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Strong genetic admixture in the Altai at the Middle Bronze Age revealed by uniparental and ancestry informative markers

      Abstract

      The Altai Mountains have been a long-term boundary zone between the Eurasian Steppe populations and South and East Asian populations. To disentangle some of the historical population movements in this area, 14 ancient human specimens excavated in the westernmost part of the Mongolian Altai were studied. Thirteen of them were dated from the Middle to the End of the Bronze Age and one of them to the Eneolithic period. The environmental conditions encountered in this region led to the good preservation of DNA in the human remains. Therefore, a multi-markers approach was adopted for the genetic analysis of identity, ancestry and phenotype markers. Mitochondrial DNA analyses revealed that the ancient Altaians studied carried both Western (H, U, T) and Eastern (A, C, D) Eurasian lineages. In the same way, the patrilineal gene pool revealed the presence of different haplogroups (Q1a2a1-L54, R1a1a1b2-Z93 and C), probably marking different origins for the male paternal lineages. To go further in the search of the origin of these ancient specimens, phenotypical characters (i.e. hair and eye color) were determined. For this purpose, we adapted the HIrisPlex assay recently described to MALDI-TOF mass spectrometry. In addition, some ancestry informative markers were analyzed with this assay. The results revealed mixed phenotypes among this group confirming the probable admixed ancestry of the studied Altaian population at the Middle Bronze Age. The good results obtained from ancient DNA samples suggest that this approach might be relevant for forensic casework too.

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      References

        • Kuzmina E.E.
        The Prehistory of the Silk Road.
        University of Pennsylvania Press, 2008
        • Di Cosmo N.
        • Frank A.J.
        • Golden P.B.
        The Cambridge history of Inner Asia: The Chinggisid Age.
        Cambridge University Press, 2009
        • Grousset R.
        L’empire des steppes.
        Editions Payot, 1989
        • Sinor D.
        The Cambridge History of Early Inner Asia.
        Cambridge University Press, 1990: 1
        • Derenko M.V.
        • Grzybowski T.
        • Malyarchuk B.A.
        • Dambueva I.K.
        • Denisova G.A.
        • Czarny J.
        • Dorzhu C.M.
        • Kakpakov V.T.
        • Miscicka-Sliwka D.
        • Wozniak M.
        • et al.
        Diversity of mitochondrial DNA lineages in South Siberia.
        Ann. Hum. Genet. 2003; 67: 391-411
        • Dulik M.C.
        • Zhadanov S.I.
        • Osipova L.P.
        • Askapuli A.
        • Gau L.
        • Gokcumen O.
        • Rubinstein S.
        • Schurr T.G.
        Mitochondrial DNA and Y chromosome variation provides evidence for a recent common ancestry between Native Americans and Indigenous Altaians.
        Am. J. Hum. Genet. 2012; 90: 229-246
        • Kharkov V.N.
        • Stepanov V.A.
        • Medvedeva O.F.
        • Spiridonova M.G.
        • Voevoda M.I.
        • Tadinova V.N.
        • Puzyrev V.P.
        Gene pool differences between northern and southern Altaians inferred from the data on Y-chromosomal haplogroups.
        Russ. J. Genet. 2007; 43: 551-562
        • Keyser C.
        • Bouakaze C.
        • Crubezy E.
        • Nikolaev V.G.
        • Montagnon D.
        • Reis T.
        • Ludes B.
        Ancient DNA provides new insights into the history of south Siberian Kurgan people.
        Hum. Genet. 2009; 126: 395-410
        • Mendisco F.
        • Keyser C.
        • Hollard C.
        • Seldes V.
        • Nielsen A.E.
        • Crubezy E.
        • Ludes B.
        Application of the iPLEX™ Gold SNP genotyping method for the analysis of Amerindian ancient DNA samples: benefits for ancient population studies.
        Electrophoresis. 2011; 32: 386-393
        • Carnese F.R.
        • Mendisco F.
        • Keyser C.
        • Dejean C.B.
        • Dugoujon J.M.
        • Bravi C.M.
        • Ludes B.
        • Crubezy E.
        Paleogenetical study of pre-Columbian samples from Pampa Grande (Salta, Argentina).
        Am. J. Phys. Anthropol. 2010; 141: 452-462
        • Parson W.
        • Dür A.
        EMPOP – a forensic mtDNA database.
        Forensic Sci. Int. Genet. 2007; 1: 88-92
        • Röck A.W.
        • Dür A.
        • van Oven M.
        • Parson W.
        Concept for estimating mitochondrial DNA haplogroups using a maximum likelihood approach (EMMA).
        Forensic Sci. Int. Genet. 2013; 7: 601-609
        • Walsh S.
        • Liu F.
        • Wollstein A.
        • Kovatsi L.
        • Ralf A.
        • Kosiniak-Kamysz A.
        • Branicki W.
        • Kayser M.
        The HIrisPlex system for simultaneous prediction of hair and eye colour from DNA.
