prehistorical east–west admixture of maternal lineages in a 2,500-year-old population in xinjiang

Prehistorical East–West Admixture of Maternal Lineagesin a 2,500-Year-Old Population in Xinjiang

Fan Zhang,1 Zhi Xu,1 Jingze Tan,1 Yuefeng Sun,2 Bosong Xu,2 Shilin Li,1

Xin Zhao,3 Hui Zhou,3 Guoqiang Gong,4 Jun Zhang,4 and Li Jin1,5*

1State Key Laboratory of Genetic Engineering and MOE Key Laboratory of Contemporary Anthropology,School of Life Sciences and Institutes of Biomedical Sciences, Fudan University, 200433 Shanghai, China2Department of Biology, Tianjin Normal University, 300387 Tianjin, China3Laboratory of Ancient DNA, Research Center for Chinese Frontier Archaeology, Jilin University, 130023 Changchun,China4Institute of Archaeology, Chinese Academy of Social Sciences, 100029 Beijing, China5Chinese Academy of Sciences and Max Planck Society (CAS-MPG), Partner Institute for Computational Biology,Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, 200031 Shanghai, China

KEY WORDS genetic admixture; mitochondrial DNA; ancient DNA

ABSTRACT As an area of contact between Asia andEurope, Central Asia witnessed a scenario of complexcultural developments, extensive migratory movements,and biological admixture between West and East Eura-sians. However, the detanglement of this complexity ofdiversity requires an understanding of prehistoric con-tacts of the people from the West and the East on theEurasia continent. We demonstrated the presence of

genetic admixture of West and East in a population of 35inhabitants excavated in Gavaerk in southern Xinjiangand dated 2,800–2,100 years before present by analyzingtheir mitochondrial DNA variations. This result indi-cates that the initial contact of the East and the WestEurasians occurred further east than Central Asia asearly as 2,500 years ago. Am J Phys Anthropol 142:314–320, 2010. VVC 2009 Wiley-Liss, Inc.

In the past decade, several genetic studies on DNAmarkers such as mitochondrial DNA (mtDNA) andY-chromosome variation have all demonstrated that con-temporary Uzbeks (Yang et al., 2008), Kazaks (Comaset al., 1998; Yao et al., 2004), and Uigurs (Comas et al.,1998; Yao et al., 2004; Xu and Jin, 2008; Yang et al.,2008) in Xinjiang, as well as present-day populations inCentral Asia (Comas et al., 1998; Perez-Lezaun et al.,1999; Karafet et al., 2001; Wells et al., 2001; Zerjalet al., 2002; Comas et al., 2004; Quintana-Murci et al.,2004; Chaix et al., 2008), are genetically admixed, carry-ing both West Eurasian (WE) and East Eurasian (EE)lineages. However, the understanding of when andwhere the West and the East initially contacted havebecome fascinating issues and would benefit from prehis-toric evidence. mtDNA sequences from ancient Kazakh-stan (Lalueza-Fox et al., 2004) indicated that EElineages did not appear in Central Asia until 2,700–3,300 years before present (YBP).In Xinjiang, hundreds of mummified humans dated

between 4,000 and 1,700 YBP were excavated recently.These mummies are notable for their European or Cau-casoid features (e.g., blond or reddish hair, and straightnoses), suggesting that an ancient WE substratum waspresent far into the east of Eurasia (Mair, 1995). Analy-ses of textiles, linguistic, and biological features (Han,1998; Mallory and Mair, 2000) of the mummies led to aconclusion that their origins and affiliations should beassigned to European-like people. Meanwhile, the skele-tons at Gavaerk (GAV), near Charchan (or Qiemo) in thesouth of Xinjiang (see Fig. 1), dated 2,800–2,100 YBP,were excavated in 1995 by the Xinjiang team of Archaeo-logical Institute of Chinese Academy of Social Sciences(Zhang, 2002). These skeletons were considered as

‘‘proto-Europoid type with Nordic characteristics’’ (Han,1998) based on the analyses of their cranial morphology(Zhang, 2002). However, they showed weakened nasalbridge salient and less orbit width (Zhang, 2002), sug-gesting possible contribution of East Eurasians (or EastAsians). Therefore, a genetic study of these inhabitantsmight reveal a complete picture of prehistorical con-tact(s) between the West and the East.

Fan Zhang and Zhi Xu contributed equally to this work.

