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North African Jewish and Non-Jewish Populations Form Distinctive, Orthogonal Clusters

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North African Jewish and Non-Jewish Populations Form Distinctive, Orthogonal Clusters North African Jewish and non-Jewish populations form distinctive, orthogonal clusters Christopher L. Campbella,1, Pier F. Palamarab,1, Maya Dubrovskyc,d,1, Laura R. Botiguée, Marc Fellousf, Gil Atzmong,h, Carole Oddouxa, Alexander Pearlmana, Li Haoi, Brenna M. Hennj, Edward Burnsg, Carlos D. Bustamantej, David Comase, Eitan Friedmanc,d, Itsik Pe’erb, and Harry Ostrera,h,2 Departments of aPathology, gMedicine, and hGenetics, Albert Einstein College of Medicine, Bronx, NY 10461; bDepartment of Computer Science, Columbia University, New York, NY 10027; cSusanne Levy Gertner Oncogenetics Unit, Danek Gertner Institute of Human Genetics, Chaim Sheba Medical Center, Tel- Hashomer 52621, Israel; dSackler School of Medicine, Tel Aviv University, Ramat Aviv 69978, Israel; eInstitute of Evolutionary Biology, Consejo Superior de Investigaciones Cientificas, Universitat Pompeu Fabra, 08003 Barcelona, Spain; fCochin Institute, Institut National de la Santé et de la Recherche Médicale 567, 75014 Paris, France; iCenter for Genome Informatics, New Jersey Medical School, University of Medicine and Dentistry of New Jersey, Newark, NJ 07101; and jDepartment of Genetics, Stanford University, Stanford, CA 94305 Edited* by Arno G. Motulsky, University of Washington, Seattle, WA, and approved July 3, 2012 (received for review March 23, 2012) North African Jews constitute the second largest Jewish Diaspora and Ethiopian Jews—groups that are thought to have limited group. However, their relatedness to each other; to European, Middle Eastern Jewish ancestry (15). Middle Eastern, and other Jewish Diaspora groups; and to their Previously, using genome-wide SNP and copy number varia- former North African non-Jewish neighbors has not been well tion data, we demonstrated that Sephardic (Greek and Turkish), defined. Here, genome-wide analysis of five North African Jewish Ashkenazi (Eastern European), and Mizrahi (Iranian, Iraqi, and groups (Moroccan, Algerian, Tunisian, Djerban, and Libyan) and Syrian) Jews with origins in Europe and the Middle East were comparison with other Jewish and non-Jewish groups demon- more related to each other than to their non-Jewish contempo- strated distinctive North African Jewish population clusters with rary neighbors (16). We showed that this relatedness could be proximity to other Jewish populations and variable degrees of explained on the basis of sharing DNA segments identical by Middle Eastern, European, and North African admixture. Two descent (IBD) within and between populations. Here, we build major subgroups were identified by principal component, neigh- on this understanding of the Jewish Diasporas by extending our analyses to members of the Jewish communities in Morocco, bor joining tree, and identity-by-descent analysis—Moroccan/ Algeria, Tunisia, Djerba, Libya, Ethiopia, Yemen, and Georgia Algerian and Djerban/Libyan—that varied in their degree of Euro- and to members of non-Jewish communities from the same pean admixture. These populations showed a high degree of en- regions. We present a comprehensive population genetic analysis dogamy and were part of a larger Ashkenazi and Sephardic Jewish of North African Jews, a group that comprises the third major group. By principal component analysis, these North African group of World Jewry, following European and Middle Eastern groups were orthogonal to contemporary populations from North Jews. In addition, we extend these analyses to Georgian, Yem- and South Morocco, Western Sahara, Tunisia, Libya, and Egypt. enite, and Ethiopian Jews, thus developing a more comprehen- Thus, this study is compatible with the history of North African sive genetic map for Jewish population genetics. Jews—founding during Classical Antiquity with proselytism of lo- cal populations, followed by genetic isolation with the rise of Results Christianity and then Islam, and admixture following the emigra- North African Jewish Populations Form Distinctive Clusters with tion of Sephardic Jews during the Inquisition. Genetic Proximity to Each Other and to European and Middle Eastern Jewish Groups. SNP data were generated for 509 un- Jewish genetics | population genetics | North African genetics | related individuals (60.5% female) from the 15 Jewish pop- identical by descent sharing | deep ancestry ulations (Table 1). These SNP data were merged with selected BIOLOGY datasets from the Human Genome Diversity Project (HGDP) to POPULATION ews lived in multiple communities in North Africa for >2,000 y examine the genetic structure of Jewish populations in both J(1). Successive waves of migration from the Middle East and global and regional contexts (Fig. 1 and SI Appendix, Fig. S1). Europe, as well as conversion and admixture of local populations The first two principal components of worldwide populations (mostly thought to be Berber and here termed “Maghrebi”), showed