and a single‘G’ deletion (M17, Del G). For marker YAP, the insertionwas identified by analysis of the PCR products of YAPusing 3–4% agar gel electrophoresis (AGE). For markerM17, detection of the single deletion was initially per-formed by using DHPLC (Denaturing High PerformanceLiquid Chromatography) and then the result was con-firmed by direct sequencing. The remaining 11 SNPsand one 5-bps deletion marker (M175) were genotypedby PCR-RFLP as previously described (Su et al., 1999).The primers for the SNP markers and the other threemarkers were designed according to the previous study(Underhill et al., 2000).Y-chromosome binary haplogroups for Tuvan samples
were defined by the analysis of all 14 binary polymor-phisms. The nomenclature of haplogroups followed thatof the Y Chromosome Consortium (YCC 2002). The hap-logroup data for 15 other populations in South Siberiaand Central Asia were retrieved from previous articlesand public databases (GenBank, UCSC web, etc.). The
Fig. 1. Geographic locations of the Chinese Tuvan villagesand the surrounding areas in Central Asia or South Siberia.A: Locations of the other populations around Chinese Tuvans.B: The enlarged box for Figure 1A, to denote the approximatelocations of three Chinese Tuvan villages in Xinjiang UygurAutonomous Region, China.
493GENETIC ANALYSIS OF TUVANS
American Journal of Physical Anthropology
combined haplogroup data from this study and the previ-ous studies (Su et al., 1999; Lell et al., 2002; Bo et al.,2004; Katoh et al., 2005; Nasidze et al., 2005; Derenko etal., 2006) were analyzed. Haplogroup diversity (HD) andits standard error (SE) were estimated. Then, principalcomponent analysis (PCA) was conducted using Y-chro-mosome haplogroup frequencies and SPSS 14.0 softwarepackage (http://www.spss.com/). AMOVA-derived molecu-lar variances and population pairwise FST values werecomputed using ARLEQUIN version 3.0 (http://anthropo-logie.unige/arlequin). The neighbor-joining (NJ) treeswere constructed using the program Mega 4.0 (Kumar etal., 2004), with a Kimura 2-parameter model and a boot-strap (number of replications 5 1,000) test.
RESULTS
The Y chromosome haplogroup frequency distributionsfor the Tuvans and other neighboring populations arepresented in Table 1. However, based on their ability fordistinguishing other haplogroups, some haplogroups(e.g., F-M89, K-M9, P-M45, DE) were paragroups (aterm that describes lineages within a haplogroup thatare not defined by any additional unique markers.). Forconvenience, the two terms were used interchangeably.The haplotype diversity (HD) for the three Tuvanvillages and the pooled sample (referred to as ChineseTuvans hereafter) were estimated from 13 haplogroups.The HD estimates indicated that a substantial amountof genetic diversity remained for all three subpopula-tions. The marked higher HD of the pooled sample forthe pooled Tuvans in China than those for the subpopu-lations living in three villages (Hemu, Kanasi andBaihaba) implied that genetic differentiation occurreddue to some evolutionary forces (e.g., founder effects,genetic drift) or other more recent factors.Among the 13 individual haplogroups, the Chinese
Tuvans had the highest frequencies of K-M9 or Q-M242haplogroups (the haplogroup frequencies were 42.0% and25.0%, respectively). The K-M9 haplogroup, which wasknown to have originated from Southwest Asia (Nasidzeet al., 2005), was frequent in the South Siberia popula-tions (Tuvans, 47.0%, Mongolians, 25.0%) and oneCentral Asia population (Uigur, 19.0%) (Table 1). TheChinese Tuvans also had the highest frequency of Q-M242 lineage (25.0%), but this lineage was highly variedamong the three villages (for example, up to 63.0% invillage Baihaba). Interestingly, native Americans alsoshowed a high frequency of the Q-M242 haplogroup(63.9%) (Lell et al., 2002). The C-M130*(xM48) and C-M48 haplogroups were the benchmark haplogroups inthe Mongolians (with frequency of 13.0% and 46.0%,respectively) and the Kazakhs (with frequency of 9.0%and 57.0%, respectively) (Nasidze et al., 2005), but theywere infrequent in Chinese Tuvans (4.0% and 6.0%,respectively), suggesting that the Tuvans were a geneti-cally separated group. Interestingly, the frequencies ofthe P-M45 and R-M17 haplogroups in Chinese Tuvanswere significantly less frequent (with a frequency of only5.0% and 1.0%) compared with the Tuvans in the TuvaRepublic (17.0% and 14.0%) (Nasidze et al., 2005). Thismay be due to the sampling effect or it may imply thatthe two populations began to diverge genetically becauseof territorial separations. Whether this trend can beattributed to the historical large-scale migration as pro-posed in the previous studies (Lell et al., 2002; Zegura etal., 2004) is yet to be studied. Except for P-M45 and R-
M17, the Y chromosome haplogroup frequencies in theTuvans in China were largely similar to those found inthe Tuvans of the Republic of Tuva while they weremarkedly different from their other neighbors, includingthe Mongolians and Kazakhs.The results from the principal component (PC) analy-
sis of Y chromosome haplogroup data are presented inFigure 2. The first three PCs explained 53.31% of thetotal variance. Through the three dimensions, the 16populations under study were grouped into three clus-ters: cluster A, made up of the Chinese Tuvans, theTuvans in the Republic of Tuva, Uigur, Uzbek (Samar-kand); cluster B, made up of Kazakh, Tajik (Koiant),Russian (Tashkent), Northern Han, Manchu, Tibetan,Mongolian (Khoton), Mongolian (Uriankhai), YeniseyEvenk; and cluster C, made up of Buryats and Tofalars.The first and second principal components separatedclusters A and B. The first principal component wassignificantly correlated with the frequencies of markersO-M122 (r 5 0.917, P \ 0.001), O-M119 (r 5 0.852,P \ 0.001) and O-M175* (x M122, M119) (r 5 0.784,P \ 0.001) while the second component was significantlycorrelated with the frequencies of K-M9 and P-M45(r 5 0.919, P \ 0.001; r 5 0.718, P 5 0.002), suggestingthat the differences in the frequencies of the threemarkers were the major reason for the clusteringpattern. The third component contributed mainly to theseparation between cluster C (i.e., Buryats and Tofalars)and clusters A and B. This component score was signifi-cantly correlated with N-M46 and C-M130* (r 5 0.669,P 5 0.005; r 5 0.662, P 5 0.005). Again, the principalcomponent plot demonstrated the close relationshipbetween the Tuvans in China and the Tuvans in theRepublic of Tuva.AMOVA was then employed to evaluate the genetic
differentiation between Tuvans and other populations inCentral Asia and South Siberia to resolve the geneticgrouping of Tuvans (Table 2). First, to test the hypothe-sis that Tuvans and Mongolians are in an identicalgroup, both Tuvans (either in China or in the Republicof Tuva) and Mongolians were grouped together as onegroup and the other populations were combined intoanother group. The source of ‘‘among groups’’ explained1.54% of the Y marker molecular variation. Neverthe-less, when the Mongolians were excluded from the groupfor the Tuvans, the ‘‘among groups’’ contributionincreased to 7.46% and the ‘‘among populations withingroups’’ variance was significantly reduced, from 30.47%to 27.29%. This result, in agreement with the aforemen-tioned principal component analysis, suggested that thegenetic groups for Tuvans and Mongolians were unlikelyto be the same.To further explore the genetic relationships between
the Tuvans at large (i.e., combining all the Tuvan popu-lations together) and the major populations in CentralAsia and South Siberia, and to identify the geneticgroups, we analyzed 13 ethnical populations using thesoftware Mega 4.0. The population tree was shown inFigure 3. Based on the analysis of 13 distinct branches,four major genetic groups were identified. The uppercluster III consisted of four populations, the NorthernHan, Manchu, Tibetans, and Tuvans. On this figure,Manchu and Northern Han were grouped together witha good support (710/1,000), as we expected. Tibetans fur-ther joined the clade, and this genetic inference hadbootstrap support of 668/1,000 (indicating 668/1,000trees grouped the Tibetans with the Manchu/Han). Mon-
