High-resolution Y chromosome haplotypes of Israeli and Palestinian Arabs reveal geographic substructure and substantial overlap with haplotypes of Jews

Abstract

High-resolution Y chromosome haplotype analysis was performed in 143 paternally unrelated Israeli and Palestinian Moslem Arabs (I&P Arabs) by screening for 11 binary polymorphisms and six microsatellite loci. Two frequent haplotypes were found among the 83 detected: the modal haplotype of the I&P Arabs (∼14%) was spread throughout the region, while its one-step microsatellite neighbor, the modal haplotype of the Galilee sample (∼8%), was mainly restricted to the north. Geographic substructuring within the Arabs was observed in the highlands of Samaria and Judea. Y chromosome variation in the I&P Arabs was compared to that of Ashkenazi and Sephardic Jews, and to that of North Welsh individuals. At the haplogroup level, defined by the binary polymorphisms only, the Y chromosome distribution in Arabs and Jews was similar but not identical. At the haplotype level, determined by both binary and microsatellite markers, a more detailed pattern was observed. Single-step microsatellite networks of Arab and Jewish haplotypes revealed a common pool for a large portion of Y chromosomes, suggesting a relatively recent common ancestry. The two modal haplotypes in the I&P Arabs were closely related to the most frequent haplotype of Jews (the Cohen modal haplotype). However, the I&P Arab clade that includes the two Arab modal haplotypes (and makes up 32% of Arab chromosomes) is found at only very low frequency among Jews, reflecting divergence and/or admixture from other populations.

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References

  1. Anderson J (1995) The impact of Rome on the periphery: the case of Palestina —Roman Period (63 BCE-324 CE). In: Levy T (ed) The archaeology of society in the Holy Land. Leicester University Press, London, pp 446–468

    Google Scholar 

  2. Arensburg B (1973) The people in the land of Israel from the Epipaleolithic to present times. Doctoral Dissertation, University of Tel Aviv, Tel Aviv

    Google Scholar 

  3. Bachi R (1974) The population of Israel. The Hebrew University, Jerusalem

    Google Scholar 

  4. Bar-Yosef O (1995) Earliest food producers —pre-pottery Neolithic. In: Levy T (ed) The archaeology of society in the Holy Land. Leicester University Press, London, pp 190–204

    Google Scholar 

  5. Bianchi NO, Catanesi CI, Bailliet G, Martinez-Marignac VL, Bravi CM, Vidal-Rioja LB, Herrera R, et al (1998) Characterization of ancestral and derived Y-chromosomal haplotypes of New World populations. Am J Hum Genet 63: 1862–1871

    PubMed  Article  CAS  Google Scholar 

  6. Bishara A, Brautbar C, Nagler A (1997) HLA and graft-versushost disease: a population-based study of HLA phenotypes of Jewish and Arab bone marrow transplanted patients in Israel. Leuk Res 21: 111–118

    PubMed  Article  CAS  Google Scholar 

  7. Bonné-Tamir B, Asbel S, Kennet R (1979) Genetic markers: benign and normal traits of Ashkenazi Jews. In: Goodman R, Motulsky A (eds) Genetic diseases among Ashkenazi Jews. Raven Press, New York, pp 54–76

    Google Scholar 

  8. Bonné-Tamir B, Johnson M, Natali A, Wallace D, Cavalli-Sforza L (1986) Human mitochondrial DNA types in two Israeli populations —a comparative study at the DNA level. Am J Hum Genet 38: 341–351

    PubMed  Google Scholar 

  9. Bosch E, Calafell F, Santos F, Pérez-Lezaun A, Comas D, Benchemsi N, Tyler-Smith C, et al (1999) Variation in short tandem repeats is deeply structured by genetic background on the Y chromosome. Am J Hum Genet 65: 1623–1638

