Human Genetics

, Volume 114, Issue 4, pp 354–365 | Cite as

Contrasting patterns of Y chromosome variation in Ashkenazi Jewish and host non-Jewish European populations

  • Doron M. Behar
  • Daniel Garrigan
  • Matthew E. Kaplan
  • Zahra Mobasher
  • Dror Rosengarten
  • Tatiana M. Karafet
  • Lluis Quintana-Murci
  • Harry Ostrer
  • Karl Skorecki
  • Michael F. Hammer
Original Investigation


The molecular basis of more than 25 genetic diseases has been described in Ashkenazi Jewish populations. Most of these diseases are characterized by one or two major founder mutations that are present in the Ashkenazi population at elevated frequencies. One explanation for this preponderance of recessive diseases is accentuated genetic drift resulting from a series of dispersals to and within Europe, endogamy, and/or recent rapid population growth. However, a clear picture of the manner in which neutral genetic variation has been affected by such a demographic history has not yet emerged. We have examined a set of 32 binary markers (single nucleotide polymorphisms; SNPs) and 10 microsatellites on the non-recombining portion of the Y chromosome (NRY) to investigate the ways in which patterns of variation differ between Ashkenazi Jewish and their non-Jewish host populations in Europe. This set of SNPs defines a total of 20 NRY haplogroups in these populations, at least four of which are likely to have been part of the ancestral Ashkenazi gene pool in the Near East, and at least three of which may have introgressed to some degree into Ashkenazi populations after their dispersal to Europe. It is striking that whereas Ashkenazi populations are genetically more diverse at both the SNP and STR level compared with their European non-Jewish counterparts, they have greatly reduced within-haplogroup STR variability, especially in those founder haplogroups that migrated from the Near East. This contrasting pattern of diversity in Ashkenazi populations is evidence for a reduction in male effective population size, possibly resulting from a series of founder events and high rates of endogamy within Europe. This reduced effective population size may explain the high incidence of founder disease mutations despite overall high levels of NRY diversity.


Jewish Community Allele Size Jewish Population Discrimination Capacity Binary Marker 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Dr. Marc-Alain Levy for help in collecting samples from the French Rhine Valley and Dr. Istvan Mucsi for donating the Hungarian samples. This work was supported by a grant from the National Institute of General Medical Sciences (GM53566-06) to M.H., a F.I.R.S.T. award grant from the Israeli Science Foundation to K.S., and kind donations from the Milin Charitable Foundation and the Jerome Tankin Foundation.

Supplementary material

Supplementary Material 1+2 Y- Chromosome Haplogroup Frequencies in Ashkenazi Jews and Hungarians

supp.pdf (28 kb)
(PDF 28 KB)