494 Z. CHEN ET AL.
American Journal of Physical Anthropology
TABLE
1.Distribution
ofY
chromosom
ehaplogroupfrequen
cies
inChineseTuvansandother
Sou
thSiberia
orCen
tralAsiapop
ulation
s
Pop
ulation
sSample
sizes
Haplogroups
C-M
130*
(xM48)
C-M
48
F-M
89
K-M
9O-M
175*
(xM122,M11
9)
P-M
45
N-M
46
O-M
122
R-M
173*
(xM17)
R-M
17
Q-M
242
DE-YAP
O-M
119
HD
Tuvan(H
emu)
51
0.04
0.08
0.06
0.52
0.08
0.04
0.02
0.04
0.02
0.02
0.10
0.723
Tuvan(K
anasi)
51
0.08
0.06
0.06
0.59
0.06
0.04
0.02
0.04
0.06
0.643
Tuvan(B
aihaba)
48
0.04
0.04
0.15
0.06
0.04
0.02
0.02
0.63
0.590
ChineseTuvans
150
0.04
0.06
0.05
0.42
0.05
0.05
0.03
0.05
0.01
0.01
0.25
0.750
Tuvan(theRep
ublic
ofTuva)a
42
0.10
0.07
0.47
0.17
0.02
0.02
0.14
0.727
NorthernHanb
42
0.10
0.07
0.19
0.07
0.52
0.05
0.684
Manch
ub
101
0.09
0.08
0.02
0.01
0.01
0.43
0.03
0.561
Tibetansc
50
0.04
0.12
0.40
0.28
0.655
Mon
goliana
24
0.13
0.46
0.08
0.25
0.04
0.04
0.732
Kaza
kha
54
0.09
0.57
0.02
0.11
0.06
0.02
0.06
0.04
0.02
0.639
Uigura
41
0.15
00.12
0.19
0.07
0.02
0.22
00.815
Uzb
ek(Samark
and)a
45
0.16
0.02
0.13
0.15
0.07
0.11
0.13
0.02
0.865
Tajik(K
oiant)a
22
0.05
0.05
0.03
0.05
0.64
0.405
Russian(Tash
ken
t)a
89
0.03
0.06
0.13
0.07
0.47
0.03
0.614
Mon
golian(K
hoton
)b40
0.10
0.03
0.83
0.240
Mon
golian
(Uriankhai)b
60
0.25
0.33
0.05
0.08
0.08
0.07
0.07
0.02
0.793
Buryats
d238
0.64
0.02
0.09
0.19
0.01
0.02
0.518
Tofalars
d32
0.06
0.03
0.25
0.13
0.13
0.760
Yen
isey
Even
ke
31
0.58
0.10
0.10
0.03
0.470
ChineseTuvansare
thepooledmem
bersof
thethreeChineseTuvanvillages.
aWells,et
al.,2001.
bKatoh,et
al.,2005.
cBo,
etal.,2004.
dDeren
ko,
etal.,2006.
eLell,et
al.,2002.
Notethatforsomepop
ulation
s(e.g.,Even
k)thesu
mof
allthelisted
freq
uen
cies
wasnot
equalto
1asthedata
forsomehaplogroupswerenot
available.
495GENETIC ANALYSIS OF TUVANS
American Journal of Physical Anthropology
golians and Kazakhs were not in this group. Instead,they combined with the Tofalars and Yenisey Evenk intoa distinct branch (Cluster II). The Rashkents in Russianand Tajiks in Koiant were on the same branch of thepopulation tree, forming Cluster I. Finally, the Buryats,Uigurs and Uzbeks in Samarkand formed into ClusterIV. In short, population tree analysis of 13 populationsin Central Asia and South Siberia identified four majordistinct braches. Tuvans were located on a differentbranch from their Mongolian and Kazakh neighbors,indicating that they may have different evolutionary his-tories or origins.