Grant sponsor: National Outstanding Youth Science Foundationof China; Grant number: 30625016; Grant sponsor: National ScienceFoundation of China; Grant number: 30890034; Grant sponsor:National Natural Science Foundation of China and 863 Program;Grant numbers: 30571013, 2007AA02Z312; Grant sponsors: Shang-hai Leading Academic Discipline Project (B111) and The Center forEvolutionary Biology.

Additional Supporting Information may be found in the onlineversion of this article.

*Correspondence to: Li Jin, State Key Laboratory of Genetic Engi-neering and MOE Key Laboratory of Contemporary Anthropology,School of Life Sciences and Institutes of Biomedical Sciences, FudanUniversity, 220 Handan Road, 200433 Shanghai, China.E-mail: [email protected]

Received 29 May 2009; accepted 23 October 2009

DOI 10.1002/ajpa.21237Published online 23 December 2009 in Wiley InterScience

(www.interscience.wiley.com).

VVC 2009 WILEY-LISS, INC.

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 142:314–320 (2010)

To shed the light on this issue, teeth were collected forancient DNA study following strict criteria and specialprecautions. mtDNA shows great advantage over nuclearDNA when dealing with fragmented, chemically modi-fied, and trace amount of DNA from both historical andprehistorical specimens (Hoss et al., 1996; Hofreiter etal., 2001), owing largely to its high copy number, rapidmutation rate, and maternal inheritance. Therefore,mtDNA variations of these samples were systematicallyanalyzed, and their places of origins were inferred bycomparing them with published data of contemporaryand ancient Eurasians.

MATERIALS AND METHODS

The skeletons in GAV site were in an excellent state ofpreservation (Supporting Information File 1). Overall, 52human teeth specimens of Gavaerk site, each from dif-ferent individual, were pulled out from alveoli and takenfor analysis.DNA extractions and amplifications were done as

described in our previous study (Xu et al., 2008). Inbrief, the teeth were soaked in bleach (�5% sodium hy-pochlorite solution) for 15 min, rinsed in ethanol (70%),and followed by 30-min UV irradiation for each face.Then each tooth was ground into fine powder in SPEXSamplePrep Freezer/Mills 6750. Subsequently, about500-mg powder was used for a silica-base DNA extrac-tion with a minor modification, that is, adding 8-lg polydA (80 mer) to circumvent carrier effect of ancient DNAwhen extracting (Xu et al., 2009). At least two independ-ent samplings and extractions were obtained from eachremain. The independent replication was conducted asdescribed (Xu et al., 2008) in Jilin University, Jilin,China.

mtDNA haplogroup assignment

By searching for hg-specific hypervariable region(HVR) I motif and matching with available modern datasets, the ancient mtDNAs obtained were tentativelyassigned to hgs. According to European (Finnila et al.,2001) and East Asian (Kivisild et al., 2002; Kong et al.,2003) phylogenetic network, hg-diagnostic coding regionpolymorphisms were typed using SNaPshot and/orrestriction fragment length polymorphism (RFLP) tomake sure the hg assignment (Yao et al., 2003). ForSNaPshot, extracted DNAs were amplified by multiplexPCR including 14 pairs of primers (Supporting Informa-tion File 2) and followed by single-base extension using

ABI PRISM SNaPshotTM Multiplex Kit (Applied Biosys-tems). Results were analyzed with GeneScan1 AnalysisSoftware version 3.7 (Applied Biosystems) on ABI 3130xlGenetic Analyzer (Applied Biosystems). For RFLP,extracted DNAs were amplified with different primers(Supporting Information File 2), and then PCR productswere digested with corresponding restriction enzymesand detected by electrophoresis on 3.5% agarose gel.

Data analysis

Overall, 9,962 contemporary mtDNA profiles, as wellas 166 ancient mtDNA profiles from seven ancienthuman DNA studies, were used for comparison. Foranalysis of shared haplotypes, the stretch-C region fromnucleotide position 16,182–16,193 and the position16,093 with a fast mutation rate (Bandelt et al., 2006)were excluded in comparison.