  1. Behar DM, Thomas MG, Skorecki K, Hammer MF, Bulygina E, Rosengarten D, Jones AL, Held K, Moses V, Goldstein D, Bradman N, Weale ME (2003) Multiple origins of Ashkenazi Levites: Y chromosome evidence for both Near Eastern and European ancestries. Am J Hum Genet 73:768–779Google Scholar
  2. Behar DM, Hammer MF, Garrigan D, Villems R, Bonne-Tamir B, Richards M, Gurwitz D, Rosengarten D, Kaplan ME, DellaPergola S, Quintana-Murci L, Skorecki K (2004) mtDNA evidence for a genetic bottleneck in the early history of the Ashkenazi Jewish population. Eur J Hum Genet (in press)Google Scholar
  3. Bertorelle G, Excoffier L (1998) Inferring admixture proportions from molecular data. Mol Biol Evol 15:1298–1311PubMedGoogle Scholar
  4. Bonne-Tamir B, Adams A (1992) Genetic diversity among Jews. Oxford University Press, OxfordGoogle Scholar
  5. Bosch E, Calafell F, Santos FR, Perez-Lezaun A, Comas D, Benchemsi N, Tyler-Smith C, Bertranpetit J (1999) Variation in short tandem repeats is deeply structured by genetic background on the human Y chromosome. Am J Hum Genet 65:1623–1638PubMedGoogle Scholar
  6. Chakravarti A, Chakraborty R (1978) Elevated frequency of Tay-Sachs disease among Ashkenazic Jews unlikely by genetic drift alone. Am J Hum Genet 30:256–261PubMedGoogle Scholar
  7. Di Giacomo F, Luca F, Anagnou N, Ciavarella G, Corbo RM, Cresta M, Cucci F, Di Stasi L, Agostiano V, Giparaki M, Loutradis A, Mammi C, Michalodimitrakis EN, Papola F, Pedicini G, Plata E, Terrenato L, Tofanelli S, Malaspina P, Novelletto A (2003) Clinal patterns of human Y chromosomal diversity in continental Italy and Greece are dominated by drift and founder effects. Mol Phylogenet Evol 28:387–395CrossRefGoogle Scholar
  8. Diamond JM (1994) Human genetics. Jewish lysosomes. Nature 368:291–292CrossRefPubMedGoogle Scholar
  9. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  10. Goldstein DB, Reich DE, Bradman N, Usher S, Seligsohn U, Peretz H (1999) Age estimates of two common mutations causing factor XI deficiency: recent genetic drift is not necessary for elevated disease incidence among Ashkenazi Jews. Am J Hum Genet 64:1071–1075PubMedGoogle Scholar
  11. Goodman RM (1979a) Genetic disorders among the Jewish people. Johns Hopkins University Press, BaltimoreGoogle Scholar
  12. Goodman RM (1979b) A perspective on genetic diseases among the Jewish people. In: Goodman RM, Motulsky AG (eds) Genetic diseases among Ashkenazi Jews. Raven, New York, pp 1–17Google Scholar
  13. Gresham D, Morar B, Underhill PA, Passarino G, Lin AA, Wise C, Angelicheva D, Calafell F, Oefner PJ, Shen P, Tournev I, Pablo R de, Kucinskas V, Perez-Lezaun A, Marushiakova E, Popov V, Kalaydjieva L (2001) Origins and divergence of the Roma (gypsies). Am J Hum Genet 69:1314–1331CrossRefPubMedGoogle Scholar
  14. Hammer MF, Zegura SL (2002) The human Y chromosome haplogroup tree: nomenclature and phylogeography of its major divisions. Annu Rev Anthropol 31:303–321CrossRefGoogle Scholar
  15. Hammer MF, Spurdle AB, Karafet T, Bonner MR, Wood ET, Novelletto A, Malaspina P, Mitchell RJ, Horai S, Jenkins T, Zegura SL (1997) The geographic distribution of human Y chromosome variation. Genetics 145:787–805PubMedGoogle Scholar
  16. Hammer MF, Redd AJ, Wood ET, Bonner MR, Jarjanazi H, Karafet T, Santachiara-Benerecetti S, Oppenheim A, Jobling MA, Jenkins T, Ostrer H, Bonne-Tamir B (2000) Jewish and Middle Eastern non-Jewish populations share a common pool of Y-chromosome biallelic haplotypes. Proc Natl Acad Sci U S A 97:6769–6774CrossRefPubMedGoogle Scholar
  17. Hammer MF, Karafet TM, Redd AJ, Jarjanazi H, Santachiara-Benerecetti S, Soodyall H, Zegura SL (2001) Hierarchical patterns of global human Y-chromosome diversity. Mol Biol Evol 18:1189–1203PubMedGoogle Scholar
  18. Hedrick PW (2000) Genetics of populations. Jones and Bartlett, SudburyGoogle Scholar
  19. Jin L, Chakraborty R (1995) Population structure, stepwise mutations, heterozygote deficiency and their implications in DNA forensics. Heredity 74:274–285PubMedGoogle Scholar
  20. Jorde LB (1992) Population diseases in the Ashkenazi population: evolutionary considerations. In: Bonne-Tamir B, Adams A (eds) Genetic diversity among Jews. Oxford University Press, New York, pp 305–312Google Scholar
  21. Karafet TM, Osipova LP, Gubina MA, Posukh OL, Zegura SL, Hammer MF (2002) High levels of Y-chromosome differentiation among native Siberian populations and the genetic signature of a boreal hunter-gatherer way of life. Hum Biol 74:761–789PubMedGoogle Scholar
  22. Kruskal JB (1964) Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Pyschometrika 29:1-27Google Scholar
  23. Mitchell RJ, Hammer MF (1996) Human evolution and the Y chromosome. Curr Opin Genet Dev 6:737–742CrossRefPubMedGoogle Scholar
  24. Nebel A, Filon D, Brinkmann B, Majumder PP, Faerman M, Oppenheim A (2001) The Y chromosome pool of Jews as part of the genetic landscape of the Middle East. Am J Hum Genet 69:1095–1112Google Scholar
  25. Nei M (1987) Molecular evolutionaty genetics. Columbia University Press, New YorkGoogle Scholar