    PubMed  Article  CAS  Google Scholar 

  10. Cooper G, Amos W, Hoffman D, Rubinsztein D (1996) Network analysis of human Y microsatellite haplotypes. Hum Mol Genet 11: 1759–1766

    Article  Google Scholar 

  11. Darke C, Guttridge M, Thompson J, McNamara S, Street J, Thomas M (1998) HLA class I and II gene and haplotype frequencies in blood donors from Wales. Exp Clin Immunogenet 15: 69–83

    PubMed  Article  CAS  Google Scholar 

  12. Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479–491

    PubMed  CAS  Google Scholar 

  13. Felsenstein J (1995) PHYLIP (phylogeny inference package), version 3.5c. University of Washington, Seattle, USA

    Google Scholar 

  14. Filon D, Oron V, Krichevski S, Shaag A, Shaag Y, Warren T, Goldfarb A, et al (1994) Diversity of β-globin mutations in Israeli ethnic groups reflect recent historic events. Am J Hum Genet 54: 836–843

    PubMed  CAS  Google Scholar 

  15. Gil M (1992) A history of Palestine. Cambridge University Press, Cambridge, pp 643–1099

    Google Scholar 

  16. Goldstein D, Ruiz-Linares A, Cavalli-Sforza L, Feldman M (1995) An evaluation of genetic distances for use with microsatellite loci. Genetics 139: 463–471

    PubMed  CAS  Google Scholar 

  17. Hammer MF (1994) A recent insertion of an Alu element on the Y chromosome is a useful marker for human population studies. Mol Biol Evol 11: 749–761

    PubMed  CAS  Google Scholar 

  18. Hammer M, Zegura S (1997) The role of the Y chromosome in human evolutionary studies. Evol Anthropol 4: 116–134

    Google Scholar 

  19. Hammer M, Spurdle A, Karafet T, Bonner M, Wood E, Novelletto A, Malaspina P, et al (1997) The geographic distribution of human Y chromosome variation. Genetics 145: 787–805

    PubMed  CAS  Google Scholar 

  20. Hammer M, Karafet T, Rasanayagam A, Wood E, Altheide T, Jenkins T, Griffiths R, et al (1998) Out of Africa and back again: nested cladistic analysis of human Y chromosome variation. Mol Biol Evol 15: 427–441

    PubMed  CAS  Google Scholar 

  21. Hammer M, Redd A, Wood E, Bonner M, Jarjanazi H, Karafet T, Santachiara-Benerecetti A, et al (2000) Jewish and Middle Eastern non-Jewish populations share a common pool of Ychromosome biallelic haplotypes. Proc Natl Acad Sci USA 97: 6769–6774

    PubMed  Article  CAS  Google Scholar 

  22. Heyer E, Puymirat J, Dieltjes P, Bakker E, Knijff P de (1997) Estimating Y chromosome specific microsatellite mutation frequencies using deep rooting pedigrees. Hum Mol Genet 6: 799–803

    PubMed  Article  CAS  Google Scholar 

  23. Hurles M, Irven C, Nicholson J, Taylor P, Santos F, Loughlin J, Jobling M, et al (1998) European Y chromosomal lineages in Polynesians: a contrast to the population structure revealed by mtDNA. Am J Hum Genet 63: 1793–1806

    PubMed  Article  CAS  Google Scholar 

  24. Jobling M, Tyler-Smith C (1995) Fathers and sons: the Y chromosome and human evolution. Trends Genet 11: 449–456

    PubMed  Article  CAS  Google Scholar 

  25. Karafet T, Zegura S, Vuturo-Brady J, Posukh O, Osipova L, Wiebe V, Romero F, et al (1997) Y chromosome markers and trans-Bering Strait dispersals. Am J Phys Anthropol 102: 301–314

    PubMed  Article  CAS  Google Scholar 

  26. Kayser M, Caglià A, Corach D, Fretwell N, Gehrig C, Graziosi G, Heidorn F, et al (1997) Evaluation of Y-chromosomal STRs: a multicenter study. Int J Legal Med 110: 125–133