RESULTS

Authenticity

Among the 52 studied specimens, 35 (Table 1) yieldedreplicable profiles within laboratory, of which none hadidentical HVR I motif with staffs’ profiles (data notshown). The HVR I motifs of these 35 specimens wereverified by sequencing cloned PCR products and in total,770 cloned sequences (data not shown) were obtained,suggesting that Type 2 (cytosine ? thymine/guanine ?adenine) miscoding lesions represented the majority ofdamage-derived miscoding lesions in most of specimens(Supporting Information File 3). This was typical of an-cient DNA and consistent with previous studies (Broth-erton et al., 2007; Gilbert et al., 2007), despite severaltransversions and more Type 1 (thymine-[cytosine/adenine-[guanine) miscoding lesions than Type 2 insome specimens, probably due to insufficient fidelity ofTaq polymerase. Additionally, to trace potential labora-tory-based contamination, a randomly selected subsam-ple of five teeth (1A, 2A, 4B, 5D, and 11A) was sent toJilin University for independent replication, and ourresults were verified. The other 17 specimens were notincluded for further analysis, because four yielded incon-gruity between HVR I sequences and coding regionSNPs, and 13 failed to be replicated within laboratory.

Phylogenetic analysis

A total of 314 nucleotides, corresponding to position16,053–16,366 in rCRS (Andrews et al., 1999), weresequenced. The total alignment included 81 substitu-tions, of which 74 were affected by transitions and sevenby transversions, whereas no deletion or insertion wasobserved. All the 35 mtDNA profiles were assigned todifferent haplogroups (hgs) based on both HVR I motifsand coding region SNPs following Yao et al. (2003).

Maternal relationship between some individuals

The archaeologists speculated that specimens from thesame burial location (the samples sharing the first num-ber of the code such as 1A, 1B, and 1E) were likelygenetically related (Zhang, 2002), As expected, five pairsof specimens, that is, A-1B, 4E-4G, 8D-8F, 16A-16B, and25C-25G, shared consistent profiles, respectively, reveal-ing their maternal relationships. Consequently, only oneof these five pairs was included in the further analysis,reducing the final sample size to 30.

Fig. 1. Geographic location of Gavaerk Site (GAV). GAV wasmarked as dark pentagram.

315PREHISTORIC ADMIXTURE

American Journal of Physical Anthropology

TABLE

1.MtD

NA

HVR

Imotifs,

codingregionSNPs,

andhaplogroupsassignmen

tof

35sp

ecim

enfrom

GAV

Specim

enHVR

Imotif

(nt1

16,000)

SNP

663

3,010

4,216

4,715

4,833

5,178

5,301

5,417

7,028

9,055

9,824

10,400

12,308

12,406

12,705

13,263

Age

hg

hg

AD4

TJ

M8

GD

D5

N9

HK

M7

MU

F1

RC

Gen

der

rCRS

AG

TA

AC

AG

CG

TC

AG

CA

1Aa

M[55

U4

134183C

189356

–.

..

..

.–

T–

––

..

1B

F30–35

U4

134183C

189356

–.

..

..

.–

T–

––

..

1E

M35–40

D223362

Ab

Tb

2A

M15–17

D362

–.

––

.A

.–

Tb

.T

.T

.2C

F14–23

C223298327

–.

.G

.–

–.

T.

T–

TG

b

2E

F~35

M*

209223362

–.

–.

..

.–

T.

T–

T.

2G

F14–16

F1

rCRS

..

..

.–

.–

T.

.–

Ab

..

3C

M~35

M10

92193223311

357

Tb

3F

M~30

NrC

RS

–.

––

.–

.–

Tb

..

–G

bT

.3G

M15–18

H311

..

..

.–

..

..

––

..

3M

aM

[56

R*

71357

–.

––

..

.–

T.

––

..

3Pa

F20–22

R*

223356

..

..

..

..

Tb

..

–.

.4A

F50–55

D4

223274362

–A

––

.A

.–

T.

––

T.

4B

M13

C223298309327

..

.G

..

..

T.

T–

TG

b

4E

M20–25

M13a

145148188189223

..

..

..

..

T.

T–

T.

4G

M14–15

M13a

145148188189223

–.

..

.–

–.

T.

T.

T.

5D

M35–40

F1a

129172293304

Cb

Ab

7D

a?

adult

K224311

..

..

..

.–

TAb

––

–.

.8D

M20–22

M*

93

–.

..

..

..

T.

T–

T.

8F

M12–13

M*

93

–.

..

.–

–.

T.

T–

T.

9D

M18–20

UrC

RS

..

..

..

..

Tb

..

GT

.11

Aa

M~25

F1

rCRS

..

..

.–

.–

Tb

.–

–Ab

..

13

M40–45

H305T311

–.

..

..

.–

..

––

..

14A

M~16

DrC

RS

–.

