Human Genetics

, Volume 114, Issue 2, pp 127–148 | Cite as

Excavating Y-chromosome haplotype strata in Anatolia

  • Cengiz Cinnioğlu
  • Roy King
  • Toomas Kivisild
  • Ersi Kalfoğlu
  • Sevil Atasoy
  • Gianpiero L. Cavalleri
  • Anita S. Lillie
  • Charles C. Roseman
  • Alice A. Lin
  • Kristina Prince
  • Peter J. Oefner
  • Peidong Shen
  • Ornella Semino
  • L. Luca Cavalli-Sforza
  • Peter A. Underhill
Original Investigation

Abstract

Analysis of 89 biallelic polymorphisms in 523 Turkish Y chromosomes revealed 52 distinct haplotypes with considerable haplogroup substructure, as exemplified by their respective levels of accumulated diversity at ten short tandem repeat (STR) loci. The major components (haplogroups E3b, G, J, I, L, N, K2, and R1; 94.1%) are shared with European and neighboring Near Eastern populations and contrast with only a minor share of haplogroups related to Central Asian (C, Q and O; 3.4%), Indian (H, R2; 1.5%) and African (A, E3*, E3a; 1%) affinity. The expansion times for 20 haplogroup assemblages was estimated from associated STR diversity. This comprehensive characterization of Y-chromosome heritage addresses many multifaceted aspects of Anatolian prehistory, including: (1) the most frequent haplogroup, J, splits into two sub-clades, one of which (J2) shows decreasing variances with increasing latitude, compatible with a northward expansion; (2) haplogroups G1 and L show affinities with south Caucasus populations in their geographic distribution as well as STR motifs; (3) frequency of haplogroup I, which originated in Europe, declines with increasing longitude, indicating gene flow arriving from Europe; (4) conversely, haplogroup G2 radiates towards Europe; (5) haplogroup E3b3 displays a latitudinal correlation with decreasing frequency northward; (6) haplogroup R1b3 emanates from Turkey towards Southeast Europe and Caucasia and; (7) high resolution SNP analysis provides evidence of a detectable yet weak signal (<9%) of recent paternal gene flow from Central Asia. The variety of Turkish haplotypes is witness to Turkey being both an important source and recipient of gene flow.