DISCUSSION
This study showed that the Chinese Tuvans have ahigh frequency of the K-M9 haplogroup, as do the peoplein the Republic of Tuva. In addition, the popular P-M45lineage in South Siberia and the R-M173*(xM17) lineagein Central Asia (Khar’kov et al., 2007) have a low fre-quency in the Tuvans at large. These results providegenetic evidence to support that the ancestors of the Chi-nese Tuvans in Central Asia migrated from the LakeBaikal region of South Siberia. Such large-scale migra-tions were not uncommon in Central Asia and SouthSiberia throughout history. Wars, famines, murrains andthe nomadic life of ancient tribes in these regions all arepossible explanations (Su et al., 1999, 2000; Cinnioglu etal., 2004). In addition, gene exchange through interracialmarriage between the Tuvans and their nearest Mongo-lian and Kazakh neighbors was thought to be inevitable,which was supposed to be another important factor influ-encing the genetic structure of the Tuvans (Thanseem etal., 2006; Zhou et al., 2007). Nevertheless, the Tuvanscan still maintain their genetic distinction under a longexposure of evolutionary forces. However, based on the Y
chromosomal data only, we are unable to infer exactlywhen the Tuvans migrated into their current region, aspreviously explained (Cinnioglu et al., 2004).Finally, we should recognize that this study (or similar
studies for that matter) may suffer from some limita-tions in drawing genetic inferences. First, this study con-sidered only paternal lineages, while other loci eitherfrom maternal sources (e.g., mitochondrial lineage) orautosomes could produce different results. Second, thegenetic results themselves could be interpreted in differ-ent ways. Third, the applied methods for population treeanalysis, originally developed for interspecies compari-sons, are often insensitive for human populations,thus leading to low bootstrap supports. In order tomake robust interpretations, we have used multipleapproaches in our analysis. Nevertheless, although mul-tiple lines of evidence support that the Tuvans (either inChina or in the Tuva Republic) were genetically distinctfrom other populations, this might be the consequence ofgenetic drift, and not necessarily reflect their ultimateorigin. Furthermore, if the assumption that the ChineseTuvans migrated from the Tuva Republic is true, the dif-ferences in the frequencies of some haplotypes betweentwo populations could be due to founder effects. Futurestudies using more appropriate ancestry informativemarkers in Chinese Tuvans and relevant potentialsource populations should provide a more specificanswer.
ACKNOWLEDGMENTS
The authors would like to express our appreciation toall of the blood donors who made this work possible.Special thanks go to the Centre for Disease Preventionand Control of Aletai city, the Administration Bureau ofKanasi Scenic Spot, the Government of Hemu Town andthree villages for their great help in collecting samples.They also thank Professor Weiying Jiang for helpingthem to use the DHPLC technology for genotyping.
Fig. 2. Principal component (PC) analysis of Y chromosomehaplogroup frequencies of Tuvans and other populations in Cen-tral Asia and South Siberia.
TABLE 2. Assessment of the genetic differentiation betweenTuvans and other populations, using AMOVA
Source of variation
Percentage of variation (%)
Two groups(include Mongolian)
Two groups(exclude Mongolian)
Among groups 1.54 7.46Among populations
within groups30.47 27.29
Within populations 67.98 65.25
Fig. 3. Population tree for 13 populations (Tuvans pooledand other populations) in Central Asia and South Siberia,constructed using NJ method and Fst. Internal numbers arebootstrap values (1,000 replicates). Roman numerals denotepopulation clusters as described in the text.
496 Z. CHEN ET AL.
American Journal of Physical Anthropology
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497GENETIC ANALYSIS OF TUVANS
American Journal of Physical Anthropology