.a/g

.A

.–

Tb

.–

–T

.16A

M50–55

D173223

Ab

Tb

16B

F[50

D173223

..

..

.A

..

T.

––

T.

17A

M18

D11

4A

223362

–.

..

.A

..

T.

.–

T.

17B

F20–25

D223

–.

..

.A

..

T.

.–

T.

22A

M20–22

F1

rCRS

–.

.–

–.b

.–

Tb

––

–Ab

..

23F

F~55

F1

114A

187192256

266304357

–.

.–

..

.–

T.

––

Ab

..

25C

M50–55

D189223362

–.

.–

.A

.–

T.

––

T.

25Fa

F30–35

U2e

129C

183C

362

..

..

..

.–

T.

.G

..

25G

F30–35

D189223362

..

..

.A

..

Tb

.–

–T

.25H

aF

22–25

T126294

..

C.

..

.–

T.

–.

..

27a

M40–45

H311

..

..

..

a/g

..

..

..

.

‘‘–’’indictesnoSNaPsh

otresu

ltsanddotsindicate

neither

SNaPsh

otnor

RFLPwasconducted

.Sites

are

numbered

accordingto

therevised

CRS(A

ndrewset

al.,1999).Thesu

ffixes

A,T,andC

indicate

transversion

s.aThesp

ecim

enwasindep

enden

tlyreplicatedin

Jilin

University.

bSNP

wasverified

byRFLP.

316 F. ZHANG ET AL.


Genetic composition

To investigate the genetic relationship between prehis-toric and contemporary populations, a comparison ofmtDNA profiles of 35 GAV individuals with those of9,962 contemporary and 166 prehistoric samples (Sup-porting Information File 4) from Eurasian continent wasconducted. All the contemporary samples were groupedby geographic locations. Because some hgs, for example,hg H, were prevalent in Europe (Macaulay et al., 1999),and, in East Asia, other hgs were of a much higher fre-quency than in other places of the World (Kivisild et al.,2002), they were assigned into WE and EE group respec-tively. And the other hgs, including South Asia-specifichgs, were grouped as ‘‘other’’ (Supporting InformationFile 5). The EE lineages included hgs A, B, F, and N9aof the major N trunk, as well as C, D, G, and Z of themacrohaplogroup M, which are prevalent in East Asianpopulations. The WE lineages were composed of hgs HV,preHV, N1, J, T, U, K, I, W, and X, which are Europe-specific. The proportions of both WE and EE lineages(Table 2) were calculated by summing-up frequencies ofhgs, respectively. The prehistoric population GAV wascomposed of 27% WE and 57% EE lineages, showing evi-dent admixture of the West and the East Eurasians.To understand geographic distribution of EE and WElineages, the relationship between the proportions and

longitudes of each population group was plotted inFigure 1. The EE lineages (Fig. 2a) showed a decreasingeast-to-west cline, while that of WE group (Fig. 2b) dis-played the opposite pattern, both showing more drasticchanges in Central Asia and Xinjiang than elsewhere.

DISCUSSION

In this study, we successfully analyzed maternalgenetic profiles of 35 specimens at Gavaerk site. Thehigh-amplification success (35 of 52 5 67%) suggestedthat these specimens were in excellent preservation,which was supported by their appearance (SupportingInformation File 1). Given the extensive precautions [asdescribed in Authentication of Xu et al. (2008)] weadopted, the mtDNA profiles of these 35 samples wereconsidered to be authentic.Previous studies (Comas et al., 1998; Perez-Lezaun et

al., 1999; Karafet et al., 2001; Wells et al., 2001; Zerjalet al., 2002; Comas et al., 2004; Quintana-Murci et al.,2004; Yao et al., 2004; Chaix et al., 2008; Xu and Jin,2008; Yang et al., 2008) unveiled that contemporary pop-ulations in Central Asia and Xinjiang were geneticallyadmixed. In this study, our analysis (Fig. 2 and Table 2)also showed that they bore higher proportion of EE line-ages compared with populations from Europe and NearEast and much more WE lineages than those from East

TABLE 2. Geographic and genetic information of contemporary and ancient populations in this study

Geographic location Population Latitude Longitude WE lineages EE lineages

Europe NWE 50.9 1.1 0.99 0.00MD 39.7 8.5 0.96 0.01NCE 51.5 10.4 0.98 0.00SEE 43.9 21.7 0.97 0.01NEE 51.7 22.2 0.98 0.02