    PubMed  Article  CAS  Google Scholar 

  27. Kayser M, Roewer L, Hedman M, Henke L, Henke J, Brauer S, Krüger C, et al (2000) Characteristics and frequency of germline mutations at microsatellite loci from the human Y chromosome, as revealed by direct observation in father/son pairs. Am J Hum Genet 66: 1580–1588

    PubMed  Article  CAS  Google Scholar 

  28. Kittles R, Perola M, Peltonen L, Bergen A, Aragon R, Virkkunen M, Linnoila M, Goldman D, Long J (1998) Dual origins of Finns revealed by Y chromosome haplotype variation. Am J Hum Genet 62: 1171–1179

    PubMed  Article  CAS  Google Scholar 

  29. Kittles R, Bergen A, Urbanek M, Virkkunen M, Linnoila M, Goldman D, Long J (1999) Autosomal, mitochondrial and Y chromosome DNA variation in Finland: evidence for a male-specific bottleneck. Am J Phys Anthropol 108: 381–399

    PubMed  Article  CAS  Google Scholar 

  30. Knijff P de, Kayser M, Caglià A, Corach D, Fretwell N, Gehrig C, Graziosi G, et al (1997) Chromosome Y microsatellites: population genetic and evolutionary aspects. Int J Legal Med 110: 134–140

    PubMed  Article  Google Scholar 

  31. Mathias N, Bayés M, Tyler-Smith C (1994) Highly informative compound haplotypes for the human Y chromosome. Hum Mol Genet 3: 115–123

    PubMed  Article  CAS  Google Scholar 

  32. Mc Graw Donner F (1981) The early Islamic conquests. Princeton University Press, Princeton

    Google Scholar 

  33. Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142: 1061–1064

    PubMed  CAS  Google Scholar 

  34. Minch E (1997) Microsat, the microsatellite distance program, version 1.5d. Stanford University, USA

    Google Scholar 

  35. Mitchell R, Earl L, Fricke B (1997) Y-chromosome specific alleles and haplotypes in European and Asian populations: linkage disequilibrium and geographic diversity. Am J Phys Anthropol 104: 167–176

    PubMed  Article  CAS  Google Scholar 

  36. Moran PAP (1975) Wandering distributions and the electrophoretic profile. Theor Popul Biol 8: 318–330

    PubMed  Article  CAS  Google Scholar 

  37. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  38. Peretz H, Mulai A, Usher S, Zivelin A, Segal A, Weisman Z, Mittelman M, et al (1997) The two common mutations causing factor XI deficiency in Jews stem from distinct founders: one of ancient Middle Eastern origin and another of more recent European origin. Blood 7: 2654–2659

    Google Scholar 

  39. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49: 1280–1283

    Article  Google Scholar 

  40. Ritte U, Neufeld E, Prager E, Gross M, Hakim I, Khatib A, Bonne-Tamir B (1993) Mitochondrial DNA affinity of several Jewish communities. Hum Biol 65: 359–385

    PubMed  CAS  Google Scholar 

  41. Roewer L, Kayser M, Dieltjes P, Nagy M, Bakker E, Krawczak M, Knijff P de (1996) Analysis of molecular variance (AMOVA) of Y-chromosome-specific microsatellites in two closely related human populations. Hum Mol Genet 5: 1029–1033

    PubMed  Article  CAS  Google Scholar 

  42. Rund D, Kornhendler N, Shalev O, Oppenheim A (1990) The origin of sickle cell alleles in Israel. Hum Genet 85: 521–524

    PubMed  Article  CAS  Google Scholar 

  43. Sandler S, Kravitz C, Sharon R, Hermani D, Ezekiel E, Cohen T (1979) The Duffy blood group system in Israel: Jews and Arabs. Vox Sang 37: 41–46