        Forensic Sci. Int. Genet. 2013; 7: 98-115
        • Fondevila M.
        • Phillips C.
        • Santos C.
        • Freire Aradas A.
        • Vallone P.M.
        • Butler J.M.
        • Lareu M.V.
        • Carracedo A.
        Revision of the SNPforID 34-plex forensic ancestry test: assay enhancements, standard reference sample genotypes and extended population studies.
        Forensic Sci. Int. Genet. 2013; 7: 63-74
        • Kosoy R.
        • Nassir R.
        • Tian C.
        • White P.A.
        • Butler L.M.
        • Silva G.
        • Kittles R.
        • Alarcon-Riquelme M.E.
        • Gregersen P.K.
        • Belmont J.W.
        • et al.
        Ancestry informative marker sets for determining continental origin and admixture proportions in common populations in America.
        Hum. Mutat. 2009; 30: 69-78
        • Phillips C.
        • Salas A.
        • Sanchez J.J.
        • Fondevila M.
        • Gomez-Tato A.
        • Alvarez-Dios J.
        • Calaza M.
        • de Cal M.C.
        • Ballard D.
        • Lareu M.V.
        • et al.
        Inferring ancestral origin using a single multiplex assay of ancestry-informative marker SNPs.
        Forensic Sci. Int. Genet. 2007; 1: 273-280
        • Pritchard J.K.
        • Stephens M.
        • Donnelly P.
        Inference of population structure using multilocus genotype data.
        Genetics. 2000; 155: 945-959
        • Regueiro M.
        • Alvarez J.
        • Rowold D.
        • Herrera R.J.
        On the origins, rapid expansion and genetic diversity of Native Americans from hunting-gatherers to agriculturalists.
        Am. J. Phys. Anthropol. 2013; 150: 333-348
        • Qamar R.
        • Ayub Q.
        • Mohyuddin A.
        • Helgason A.
        • Mazhar K.
        • Mansoor A.
        • Zerjal T.
        • Tyler-Smith C.
        • Mehdi S.Q.
        Y-chromosomal DNA variation in Pakistan.
        Am. J. Hum. Genet. 2002; 70: 1107-1124
        • Hedman M.
        • Brandstätter A.
        • Pimenoff V.
        • Sistonen P.
        • Palo J.U.
        • Parson W.
        • Sajantila A.
        Finnish mitochondrial DNA HVS-I and HVS-II population data.
        Forensic Sci. Int. Genet. 2007; 172: 171-178
        • Pamjav H.
        • Feher T.
        • Nemeth E.
        • Padar Z.
        Brief communication: new Y-chromosome binary markers improve phylogenetic resolution within haplogroup R1a1.
        Am. J. Phys. Anthropol. 2012; 149: 611-615
        • Underhill P.A.
        • Myres N.M.
        • Rootsi S.
        • Metspalu M.
        • Zhivotovsky L.A.
        • King R.J.
        • Lin A.A.
        • Chow C.E.
        • Semino O.
        • Battaglia V.
        • et al.
        Separating the post-Glacial coancestry of European and Asian Y chromosomes within haplogroup R1a.
        Eur. J. Hum. Genet. 2010; 18: 479-484
        • Li H.
        • Zhao X.
        • Zhao Y.
        • Li C.
        • Si D.
        • Zhou H.
        • Cui Y.
        Genetic characteristics and migration history of a bronze culture population in the West Liao-River valley revealed by ancient DNA.
        J. Hum. Genet. 2011; 56: 815-822
        • Keyser-Tracqui C.
        • Crubezy E.
        • Ludes B.
        Nuclear and mitochondrial DNA analysis of a 2,000-year-old necropolis in the Egyin Gol Valley of Mongolia.
        Am. J. Hum. Genet. 2003; 73: 247-260
        • Kim K.
        • Brenner C.H.
        • Mair V.H.
        • Lee K.H.
        • Kim J.H.
        • Gelegdorj E.
        • Batbold N.
        • Song Y.C.
        • Yun H.W.
        • Chang E.J.
        • et al.
        A western Eurasian male is found in 2000-year-old elite Xiongnu cemetery in Northeast Mongolia.
        Am. J. Phys. Anthropol. 2010; 142: 429-440
        • Zhao Y.B.
        • Li H.J.
        • Cai D.W.
        • Li C.X.
        • Zhang Q.C.
        • Zhu H.
        • Zhou H.
        Ancient DNA from nomads in 2500-year-old archeological sites of Pengyang, China.
        J. Hum. Genet. 2010; 55: 215-218
        • Zhang F.
        • Xu Z.
        • Tan J.
        • Sun Y.
        • Xu B.
        • Li S.
        • Zhao X.
        • Zhou H.
        • Gong G.
        • Zhang J.
        • et al.
        Prehistorical East-West admixture of maternal lineages in a 2,500-year-old population in Xinjiang.
        Am. J. Phys. Anthropol. 2010; 142: 314-320
        • Der Sarkissian C.