Near East and Caucasus NE 35.5 39.8 0.84 0.03CAU 45.2 54.9 0.82 0.07

Central Asia and Xinjiang TUR 38.9 60.6 0.58 0.32UZB 41.0 64.6 0.51 0.38TAI 38.9 69.5 0.67 0.27KAZ 44.0 72.9 0.37 0.52KRY 41.6 73.6 0.25 0.67Uigur 42.7 81.1 0.42 0.51XUK 42.2 81.6 0.28 0.61XHM 44.2 87.7 0.10 0.88

East Asia CQ 35.5 98.1 0.04 0.79MOG 47.9 106.3 0.09 0.78SWC 25.3 110.6 0.00 0.82NH 37.6 113.6 0.02 0.80SH 27.5 114.3 0.00 0.90NIM 48.8 120.2 0.05 0.93KOR 36.9 127.3 0.00 0.84JAP 36.3 138.7 0.00 0.92

Siberia NWS 63.4 70.0 0.59 0.37NS 72.0 107.8 0.21 0.79SCS 54.0 102.5 0.16 0.79NCS 66.5 121.3 0.20 0.80NES 67.5 170.0 0.00 1.00

South Asia PNI 32.9 72.9 0.50 0.07Ancient DAN 55.4 10.1 0.97 0.00

HUNG 47.3 19.2 0.85 0.07KAZA 47.0 72.9 0.78 0.15GAV 38.0 85.6 0.27 0.57LAJ 36.2 102.6 0.00 0.75HUN 49.4 103.7 0.12 0.82WAN 41.3 111.7 0.08 0.33HA 42.1 115.3 0.00 0.76

For population codes, see Supporting Information File 2.



Asia. And the drastic changes of both WE and EE line-ages of contemporary populations in Central Asia andXinjiang (see Fig. 2) provided additional information onthe extent of genetic admixture in Eurasia continent.Because both WE and EE mtDNA lineages wereobserved in GAV, as seen in these contemporary CentralAsia populations, it could be concluded that geneticadmixture indeed existed in GAV.

Given substitution rate of human mtDNA HVR[0.32/site/million years, 95% CI 0.065–0.97 (Sigurgar-dottir et al., 2000)], the estimated probability of no sub-stitutions over 2,500 years on the 314 nucleotides was0.787, so that the distribution of identical sequenceswith GAV individuals might provide clues to their ori-gins. Therefore, we searched the profiles of 9,962 con-temporary samples for the shared haplotypes with GAV

Fig. 2. Plots of geographic distribution of EE and WE lineages. The curves are expected lines using logistic function based oncontemporary samples only.

Fig. 3. Plots of shared haplotypes of four GAV specimens. A dot represents a contemporary sample that has the same haplotypewith the specific GAV specimen. (a) specimen 4B (hg C, 16223-16298-16309-16327); (b) 4E (hg M13a, 16145-16148-16188-16189-16223); (c) 3G and 27 (hg H, 16311); (d) 7D (hg K, 16224-16311).

318 F. ZHANG ET AL.


specimens and plotted them onto Eurasian continent(see Fig. 3). The haplotypes of GAV specimen 4B (hg C)and 4E (hg M13a) were shared by several contemporarysamples in Siberia and/or East Asia, whereas specimens3G (hg H), 27 (hg H) and 7D (hg K) had the samehaplotypes with those in Europe and/or Near East. Thedistributions of these four hgs were consistent with theprevious studies (Macaulay et al., 1999; Kivisild et al.,2002), that is, hg C and M13a are specific to EE popula-tions, whereas hg H and K are prevalent in Europe.Consequently, the distributions of shared haplotypes(Supporting Information File 6) suggested that speci-mens have maternal ancestors of EE origins, of which5D and 2G might be genetically related with populationsin south China; specimens 3M, 9D, 3G, 27, and 7D havematernal ancestors of WE origins; specimens 25F and1A shared motifs with samples in both West and EastEurasians. Taken together, most of GAV individualscould find their ‘‘close relatives’’ in the contemporarysamples in the West and/or the East Eurasia, and fur-ther study of the places of origins of those hgs could pro-vide a more detailed picture of the initial contact of theWest and the East.In conclusion, this study of mtDNA profiles of prehis-

toric inhabitants in southern Xinjiang showed that thegenetic admixture of the West and the East Eurasiansexisted in GAV. More studies on genetic profiles of an-cient inhabitants from extensive areas and different agesare necessary for further understanding of geneticadmixture in Central Asia and Xinjiang.