    PubMed  Article  CAS  Google Scholar 

  44. Santachiara-Benerecetti A, Semino O, Passarino G, Torroni A, Brdicka R, Fellous M, Modiano G (1993) The common Near Eastern origin of Ashkenazi and Sephardi Jews supported by Y-chromosome similarity. Ann Hum Genet 57: 55–64

    PubMed  Article  CAS  Google Scholar 

  45. Schneider S, Kueffer J-M, Roessli D, Excoffier L (1997) Arlequin ver. 1.1: a software for population genetic data analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland

    Google Scholar 

  46. Seielstad MT, Herbert JM, Lin AA, Underhill PA, Ibrahim M, Vollrath D, Cavalli-Sforza LL (1994) Construction of human Y-chromosomal haplotypes using a new polymorphic A to G transition. Hum Mol Genet 3: 2159–2161

    PubMed  Article  CAS  Google Scholar 

  47. Sellers J, Thompson J, Guttridge MG, Darke C (1999) Human platelet antigens: typing by PCR using sequence-specific primers and their distribution in blood donors resident in Wales. Eur J Immunogenet 26: 393–397

    PubMed  Article  CAS  Google Scholar 

  48. Shaban MA (1971) Islamic history AD 600–750: a new interpretation. Cambridge University Press, Cambridge.

    Google Scholar 

  49. Skorecki K, Selig S, Blazer S, Bradman R, Bradman N, Warburton P, Ismajlowicz M, et al (1997) Y chromosomes of Jewish priests. Nature 385: 32

    PubMed  Article  CAS  Google Scholar 

  50. Thomas M, Skorecki K, Ben-Ami H, Parfitt T, Bradman N, Goldstein D (1998) Origins of Old Testament priests. Nature 394: 138–140

    PubMed  Article  CAS  Google Scholar 

  51. Thomas M, Bradman N, Flinn H (1999) High throughput analysis of 10 microsatellite and 11 diallelic polymorphisms on the human Y chromosome. Hum Genet 105: 577–581

    PubMed  Article  CAS  Google Scholar 

  52. Thomas M, Parfitt T, Weiss D, Skorecki K, Wilson J, Roux M le, Bradman N, Goldstein D (2000) Y chromosomes travelling south: the Cohen modal haplotype and the origins of the Lemba —the “black Jews of Southern Africa”. Am J Hum Genet 66: 674–686

    PubMed  Article  CAS  Google Scholar 

  53. Underhill P, Jin L, Lin A, Mehdi S, Jenkins T, Vollrath D, Davis R, et al (1997) Detection of numerous Y chromosome biallelic polymorphisms by denaturing high-performance liquid chromatography. Genome Res 7: 996–1005

    PubMed  CAS  Google Scholar 

  54. Whitfield LS, Sulston JE, Goodfellow PN (1995) Sequence variation of the human Y chromosome. Nature 378: 379–380

    PubMed  Article  CAS  Google Scholar 

  55. Wilson IJ, Balding DJ (1998) Genealogical inference from microsatellite data. Genetics 150: 499–510

    PubMed  CAS  Google Scholar 

  56. Zerjal T, Dashnyam B, Pandya A, Kayser M, Roewer L, Santos FR, Schiefenhövel W, et al (1997) Genetic relationships of Asians and northern Europeans, revealed by Y-chromosomal DNA analysis. Am J Hum Genet 60: 1174–1183

    PubMed  CAS  Google Scholar 

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Correspondence to Ariella Oppenheim.

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Nebel, A., Filon, D., Weiss, D.A. et al. High-resolution Y chromosome haplotypes of Israeli and Palestinian Arabs reveal geographic substructure and substantial overlap with haplotypes of Jews. Hum Genet 107, 630–641 (2000). https://doi.org/10.1007/s004390000426

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Keywords

  • Thalassemia
  • Jewish Community
  • Neighbor Join
  • Haplo
  • Arab Population