        • Balanovsky O.
        • Brandt G.
        • Khartanovich V.
        • Buzhilova A.
        • Koshel S.
        • Zaporozhchenko V.
        • Gronenborn D.
        • Moiseyev V.
        • Kolpakov E.
        • et al.
        Ancient DNA reveals prehistoric gene-flow from Siberia in the complex human population history of North East Europe.
        PLoS Genet. 2013; 9: e1003296
        • Lalueza-Fox C.
        • Sampietro M.L.
        • Gilbert M.T.
        • Castri L.
        • Facchini F.
        • Pettener D.
        • Bertranpetit J.
        Unravelling migrations in the steppe: mitochondrial DNA sequences from ancient central Asians.
        Proc. Biol. Sci. R. Soc. 2004; 271: 941-947
        • Chikisheva T.A.
        • Gubina M.A.
        • Kulikov I.V.
        • Karafet T.M.
        • Voevoda M.I.
        • Romaschenko A.G.
        A paleogenetic study of the prehistoric populations of the Altai.
        Archeol. Ethnol. Anthropol. Eurasia. 2007; 4: 130-142
        • Clisson I.
        • Keyser C.
        • Francfort H.P.
        • Crubezy E.
        • Samashev Z.
        • Ludes B.
        Genetic analysis of human remains from a double inhumation in a frozen kurgan in Kazakhstan (Berel site, Early 3rd Century BC).
        Int. J. Legal Med. 2002; 116: 304-308
        • Gao S.
        • Cui Y.
        • Yang Y.
        • Duan R.
        • Abuduresule I.
        • Mair V.H.
        • Zhu H.
        • Zhou H.
        Mitochondrial DNA analysis of human remains from the Yuansha site in Xinjiang, China.
        Sci. China Ser. C Life Sci./Chin. Acad. Sci. 2008; 51: 205-213
        • Li C.
        • Li H.
        • Cui Y.
        • Xie C.
        • Cai D.
        • Li W.
        • Mair V.H.
        • Xu Z.
        • Zhang Q.
        • Abuduresule I.
        • et al.
        Evidence that a West-East admixed population lived in the Tarim Basin as early as the early Bronze Age.
        BMC Biol. 2010; 8: 15
        • Crubezy E.
        • Alekeev A.
        Chamane: Kyys, jeune fille des glaces.
        Editions Errance, 2007
        • Gonzalez-Ruiz M.
        • Santos C.
        • Jordana X.
        • Simon M.
        • Lalueza-Fox C.
        • Gigli E.
        • Aluja M.P.
        • Malgosa A.
        Tracing the origin of the east-west population admixture in the Altai region (Central Asia).
        PLOS ONE. 2012; 7: e48904
        • Wells R.S.
        • Yuldasheva N.
        • Ruzibakiev R.
        • Underhill P.A.
        • Evseeva I.
        • Blue-Smith J.
        • Jin L.
        • Su B.
        • Pitchappan R.
        • Shanmugalakshmi S.
        • et al.
        The Eurasian heartland: a continental perspective on Y-chromosome diversity.
        Proc. Natl. Acad. Sci. U. S. A. 2001; 98: 10244-10249
        • Bortolini M.C.
        • Salzano F.M.
        • Thomas M.G.
        • Stuart S.
        • Nasanen S.P.
        • Bau C.H.
        • Hutz M.H.
        • Layrisse Z.
        • Petzl-Erler M.L.
        • Tsuneto L.T.
        • et al.
        Y-chromosome evidence for differing ancient demographic histories in the Americas.
        Am. J. Hum. Genet. 2003; 73: 524-539
        • Karafet T.M.
        • Zegura S.L.
        • Posukh O.
        • Osipova L.
        • Bergen A.
        • Long J.
        • Goldman D.
        • Klitz W.
        • Harihara S.
        • de Knijff P.
        • et al.
        Ancestral Asian source(s) of new world Y-chromosome founder haplotypes.
        Am. J. Hum. Genet. 1999; 64: 817-831
        • Santos F.R.
        • Pandya A.
        • Tyler-Smith C.
        • Pena S.D.
        • Schanfield M.
        • Leonard W.R.
        • Osipova L.
        • Crawford M.H.
        • Mitchell R.J.
        The central Siberian origin for native American Y chromosomes.
        Am. J. Hum. Genet. 1999; 64: 619-628
        • Zegura S.L.
        • Karafet T.M.
        • Zhivotovsky L.A.
        • Hammer M.F.
        High-resolution SNPs and microsatellite haplotypes point to a single, recent entry of Native American Y chromosomes into the Americas.
        Mol. Biol. Evol. 2004; 21: 164-175
        • Draus-Barini J.
        • Walsh S.
        • Pospiech E.
        • Kupiec T.
        • Glab H.
        • Branicki W.
        • Kayser M.
        Bona fide colour: DNA prediction of human eye and hair colour from ancient and contemporary skeletal remains.
        Investig. Genet. 2013; 4: 3