Accession numbers

Sequences are available in GenBank (accession num-bers FJ809949–FJ809983).

Authors’ contributions

Conceived and designed the experiments: FZ, ZX, andLJ. Performed the experiments: ZX, YS, and BX. Ana-lyzed the data: FZ, ZX, and LJ. Contributed reagents/materials/analysis tools: SL, GG, ZJ, and TZ. Independentreplication: XZ and ZH. Wrote the paper: FZ, ZX, and LJ.

ACKNOWLEDGMENTS

We thank Dr. Kangxin Han (Chinese Academy ofSocial Sciences, Beijing, China) for critical suggestion ofthe manuscript.

LITERATURE CITED

Andrews RM, Kubacka I, Chinnery PF, Lightowlers RN, Turn-bull DM, Howell N. 1999. Reanalysis and revision of the Cam-bridge reference sequence for human mitochondrial DNA. NatGenet 23:147.

Bandelt HJ, Kong QP, Richards M, Macaulay V. 2006. Estima-tion of mutation rates and coalescence times: some caveats.In: Bandelt HJ, Macaulay V, Richards M, editors. Human mi-tochondrial DNA and the evolution of Homo sapiens. Berlin,Germany: Springer-Verlag. p 47–90.

Brotherton P, Endicott P, Sanchez JJ, Beaumont M, Barnett R,Austin J, Cooper A. 2007. Novel high-resolution characteriza-tion of ancient DNA reveals C [ U-type base modificationevents as the sole cause of post mortem miscoding lesions.Nucleic Acids Res 35:5717–5728.

Chaix R, Austerlitz F, Hegay T, Quintana-Murci L, Heyer E.2008. Genetic traces of east-to-west human expansion wavesin Eurasia. Am J Phys Anthropol 136:309–317.

Comas D, Calafell F, Mateu E, Perez-Lezaun A, Bosch E, Martı-nez-Arias R, Clarimon J, Facchini F, Fiori G, Luiselli D, Pet-tener D, Bertranpetit J. 1998. Trading genes along the silkroad: mtDNA sequences and the origin of central Asian popu-lations. Am J Hum Genet 63:1824–1838.

Comas D, Plaza S, Wells RS, Yuldaseva N, Lao O, Calafell F,Bertranpetit J. 2004. Admixture, migrations, and dispersalsin Central Asia: evidence from maternal DNA lineages. Eur JHum Genet 12:495–504.

Finnila S, Lehtonen MS, Majamaa K. 2001. Phylogenetic net-work for European mtDNA. Am J Hum Genet 68:1475–1484.

Gilbert MT, Binladen J, Miller W, Wiuf C, Willerslev E, PoinarH, Carlson JE, Leebens-Mack JH, Schuster SC. 2007. Rechar-acterization of ancient DNA miscoding lesions: insights in theera of sequencing-by-synthesis. Nucleic Acids Res 35:1–10.

Han K. 1998. The physical anthropology of the ancient popula-tions of the Tarim Basin and surrounding areas. In: Mair,VH, editor. The Bronze Age and early Iron Age peoples ofeastern Central Asia, Vol. 2. Philadelphia: University of Penn-sylvania Museum. p 558–570.

Hofreiter M, Serre D, Poinar HN, Kuch M, Paabo S. 2001.Ancient DNA. Nat Rev Genet 2:353–359.

Hoss M, Jaruga P, Zastawny TH, Dizdaroglu M, Paabo S. 1996.DNA damage and DNA sequence retrieval from ancient tis-sues. Nucleic Acids Res 24:1304–1307.

Karafet T, Xu L, Du R, Wang W, Feng S, Wells RS, Redd AJ,Zegura SL, Hammer MF. 2001. Paternal population history ofEast Asia: sources, patterns, and microevolutionary processes.Am J Hum Genet 69:615–628.

Kivisild T, Tolk HV, Parik J, Wang Y, Papiha SS, Bandelt HJ,Villems R. 2002. The emerging limbs and twigs of the EastAsian mtDNA tree. Mol Biol Evol 19:1737–1751.

Kong QP, Yao YG, Sun C, Bandelt HJ, Zhu CL, Zhang YP. 2003.Phylogeny of east Asian mitochondrial DNA lineages inferredfrom complete sequences. Am J Hum Genet 73:671–676.

