A Substantial Prehistoric European Ancestry Amongst Ashkenazi Maternal Lineages
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ARTICLE Received 11 Jul 2013 | Accepted 4 Sep 2013 | Published 8 Oct 2013 DOI: 10.1038/ncomms3543 OPEN A substantial prehistoric European ancestry amongst Ashkenazi maternal lineages Marta D. Costa1,2,*, Joana B. Pereira1,2,*, Maria Pala3, Vero´nica Fernandes1,2, Anna Olivieri4, Alessandro Achilli5, Ugo A. Perego4,6, Sergei Rychkov7, Oksana Naumova7, Jirˇi Hatina8, Scott R. Woodward6,9, Ken Khong Eng1,10, Vincent Macaulay11, Martin Carr3, Pedro Soares2, Luı´sa Pereira2,12 & Martin B. Richards1,3 The origins of Ashkenazi Jews remain highly controversial. Like Judaism, mitochondrial DNA is passed along the maternal line. Its variation in the Ashkenazim is highly distinctive, with four major and numerous minor founders. However, due to their rarity in the general population, these founders have been difficult to trace to a source. Here we show that all four major founders, B40% of Ashkenazi mtDNA variation, have ancestry in prehistoric Europe, rather than the Near East or Caucasus. Furthermore, most of the remaining minor founders share a similar deep European ancestry. Thus the great majority of Ashkenazi maternal lineages were not brought from the Levant, as commonly supposed, nor recruited in the Caucasus, as sometimes suggested, but assimilated within Europe. These results point to a significant role for the conversion of women in the formation of Ashkenazi communities, and provide the foundation for a detailed reconstruction of Ashkenazi genealogical history. 1 Institute of Integrative and Comparative Biology, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, UK. 2 IPATIMUP (Instituto de Patologia e Imunologia Molecular da Universidade do Porto), Porto 4200-465, Portugal. 3 School of Applied Sciences, University of Huddersfield, Queensgate, Huddersfield HD1 3DH, UK. 4 Dipartimento di Biologia e Biotecnologie, Universita` di Pavia, Pavia 27100, Italy. 5 Dipartimento di Chimica, Biologia e Biotecnologie, Universita` di Perugia, Perugia 06123, Italy. 6 Sorenson Molecular Genealogy Foundation, Salt Lake City, Utah 84115, USA. 7 Vavilov Institute of General Genetics, Moscow 119991, Russia. 8 Charles University, Medical Faculty in Pilsen, Institute of Biology, CZ-301 66 Pilsen, Czech Republic. 9 Ancestry, Provo, Utah 84604, USA. 10 Centre for Global Archaeological Research, Universiti Sains Malaysia, 11800 USM Penang, Malaysia. 11 School of Mathematics and Statistics, University of Glasgow, Glasgow G12 8QQ, UK. 12 Faculdade de Medicina da Universidade do Porto, Porto 4200-319, Portugal. * These authors contributed equally to this work. Correspondence and requests for materials should be addressed to M.B.R. (email: [email protected]). NATURE COMMUNICATIONS | 4:2543 | DOI: 10.1038/ncomms3543 | www.nature.com/naturecommunications 1 & 2013 Macmillan Publishers Limited. All rights reserved. ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms3543 he origins of Ashkenazi Jews—the great majority of Using this approach, Behar et al.2 identified four major founder living Jews—remain highly contested and enigmatic to clusters, three within haplogroup K—amounting to 32% of Tthis day1–11. The Ashkenazim are Jews with a recent sampled Ashkenazi lineages—and one within haplogroup N1b, ancestry in central and Eastern Europe, in contrast to Sephardim amounting to another 9%. These lineages are extremely (with an ancestry in Iberia, followed by exile after 1492), infrequent across the Near East and Europe, making the Mizrahim (who have always resided in the Near East) and identification of potential source populations very challenging. North African Jews (comprising both Sephardim and Mizrahim). Nevertheless, they concluded that all four most likely arose in the There is consensus that all Jewish Diaspora groups, including Near East and were markers of a migration to Europe of people the Ashkenazim, trace their ancestry, at least in part, to the ancestral to the Ashkenazim only B2,000 years ago1,2. The Levant, B2,000–3,000 years ago5,12–14. There were Diaspora remaining B60% of mtDNA lineages in the Ashkenazim communities throughout Mediterranean Europe and the Near remained unassigned to any source, with the exception of the East for several centuries prior to the destruction of the Second minor haplogroup U5 and V lineages (B6% in total), which Temple in Jerusalem in 70 CE (Common Era), and some scholars implied European ancestry1,23. suggest that their scale implies proselytism and wide-scale Here we focus on both major and minor founders, with a much conversion, although this view is very controversial9,15. larger database from potential source populations. We first The Ashkenazim are thought to have emerged from dispersals analyse 956 (72 newly