that the North African Jewish populations clustered with contributed to the formation of Jewish communities (2). Al- the European and Middle Eastern Jewish groups and European “ ” non-Jewish groups, but not with the North African non-Jewish though termed Sephardic, the formation of these communities A antedated the presence of Jews in the Iberian Peninsula with groups, suggesting origins distinctive from the latter (Fig. 1 ). significant admixture occurring only after the expulsions from Georgian Jews formed part of this cluster, whereas Yemenite and Ethiopian Jews did not. When compared only to the Euro- Spain and Portugal in 1492 and 1497, respectively (2). From that pean, Middle Eastern, and North African Jewish and non-Jewish time up to their migration to current Israel starting in the 1940s populations, the North African Jewish populations formed and more massively in the 1950s, each of these populations lived a common but distinctive cluster—observed by principal com- in relative seclusion and was endogamous (3, 4). This separation ponents 1 and 2—that was overlapping with the Greek and led to their developing the characteristics of genetic isolates, such as high frequencies of founder mutations for Mendelian disorders and limited repertoires of mitochondrial and Y chro- Author contributions: C.L.C., P.F.P., M.D., L.R.B., M.F., G.A., C.O., A.P., L.H., B.M.H., E.B., mosomal haplotypes (5–7). C.D.B., D.C., E.F., I.P., and H.O. designed research; C.L.C., P.F.P., M.D., L.H., I.P., and H.O. The relatedness of these Jewish groups to each other, to Eu- performed research; C.L.C., P.F.P., M.D., L.H., I.P., and H.O. analyzed data; and C.L.C., ropean and Middle Eastern Jews, and to their non-Jewish North P.F.P., M.D., L.R.B., G.A., B.M.H., I.P., and H.O. wrote the paper. African neighbors has been addressed in only a fragmentary The authors declare no conflict of interest. fashion in prior studies (8–14). Most studies were limited to one *This Direct Submission article had a prearranged editor. or two North African groups. One study challenged the story line 1C.L.C., P.F.P., and M.D. contributed equally to this work. of Judean migrants, Berber tribesmen, and Sephardic Jewish 2To whom correspondence should be addressed. E-mail: [email protected]. refugees contributing to the formation of these groups by dem- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. onstrating shared ancestry between Libyan Jews and Yemenite 1073/pnas.1204840109/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1204840109 PNAS | August 21, 2012 | vol. 109 | no. 34 | 13865–13870 Downloaded by guest on September 30, 2021 Table 1. Summary of populations included in this study Jews and the other proximal to the Moroccan and Algerian Jews C Population ID Female Male Total Population (Fig. 1 ). The neighbor-joining tree supported this clustering of the ALGJ 23 1 24 Algerian Jewish Jewish populations, with the previously described European/ ASHJ 14 20 34 Ashkenazi Jewish* Syrian and Middle Eastern branches being discernible (Fig. 2). DJEJ 0 17 17 Djerban Jewish The European Turkish, Greek, and Italian Jews shared a com- ETHJ 13 3 16 Ethiopian Jewish mon branch, with Ashkenazi and Syrian Jews forming con- GEOJ 4 9 13 Georgian Jewish nections to this branch. The North African populations added GRKJ 25 29 54 Greek Jewish* a subbranch to the European/Syrian branch, which in turn bi- – – – IRNJ 22 27 49 Iranian Jewish* furcated into Moroccan Algerian and Tunisian Djerban Libyan IRQJ 25 28 53 Iraqi Jewish* subbranches. As reported previously (16), the Middle Eastern ITAJ 20 19 39 Italian Jewish* Jewish branch included the Iranian and Iraqi Jews and the non- LIBJ 31 6 37 Libyan Jewish Jewish Adygei. This branch was observed now to include Geor- MORJ 32 6 38 Moroccan Jewish gian Jews. The Yemenite and Ethiopian Jews were on distinctive SYRJ 15 21 36 Syrian Jewish* branches with the Yemenite Jews on a branch between Pales- tinians and Bedouins. The robustness of this phylogenetic tree TUNJ 24 5 29 Tunisian Jewish was demonstrated by the fact that a majority of branches were TURJ 24 10 34 Turkish Jewish* supported by >90% of bootstrap replications. YMNJ 36 0 36 Yemini Jewish Pairwise FST analysis indicated that each of the North African ADYG 10 7 17 Adygei Jewish populations was distinct and, by bootstrap analysis, sta- ALGE 9 9 18 Algerian tistically different from all of the others [SI Appendix, Tables S1 BASQ 8 16 24 Basque (upper triangle) and S2]. Although FST may be sensitive to small BEDN 20 27 47 Bedouin sample sizes, these population differences were confirmed by DRUZ 32 13 45 Druze ANOVA on the principal component analysis (PCA) eigenvec- EGYP 0 19 19 Egyptian tors (P < 0.05; SI Appendix, Table S3), with the exception of FREN 17 12 29 French Algerian and Moroccan Jews, who were found to overlap. These LIBY 1 16 17 Libyan differences were also confirmed by permutation testing of be- MORN 0 18 18 North Moroccan tween-group IBS for all pairwise comparisons of the 15 Jewish MORS 5 5 10 South Moroccan populations (SI Appendix, Table S5).
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