References

  1. Al-Zahery N, Semino O, Benuzzi G, Magri C, Passarino G, Torroni A, Santachiara-Benerecetti AS (2003) Y-chromosome and mtDNA polymorphisms in Iraq, a crossroad of the early human dispersal and of post-Neolithic migrations. Mol Phylogenet Evol 28:458–472CrossRefPubMedGoogle Scholar
  2. Ammerman AJ, Cavalli-Sforza LL (1984) The Neolithic Transition and the Genetics of Populations in Europe. Princeton University Press, Princeton, N.J.Google Scholar
  3. Ayub Q, Mohyuddin A, Qamar R, Mazhar K, Zerjal T, Mehdi SQ, Tyler-Smith C (2000) Identification and characterisation of novel human Y-chromosomal microsatellites from sequence database information. Nucleic Acids Res 28:8CrossRefPubMedGoogle Scholar
  4. Barac L, Pericic M, Klaric IM, Rootsi S, Janicijevi B, Kivisild T, Parik J, Rudan I, et al. (2003) Y chromosomal heritage of Croatian population and its island isolates. Eur J Hum Genet 11:535–542CrossRefPubMedGoogle Scholar
  5. Bar-Yosef O (1998) The Natufian culture in the Levant, threshold to the origins of agriculture. Evol Anthropol6:159–177Google Scholar
  6. Blanco P, Shlumukova M, Sargent CA, Jobling MA, Affara N, Hurles ME (2000) Divergent outcomes of intrachromosomal recombination on the human Y chromosome: male infertility and recurrent polymorphism. J Med Genet 37:752–758CrossRefPubMedGoogle Scholar
  7. Cavalli-Sforza LL, Menozzi P, Piazza A (1994) The history and geography of human genes. Princeton University Press, PrincetonGoogle Scholar
  8. Cooper G, Amos W, Hoffman D, Rubinsztein DC (1996) Network analysis of human Y microsatellite haplotypes. Hum Mol Genet 5:1759–1766CrossRefPubMedGoogle Scholar
  9. Cruciani F, Santolamazza P, Shen P, Macaulay V, Moral P, Olckers A, Modiano D, Destro-Bisol G, et al. (2002) An Asia to Sub-Saharan Africa back migration is supported by high-resolution analysis of human Y chromosome haplotypes. Am J Hum Genet 70:1197–1214Google Scholar
  10. de Knijff P (2000) Messages through bottlenecks: on the combined use of slow and fast evolving polymorphic markers on the human Y chromosome. Am J Hum Genet 67:1055–1061PubMedGoogle Scholar
  11. Di Benedetto G, Erguven A, Stenico M, Castri L, Bertorelle G, Togan I, Barbujani G (2001) DNA diversity and population admixture in Anatolia. Am J Phys Anthropol 115:144–156CrossRefPubMedGoogle Scholar
  12. Di Giacomo F, Luca F, Anagnou N, Ciavarella G, Corbo RM, Cresta M, Cucci F, Di Stasi L, et al. (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
  13. Di Rienzo A, Peterson A, Garza J, Valdes A, Slatkin M, Freimer N (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170PubMedGoogle Scholar
  14. Hammer MF, Redd AJ, Wood ET, Bonner MR, Jarjanazi H, Karafet T, Santachiara-Benerecetti S, Oppenheim A, et al. (2000) Jewish and middle eastern non-Jewish populations share a common pool of Y-chromosome biallelic haplotypes. Proc Natl Acad Sci USA 97:6769–6774PubMedGoogle Scholar
  15. 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
  16. Jobling MA, Tyler-Smith C (2003) The human Y chromosome: an evolutionary marker comes of age. Nat Reviews Genet 4:598–612CrossRefGoogle Scholar
  17. Karafet T, Xu L, Du R, Wang W, Feng S, Wells RS, Redd AJ, Zegura SL, et al. (2001) Paternal population history of East Asia: sources, patterns, and microevolutionary processes. Am J Hum Genet 69:615–628CrossRefPubMedGoogle Scholar
  18. Kayser M, Caglia A, Corach D, Fretwell N, Gehrig C, Graziosi G, Heidorn F, Herrmann S, et al (1997) Evaluation of Y-chromosomal STRs: a multicenter study. Int J Legal Med 110:125–133PubMedGoogle Scholar
  19. Khazanov AM (1984) Nomads and the outside world. Cambridge, Cambridge University PressGoogle Scholar
  20. King R, Underhill PA (2002) Congruent distribution of Neolithic painted pottery and ceramic figurines with Y-chromosome lineages. Antiquity 76:707–714Google Scholar
  21. Kittles RA, Perola M, Peltonen L, Bergen AW, Aragon RA, Virkkunen M, Linnoila M, Goldman D, et al. (1998) Dual origins of Finns revealed by Y chromosome haplotype variation. Am J Hum Genet 62:1171–1179PubMedGoogle Scholar
  22. Kivisild T, Rootsi S, Metspalu M, Mastana S, Kaldma K, Parik J, Metspalu E, Adojaan M, et al. (2003) The genetic heritage of earliest settlers persist in both the Indian tribal and caste populations. Am J Hum Genet 72:313–332CrossRefPubMedGoogle Scholar
  23. Knight A, Underhill PA, Zhivotovsky LA, Mortensen HM, Ruhlen M, Mountain JL (2003) African Y chromosome and mtDNA diversity and the antiquity of click languages. Curr Biol 13:464–473CrossRefPubMedGoogle Scholar
