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The Genome-Wide Structure of the Jewish People

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The Genome-Wide Structure of the Jewish People doi:10.1038/nature09103 LETTERS The genome-wide structure of the Jewish people Doron M. Behar1,2*, Bayazit Yunusbayev2,3*, Mait Metspalu2*, Ene Metspalu2, Saharon Rosset4,Ju¨ri Parik2, Siiri Rootsi2, Gyaneshwer Chaubey2, Ildus Kutuev2,3, Guennady Yudkovsky1,5, Elza K. Khusnutdinova3, Oleg Balanovsky6, Ornella Semino7, Luisa Pereira8,9, David Comas10, David Gurwitz11, Batsheva Bonne-Tamir11, Tudor Parfitt12, Michael F. Hammer13, Karl Skorecki1,5 & Richard Villems2 Contemporary Jews comprise an aggregate of ethno-religious communities clustered close to each other and intermediate between communities whose worldwide members identify with each other non-Jewish Middle Eastern and European populations10. through various shared religious, historical and cultural tradi- Illumina 610K and 660K bead arrays were used to genotype 121 tions1,2. Historical evidence suggests common origins in the Middle samples from 14 Jewish communities. The results were compared East, followed by migrations leading to the establishment of com- with 1,166 individuals from 69 non-Jewish populations (Supplemen- munities of Jews in Europe, Africa and Asia, in what is termed the tary Note 1 and Supplementary Table 1), with particular attention to Jewish Diaspora3–5. This complex demographic history imposes neighbouring or ‘host’ populations in corresponding geographic special challenges in attempting to address the genetic structure regions. These results were also integrated with analyses of genotype of the Jewish people6. Although many genetic studies have shed data from about 8,000 Y chromosomes and 14,000 mitochondrial light on Jewish origins and on diseases prevalent among Jewish DNA (mtDNA) samples (Supplementary Note 6 and Supplemen- communities, including studies focusing on uniparentally and tary Tables 4 and 5). Several questions were then addressed: What biparentally inherited markers7–16, genome-wide patterns of are the locations of the various Jewish communities in a global genetic variation across the vast geographic span of Jewish Diaspora com- variation context? What are the features of the Middle Eastern (Sup- munities and their respective neighbours have yet to be addressed. plementary Fig. 1) population genetic substructure? What are the Here we use high-density bead arrays to genotype individuals from genetic distances between contemporary Jewish communities, their 14 Jewish Diaspora communities and compare these patterns of Diaspora neighbours and Middle Eastern populations? Can the genetic genome-wide diversity with those from 69 Old World non-Jewish origin of Jews be pinpointed within the Middle East? populations, of which 25 have not previously been reported. The EIGENSOFT package24 was used to identify the principal These samples were carefully chosen to provide comprehensive components (PCs) of autosomal variation in our Old World sample comparisons between Jewish and non-Jewish populations in the set (Fig. 1 and Supplementary Fig. 2a). This analysis places the Diaspora, as well as with non-Jewish populations from the Middle studied samples along two well-established geographic axes of global East and north Africa. Principal component and structure-like genetic variation18,19,22: PC1 (sub-Saharan Africa versus the rest of the analyses identify previously unrecognized genetic substructure Old World) and PC2 (east versus west Eurasia). Focusing on the within the Middle East. Most Jewish samples form a remarkably Middle Eastern populations in the PC1–PC2 plot (Fig. 1b) reveals tight subcluster that overlies Druze and Cypriot samples but not more geographically refined groupings. Populations of the Caucasus, samples from other Levantine populations or paired Diaspora host flanked by Cypriots, form an almost uninterrupted rim that separates populations. In contrast, Ethiopian Jews (Beta Israel) and Indian the bulk of Europeans from Middle Eastern populations. Bedouins, Jews (Bene Israel and Cochini) cluster with neighbouring auto- Jordanians, Palestinians and Saudi Arabians are located in close chthonous populations in Ethiopia and western India, respec- proximity to each other, which is consistent with a common origin tively, despite a clear paternal link between the Bene Israel and in the Arabian Peninsula25, whereas the Egyptian, Moroccan, the Levant. These results cast light on the variegated genetic archi- Mozabite Berber, and Yemenite samples are located closer to sub- tecture of the Middle East, and trace the origins of most Jewish Saharan populations (Fig. 1a and Supplementary Fig. 2a). Diaspora communities to the Levant. Most Jewish samples, other than those from Ethiopia and India, Recently, the capacity to obtain whole-genome genotypes