generated) mitogenomes from haplogroup north into the Rhineland of Mediterranean Jews in the early U8 (including 909 from haplogroup K, U8’s major subclade): 477 Middle Ages, although there is little evidence before the twelfth of these are from Europe and 106 from the Near East/Caucasus. century5,15. After expulsions from Western Europe between the We show that European and Near Eastern lineages largely fall thirteenth and fifteenth centuries, the communities are thought to into discrete, ancient clusters, with minor episodes of gene flow, have expanded eastwards, especially in Poland, Lithuania and suggesting that haplogroup K diversified separately in Europe then Russia. The implied scale of this expansion has led some to and the Near East during the last glacial period. Of the three argue, again very controversially, for mass conversions in the Ashkenazi founders, K1a1b1a and K1a9 were most likely Khazar kingdom, in the North Caucasus region to the north and assimilated in west (perhaps Mediterranean) Europe and east of the Black Sea, following the Khazar leadership’s adoption K2a2a1 in west/central Europe. Most surprisingly, by analysing of Judaism between the ninth and tenth centuries CE8,9. two new N1b2 sequences selected from a database of 278 N1b We are then faced with several competing models for HVS-I sequences, in the context of 44 published N1b sequences24, Ashkenazi origins: a Levantine ancestry; a Mediterranean/west we show that the highly distinctive N1b2 subclade, making up European ancestry; a North Caucasian ancestry; or, of course, a another 9% of Ashkenazi lineages, was likely assimilated in blend of these. This seems an ideal problem to tackle with genetic Mediterranean Europe, rather than in the Near East as previously analysis, but after decades of intensive study a definitive answer proposed2. Moreover, from a survey of another 42,500 complete remains elusive. Although we might imagine that such an mtDNA genomes and 428,000 control-region sequences from apparently straightforward admixture question might be readily Europe, the Near East and the Caucasus, in comparison with the addressed using genome-wide autosomal markers, recent studies available database of 836 Ashkenazi control-region sequences and have proposed contradictory conclusions. Several suggest a a handful of published mitogenomes, we also evaluate the minor primarily Levantine ancestry with south/west European admix- founders. Overall, we estimate that most (480%) Ashkenazi ture3,4, but another concludes that the ancestry is largely mtDNAs were assimilated within Europe. Few derive from a Near Caucasian16, implying a major source from converts in the Eastern source, and despite the recent revival of the ‘Khazar Khazar kingdom17. An important reason for disagreement is that hypothesis’16, virtually none are likely to have ancestry in the the Ashkenazim have undergone severe founder effects during North Caucasus. Therefore, whereas on the male side there may their history, drastically altering the frequencies of genetic have been a significant Near Eastern (and possibly east European/ markers and distorting the relationship with their ancestral Caucasian) component in Ashkenazi ancestry, the maternal populations. lineages mainly trace back to prehistoric Western Europe. These This problem can be resolved by reconstructing the relation- results emphasize the importance of recruitment of local women ships genealogically, rather than relying on allele frequencies, and conversion in the formation of Ashkenazi communities, and using the non-recombining marker systems: the paternally represent a significant step in the detailed reconstruction of inherited male-specific part of the Y chromosome (MSY) and Ashkenazi genealogical history. the maternally inherited mitochondrial DNA (mtDNA). This kind of analysis can be very powerful, because nesting of particular lineages within clusters from a particular geographical Results region allows us to pinpoint the source for those lineages, by Four major founder lineages within haplogroup K and N1b. applying the parsimony principle. This has indeed been Haplogroup K arose within haplogroup U8B36 ka, in Europe or attempted, with the MSY results interpreted plausibly to suggest the Near East, with the minor subclades K1b, K1c and K2 all most an overwhelming majority of Near Eastern ancestry on the likely arising in Europe, between the last glacial period and the Ashkenazi male line of descent11,18–21, albeit with much higher Neolithic (Fig. 1; Supplementary Note 1; Supplementary Data 1–3; levels (450%) of European (potentially east European) lineages Supplementary Figs S1–S3; Supplementary Tables S1–S3). K1a in Ashkenazi Levites22, suggesting a possible Khazar source in expanded from B20 ka onwards, both in the Near East and that particular case. Europe, with its major