  26. Ostrer H (2001) A genetic profile of contemporary Jewish populations. Nat Rev Genet 2:891–898PubMedGoogle Scholar
  27. Redd AJ, Agellon AB, Kearney VA, Contreras VA, Karafet T, Park H, Knijff P de, Butler JM, Hammer MF (2002) Forensic value of 14 novel STRs on the human Y chromosome. Forensic Sci Int 130:97–111CrossRefPubMedGoogle Scholar
  28. Risch N, Leon D de, Ozelius L, Kramer P, Almasy L, Singer B, Fahn S, Breakefield X, Bressman S (1995) Genetic analysis of idiopathic torsion dystonia in Ashkenazi Jews and their recent descent from a small founder population. Nat Genet 9:152–159PubMedGoogle Scholar
  29. Risch N, Tang H, Katzenstein H, Ekstein J (2003) Geographic distribution of disease mutations in the Ashkenazi Jewish population supports genetic drift over selection. Am J Hum Genet 72:812–822CrossRefPubMedGoogle Scholar
  30. Rohlf FJ (1998) NTSYS-pc: numerical taxonomy and multivariant analysis system. Setauket, release 2.02H, NYGoogle Scholar
  31. Rolf B, Meyer E, Brinkmann B, Knijff P de (1998) Polymorphism at the tetranucleotide repeat locus DYS389 in 10 populations reveals strong geographic clustering. Eur J Hum Genet 6:583–588CrossRefPubMedGoogle Scholar
  32. Rosser ZH, Zerjal T, Hurles ME, Adojaan M, Alavantic D, Amorim A, Amos W, Armenteros M, Arroyo E, Barbujani G, Beckman G, Beckman L, Bertranpetit J, Bosch E, Bradley DG, Brede G, Cooper G, Corte-Real HB, Knijff P de, Decorte R, Dubrova YE, Evgrafov O, Gilissen A, Glisic S, Golge M, Hill EW, Jeziorowska A, Kalaydjieva L, Kayser M, Kivisild T, Kravchenko SA, Krumina A, Kucinskas V, Lavinha J, Livshits LA, Malaspina P, Maria S, McElreavey K, Meitinger TA, Mikelsaar AV, Mitchell RJ, Nafa K, Nicholson J, Norby S, Pandya A, Parik J, Patsalis PC, Pereira L, Peterlin B, Pielberg G, Prata MJ, Previdere C, Roewer L, Rootsi S, Rubinsztein DC, Saillard J, Santos FR, Stefanescu G, Sykes BC, Tolun A, Villems R, Tyler-Smith C, Jobling MA (2000) Y-chromosomal diversity in Europe is clinal and influenced primarily by geography, rather than by language. Am J Hum Genet 67:1526–1543PubMedGoogle Scholar
  33. Schneider S, Roessli D, Excoffier L (2002) Arlequin: a software for population genetic analysis. Release 1.1, GenevaGoogle Scholar
  34. Semino O, Passarino G, Oefner PJ, Lin AA, Arbuzova S, Beckman LE, De Benedictis G, Francalacci P, Kouvatsi A, Limborska S, Marcikiae M, Mika A, Mika B, Primorac D, Santachiara-Benerecetti AS, Cavalli-Sforza LL, Underhill PA (2000) The genetic legacy of Paleolithic Homo sapiens sapiens in extant Europeans: a Y chromosome perspective. Science 290:1155–1159PubMedGoogle Scholar
  35. Shriver MD (1997) Ethnic variation as a key to the biology of human disease. Ann Intern Med 127:401–403PubMedGoogle Scholar
  36. Skorecki K, Selig S, Blazer S, Bradman R, Bradman N, Waburton PJ, Ismajlowicz M, Hammer MF (1997) Y chromosomes of Jewish priests. Nature 385:32PubMedGoogle Scholar
  37. Thomas MG, Skorecki K, Ben-Ami H, Parfitt T, Bradman N, Goldstein DB (1998) Origins of Old Testament priests. Nature 394:138–140PubMedGoogle Scholar
  38. Thomas MG, Weale ME, Jones AL, Richards M, Smith A, Redhead N, Torroni A, Scozzari R, Gratrix F, Tarekegn A, Wilson JF, Capelli C, Bradman N, Goldstein DB (2002) Founding mothers of Jewish communities: geographically separated Jewish groups were independently founded by very few female ancestors. Am J Hum Genet 70:1411–1420CrossRefPubMedGoogle Scholar
  39. Underhill PA, Passarino G, Lin AA, Shen P, Mirazon Lahr M, Foley RA, Oefner PJ, Cavalli-Sforza LL (2001) The phylogeography of Y chromosome binary haplotypes and the origins of modern human populations. Ann Hum Genet 65:43–62Google Scholar
  40. Weinryb BD (1972) The Jews of Poland: a social and economic history of the Jewish community in Poland from 1100 to 1800. Jewish Publication Society of America, PhiladelphiaGoogle Scholar
  41. Wilson JF, Weiss DA, Richards M, Thomas MG, Bradman N, Goldstein DB (2001) Genetic evidence for different male and female roles during cultural transitions in the British Isles. Proc Natl Acad Sci USA 98:5078–5083CrossRefPubMedGoogle Scholar
  42. YCC (2002) A nomenclature system for the tree of human Y-chromosomal binary haplogroups. Genome Res 12:339–348PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Doron M. Behar
    • 1
  • Daniel Garrigan
    • 2
  • Matthew E. Kaplan
    • 2
  • Zahra Mobasher
    • 2
  • Dror Rosengarten
    • 1
  • Tatiana M. Karafet
    • 2
  • Lluis Quintana-Murci
    • 3
  • Harry Ostrer
    • 4
  • Karl Skorecki
    • 1
    • 5
  • Michael F. Hammer
    • 2
  1. 1.Bruce Rappaport Faculty of Medicine and Research InstituteTechnion and Rambam Medical CenterHaifaIsrael
  2. 2.Division of BiotechnologyUniversity of ArizonaTucsonUSA
  3. 3.CNRS URA1961Institut PasteurParisFrance
  4. 4.Human Genetics ProgramNew York University School of MedicineNew YorkUSA
  5. 5.Department of Nephrology and Molecular MedicineTechnion and Rambam Medical CenterHaifaIsrael

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