with the overlie non-Jewish samples from the Levant (Fig. 1b). The tight cluster use of array technology has provided a robust tool for elucidating fine- comprising the Ashkenazi, Caucasus (Azerbaijani and Georgian), scale population structure and aspects of demographic history17–23. Middle Eastern (Iranian and Iraqi), north African (Moroccan) and This approach, initially used to account for population stratification Sephardi (Bulgarian and Turkish) Jewish communities, as well as in genome-wide association studies, identified genome-wide patterns Samaritans, strongly overlaps Israeli Druze and is centrally located of variation that distinguished between Ashkenazi Jews and non- on the principal component analysis (PCA) plot when compared with Jews of European descent7,11,12,14–16. Similarly, a large-scale survey of Middle Eastern, European Mediterranean, Anatolian and Caucasus autosomal microsatellites found that samples from four Jewish non-Jewish populations (Fig. 1). This Jewish cluster consists of 1Molecular Medicine Laboratory, Rambam Health Care Campus, Haifa 31096, Israel. 2Estonian Biocentre and Department of Evolutionary Biology, University of Tartu, Tartu 51010, Estonia. 3Institute of Biochemistry and Genetics, Ufa Research Center, Russian Academy of Sciences, Ufa 450054, Russia. 4Department of Statistics and Operations Research, School of Mathematical Sciences, Tel Aviv University, Tel Aviv 69978, Israel. 5Rappaport Faculty of Medicine and Research Institute, Technion – Israel Institute of Technology, Haifa 31096, Israel. 6Research Centre for Medical Genetics, Russian Academy of Medical Sciences, Moscow 115478, Russia. 7Dipartimento di Genetica e Microbiologia, Universita` di Pavia, Pavia 27100, Italy. 8Instituto de Patologia e Imunologia Molecular da Universidade do Porto (IPATIMUP), Porto 4200-465, Portugal. 9Faculdade de Medicina, Universidade do Porto, Porto 4200-319, Portugal. 10Institute of Evolutionary Biology (CSIC-UPF), CEXS-UPF-PRBB and CIBER de Epidemiologı´a y Salud Pu´blica, Barcelona 08003, Spain. 11Department of Human Molecular Genetics and Biochemistry, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv 69978, Israel. 12Department of the Languages and Cultures of the Near and Middle East, Faculty of Languages and Cultures, School of Oriental and African Studies (SOAS), University of London, London WC1H 0XG, UK. 13ARL Division of Biotechnology, University of Arizona, Tucson, Arizona 85721, USA. *These authors contributed equally to this work. 1 ©2010 Macmillan Publishers Limited. All rights reserved LETTERS NATURE d PtPtnn PtnPtn Sin Bur Ptn Bur Bur SinPtnPtnPt Sin Bur Bur Sinn Bur Bur Bur Bur PtnSinSinSin Sin Ptn Bur BurBur BurBur Sin Bur Bur Bur Sin Bur BurBur Blo Sin Sin Sin Sin Bur Bur SinSin Ptn Ptn Bur Bur, Burusho Si Bur IbJ Sin n Blo Ptn, Pathan IbJ Sin, Sindhi IbJ IcJ IbJ Blo, Balochi IcJIcJ IcJ Ind Ind, India (southern) IbJ, Mumbai Jews c 2 0 a IcJ, Cochini Jews EtA 0.02 EtT EJ Ind EtT EtAEtA Ind EtA Ind Mor EtT Ind Ind Ind EtA EtT EJ EtT Lit Lit Bel Ru Ru BelLitBel Ady Orc Orc HngLit Chu Ru Bel LitLit Bel Ru Ruu R b OrcLit Bel Ru Fr Lit Bel EJ FB Orc OrcOrcFr LitHng Europeans Go LLezginsezgins FB Orc Orc HngHng Hng Rmn EJ FB OrcBelHngHng AdyAdygeigei EJEJ EJ Fr Fr Orc Orc Hng HngOrcHngHngHng RmnHng Bel EJ FB FB Fr HngRmn OrcRmn Ady FBFBFB FrFr Ady EJ FB FB Fr Fr Fr Hng Hng Hngng Tur EtO FB FB FrFrFr Fr Fr Fr Rmn Arm Lzg Ady Ady Ady FBFB FB FrFr Fr Orc RmnRmnRmHngHnngn Lzg E FB Fr Fr Fr RmnRmn HngHngRmn LzgAdy LzgLzg J FB Spa Fr Fr RmnHng AdyAdy Lzg Eigenvector 1 FB FB RmnRmn GoGo Lzg Lzg Lzg ArmLzg EJ FB Spa Fr Rmn Lzg Lzg Ady Lzg Tur Ady FB Arm LzgAdy AdyLzg Ady Fr Lzg Ady Tus AJ Go Go Ady SpaTusTus Tur TurTur Tur Tus SpaSpa Go Go Go Go Arm AJ Go Tur Tur Spa Tus Go GoGo Lzg Tur Tur Fr Tur Go Go Tur Tur Tur TTus Go Armenians −0.06 −0.04 −0.02 0.00 Arm Go Go Tus SpaArm AJ Arm Arm Tur Tur ArmArm Georgians Tur ArmGo ArmArm Irn Irn Spa Arm AJ Irn Turks SpaArm ArmAJAJ GJ Tur Irn Irn SpaSp GJ AJ CyrSpaSppapa GJAzJAzJ Irn CyrSyr Arm AzJ IrnIrn Cyr SpaS Arm −0.08 AJ AJ UJ Cyr CyrCyr AJ AJAJAzJ AzJ AJ Irn Irn Cyr SJAJ AzJ IqJ Tur EtA CyrCyr AzJ AJ InJ Irn AJ AzJ Syr Druze CyrIqJ CyrSJAJIqJUJ AJ IqJSJ IqJIqJIqJ InJ InJ Cypriots DrzSJDrz Drz SJ AJAJ DrzIqJIqJ Samaritans Drz IqJ Iranians SJ DrzDrzSJ Drz Drz InJ Irn Cyr Drz Drz Drz −0.02 Sm SJ DrzSJDrzDrzDrz Syr Irn Irn Irn SbJ SJ SJ AJ SJ SJ DrzSJDrz DrzSJ Drz 0 Sm Drz Drz Drz Drz Drz Jor 000.00.02 Sm DrzMJ DrzDrz Leb 2 MJSJ Drz Drz EigenvectorE 2 Drz Drz Leb DrzDrz ector 2 0.04 0.06 Drz MJ MJDrzMJ Drz Syr SJ Drz MJ Syr MJDrz Drz MJ Leb Leb Syr MJMJ EtO Sub-Saharan Africa MJ North and east Africa MJ MJ Sdi Leb Levantine Middle East MJ Syr non-Jewish populations Irn Europe GJ Syr Jewish communities Syr MJ South Asia Irn EtO East Asia Syr Jor YJ Sdi Sdi Sdi Pal Pal Jor Mor DrzPal Pal YJ Pal Syr SdiJor Sdi Pal
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