  24. Korfmann M (1996) Troia — Ausgrabungen 1995. Studia Troica 6:1–64Google Scholar
  25. Kuhn SL (2002) Paleolithic archeology in Turkey. Evol Anthropol 11:198–210CrossRefGoogle Scholar
  26. Malaspina P, Tsopanomichalou M, Duman T, Stefan M, Silvestri A, Rinaldi B, Garcia O, Giparaki M, et al. (2001) A multistep process for the dispersal of a Y chromosomal lineage in the Mediterranean area. Ann Hum Genet 65:339–349Google Scholar
  27. Manni F, Leonardi P, Barakat A, Rouba H, Heyer E, Klintschar M, McElreavey K, Quintana-Murci L (2002) Y-chromosome analysis in Egypt suggests a genetic regional continuity in northeastern Africa. Hum Biol 74:645–658PubMedGoogle Scholar
  28. Nasidze I, Sarkisian T, Kerimov A, Stoneking (2003) Testing hypotheses of language replacement in the Caucasus: evidence from the Y-chromosome. Hum Genet 112:255–261PubMedGoogle Scholar
  29. Nebel A, Filon D, Hohoff C, Faerman M, Brinkmann B, Oppenheim A (2001a) Haplogroup-specific deviation from the stepwise mutation model at the microsatellite loci DYS388 and DYS392. Eur J Hum Genet 9:22–26CrossRefPubMedGoogle Scholar
  30. Nebel A, Filon D, Brinkmann B, Majumder PP, Faerman M, Oppenheim A (2001b) The Y chromosome pool of Jews as part of the genetic landscape of the Middle East. Am J Hum Genet 69:1095–1112Google Scholar
  31. Nebel A, Landau-Tasseron E, Filon D, Oppenheim A, Faerman M (2002) Genetic evidence for the expansion of Arabian tribes into the Southern Levant and North Africa. Am J Hum Genet 70:1594–1596CrossRefPubMedGoogle Scholar
  32. Oefner PJ, Underhill PA (1998) DNA mutation detection using denaturing high performance liquid chromatography (DHPLC). Current protocols in human genetics, Suppl 19. Wiley, New York, pp 7.10.1–7.10.12Google Scholar
  33. Passarino G, Semino O, Magri C, Al-Zahery N, Benuzzi G, Quintana-Murci L, Andellnovic S, Bullc-Jakus F, et al. (2001) The 49a,f haplotype 11 is a new marker of the EU19 lineage that traces migrations from northern regions of the Black Sea. Hum Immunol 62:922–932CrossRefPubMedGoogle Scholar
  34. Qamar R, Ayub Q, Mohyuddin A, Helgason A, Mazhar K, Mansoor A, Zerjal T, Tyler-Smith C, Mehdi SQ (2002) Y-chromosomal DNA variation in Pakistan. Am J Hum Genet 70:1107–1124CrossRefPubMedGoogle Scholar
  35. Quintana-Murci L, Krausz C, Zerjal T, Sayar SH, Hammer MF, Mehdi SQ, Ayub Q, Qamar R, et al. (2001) Y-chromosome lineages trace diffusion of people and languages in southwestern Asia. Am J Hum Genet 68:537–542PubMedGoogle Scholar
  36. Raitio M, Lindroos K, Laukkanen M, Pastinen T, Sistonen P, Sajantila A, Syvänen A-C (2001) Y-chromosomal SNPs in Finno-Ugric speaking populations analyzed by minisequencing on microarrays. Genome Res 11:471–482CrossRefPubMedGoogle Scholar
  37. Renfrew C (1998) Word of Minos: the Minoan contribution to Mycenaean Greek and the linguistic geography of the Bronze Age Aegean. Cambridge Archaeol J 8:239–264Google Scholar
  38. Richards M, Macaulay V, Hickey E, Vega E, Sykes B, Guida V, Rengo C, Sellitto D, et al. (2000) Tracing European founder lineages in the Near Eastern mtDNA pool. Am J Hum Genet 67:1251–1276PubMedGoogle Scholar
  39. Richards M, Macaulay V, Torroni A, Bandelt H-J (2002) In search of geographical patterns in European mitochondrial DNA. Am J Hum Genet 71:1168–1174CrossRefPubMedGoogle Scholar
  40. Roberts N (2002) Did prehistoric landscape management retard the post-glacial spread of woodland Southwest Asia? Antiquity 76:1002–1010Google Scholar
  41. Rolf B, Meyer E, Brinkmann B, de Knijff P (1998) Polymorphism at the tetranucleotide repeat locus DYS389 in 10 populations reveals strong geographic clustering. Eur J Hum Genet 6:583–588CrossRefPubMedGoogle Scholar
  42. Rolf B, Röhl A, Forster P, Brinkmann B (1999) On the genetic origins of the Turks study of six Y-chromosomal short tandem repeats. In: Papiha S, Deka R, Chakraborty R (eds) Genomic diversity: applications in human population genetics. Kluwer Academic/Plenum, New York, pp 75–82Google Scholar
  43. Rosser ZH, Zerjal T, Hurles ME, Adojaan M, Alavantic D, Amorim A, Amos W, Armenteros M, et al. (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
  44. Russell J (1958) Late ancient and medieval populations. Trans Am Philos Soc 48:81Google Scholar
  45. Santachiara Benerecetti AS, 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 57:55–64PubMedGoogle Scholar
  46. Scozzari R, Cruciani F, Pangrazio A, Santolamazza P, Vona G, Moral P, Latini V, Varesi L, et al. (2001) Human Y-chromosome variation in the western Mediterranean area: implications for the peopling of the region. Hum Immunol 62:871–884CrossRefPubMedGoogle Scholar