Lalueza-Fox C, Sampietro ML, Gilbert MT, Castri L, Facchini F,Pettener D, Bertranpetit J. 2004. Unravelling migrations inthe steppe: mitochondrial DNA sequences from ancient cen-tral Asians. Proc Biol Sci 271:941–947.

Macaulay V, Richards M, Hickey E, Vega E, Cruciani F, Guida V,Scozzari R, Bonne-Tamir B, Sykes B, Torroni A. 1999. Theemerging tree of West Eurasian mtDNAs: a synthesis of control-region sequences and RFLPs. Am J Hum Genet 64:232–249.

Mair V. 1995. Prehistoric Caucasoid corpses of the Tarim Basin.J Indo Eur Stud 23:281–307.

Mallory JP, Mair VH. 2000. The Tarim mummies. London:Thames and Hudson.

Perez-Lezaun A, Calafell F, Comas D, Mateu E, Bosch E, Marti-nez-Arias R, Clarimon J, Fiori G, Luiselli D, Facchini F, Pet-tener D, Bertranpetit J. 1999. Sex-specific migration patternsin Central Asian populations, revealed by analysis of Y-chro-mosome short tandem repeats and mtDNA. Am J Hum Genet65:208–219.

Quintana-Murci L, Chaix R, Wells RS, Behar DM, Sayar H, Scoz-zari R, Rengo C, Al-Zahery N, Semino O, Santachiara-Benere-cetti AS, Coppa A, Ayub Q, Mohyuddin A, Tyler-Smith C,Qasim Mehdi S, Torroni A, McElreavey K. 2004. Where westmeets east: the complex mtDNA landscape of the southwestand Central Asian corridor. Am J Hum Genet 74:827–845.

Sigurgardottir S, Helgason A, Gulcher JR, Stefansson K, Don-nelly P. 2000. The mutation rate in the human mtDNA con-trol region. Am J Hum Genet 66:1599–1609.

Wells RS, Yuldasheva N, Ruzibakiev R, Underhill PA, EvseevaI, Blue-Smith J, Jin L, Su B, Pitchappan R, Shanmuga-lakshmi S, Balakrishnan K, Read M, Pearson NM, Zerjal T,Webster MT, Zholoshvili I, Jamarjashvili E, Gambarov S, Nik-bin B, Dostiev A, Aknazarov O, Zalloua P, Tsoy I, Kitaev M,Mirrakhimov M, Chariev A, Bodmer WF. 2001. The Eurasianheartland: a continental perspective on Y-chromosome diver-sity. Proc Natl Acad Sci USA 98:10244–10249.



Xu S, Jin L. 2008. A Genome-wide analysis of admixture inUyghurs and a high-density admixture map for disease-genediscovery. Am J Hum Genet 83:322–336.

Xu Z, Zhang F, Xu B, Tan J, Li S, Jin L. 2009. Improving thesensitivity of negative controls in ancient DNA extractions.Electrophoresis 30:1–4.

Xu Z, Zhang F, Xu B, Tan J, Li S, Li C, Zhou H, Zhu H, ZhangJ, Duan Q, Jin L. 2008. Mitochondrial DNA evidence for adiversified origin of workers building First Emperor of China.PLoS ONE 3:e3275.

Yang L, Tan S, Yu H, Zheng B, Qiao E, Dong Y, Zan R, Xiao C.2008. Gene admixture in ethnic populations in upper part ofSilk Road revealed by mtDNA polymorphism. Sci China CLife Sci 51:435–444.

Yao YG, Kong QP, Man XY, Bandelt HJ, Zhang YP. 2003.Reconstructing the evolutionary history of China: a caveatabout inferences drawn from ancient DNA. Mol Biol Evol20:214–219.

Yao YG, Kong QP, Wang CY, Zhu CL, Zhang YP. 2004. Differ-ent matrilineal contributions to genetic structure of ethnicgroups in the silk road region in china. Mol Biol Evol21:2265–2280.

Zerjal T, Wells RS, Yuldasheva N, Ruzibakiev R, Tyler-Smith C.2002. A genetic landscape reshaped by recent events: Y-chromo-somal insights into central Asia. Am J Hum Genet 71:466–482.

Zhang J. 2002. Studies of human skulls in Gavaerk site inQiemo, Xinjiang. Proceedings of the International Symposiumof Anthropological Studies at Fudan University.


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prehistorical east–west admixture of maternal lineages in a 2,500-year-old population in xinjiang

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