  47. Semino O, Passarino G, Brega A, Fellous M, Santachiara-Benerecetti AS (1996) A view of the Neolithic demic-diffusion in Europe through two Y chromosome-specific markers. Am J Hum Genet 9:964–968Google Scholar
  48. Semino O, Passarino G, Oefner PJ, Lin AA, Arbuzova S, Beckman LE, De Benedictis G, Francalacci, et al. (2000a) The genetic legacy of Palaeolithic Homo sapiens in extant Europeans: a Y-chromosome perspective. Science 290:1155–1159PubMedGoogle Scholar
  49. Semino O, Passarino G, Quintana-Murci L, Liu A, Beres J, Czeizel A, Santachiara-Benerecetti AS (2000b) MtDNA and Y chromosome polymorphisms in Hungary: inferences from the palaeolithic, neolithic and Uralic influences on the modern Hungarian gene pool. Eur J Hum Genet 8:339–346CrossRefPubMedGoogle Scholar
  50. Shen P, Wang F, Underhill PA, Franco C, Yang W-H, Roxas A, Sung R, Lin AA, et al. (2000) Population genetic implications from sequence variation in four Y chromosome genes. Proc Natl Acad USA 97:7354–7359CrossRefGoogle Scholar
  51. Su B, Xiao C, Deka R, Seielstad MT, Kangwanpong D, Xiao J, Lu D, Underhill, PA, et al. (2000) Y chromosome haplotypes reveal prehistoric migrations to the Himalayas. Hum Genet 107:582–590CrossRefPubMedGoogle Scholar
  52. Sun C, Skaletsky H, Rozen S, Gromoll J, Nieschlag E, Oates R, Page DC (2000) Deletion of azoospermia factor a (AZFa) region of human Y chromosome caused by recombination between HERV15 proviruses. Hum Mol Genetics 9:2291–2296Google Scholar
  53. Thissen L (1999) Trajectories towards the neolithisation of NW Turkey. Documenta Praehistorica 26:29–39Google Scholar
  54. Thomas MG, Parfitt T, Weiss DA, Skorecki K, Wilson JF, le Roux M, Bradman N, Goldstein D (2000) Y chromosomes traveling south: the Cohen modal haplotype and the origins of the Lemba-the “black Jews of Southern Africa.” Am J Hum Genet 66:674–686Google Scholar
  55. Torroni A, Semino O, Scozzari R, Sirugo G, Spedini G, Abbas N, Fellous M, Santachiara Benerecetti AS (1990) Y chromosome DNA polymorphisms in human populations: differences between Caucasoids and Africans detected by 49a and 49f probes. Ann Hum Genet 54:287–296PubMedGoogle Scholar
  56. Torroni A, Bandelt HJ, D’Urbano L, Lahermo P, Moral P, Sellitto D, Rengo C, Forster P, et al. (1998) mtDNA analysis reveals a major late Paleolithic population expansion from southwestern to northeastern Europe. Am J Hum Genet 62:1137–1152PubMedGoogle Scholar
  57. Underhill PA (2002) Inference of Neolithic population histories using Y-chromosome haplotypes. In: Bellwood P, Renfrew P (eds) Examining the farming/language dispersal hypothesis. McDonald Institute for Archaeological Research, Cambridge, pp 65–78Google Scholar
  58. Underhill PA, Shen P, Lin AA, Jin L, Passarino G, Yang WH, Kauffman E, Bonné-Tamir B, et al. (2000) Y chromosome sequence variation and the history of human populations. Nat Genet 26:358–361CrossRefPubMedGoogle Scholar
  59. Underhill PA, Passarino G, Lin AA, Shen P, Foley RA, Mirazón Lahr M, Oefner PJ Cavalli-Sforza LL (2001) The phylogeography of Y chromosome binary haplotypes and the origins of modern human populations. Ann. Hum Genet 65:43–62CrossRefGoogle Scholar
  60. Weale ME, Yepiskoposyan L, Jager RF, Hovhannisyan N, Khudoyan A, Burbage-Hall O, Bradman N, Thomas MG (2001) Armenian Y chromosome haplotypes reveal strong regional structure within a single ethno-national group. Hum Genet 109:659–674PubMedGoogle Scholar
  61. Wells RS, Yuldasheva N, Ruzibakiev R, Underhill PA, Evseeva I, Blue-Smith J, Jin L, Su B, et al. (2001) The Eurasian heartland: a continental perspective on Y-chromosome diversity. Proc Natl Acad Sci USA 98:10244–10249CrossRefPubMedGoogle Scholar
  62. White PS, Tatum OL, Deaven LL, Longmire JL (1999) New, male-specific microsatellite markers from the human Y chromosome. Genomics 57:433–437PubMedGoogle Scholar
  63. Wilson I, Weale M, Balding D (1998) Genealogical inference from microsatellite data. Genetics 150:499–510PubMedGoogle Scholar
  64. 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
  65. Y Chromosome Consortium (2002) A nomenclature system for the tree of human Y-chromosomal binary haplogroups. Genome Res 12:339–348PubMedGoogle Scholar
  66. Zerjal T, Xue Y, Bertorelle G, Wells RS, Bao W, Zhu S, Qamar R, Ayub Q, et al. (2003) The genetic legacy of the Mongols. Am J Hum Genet 72:717–721CrossRefPubMedGoogle Scholar
  67. Zhivotovsky LA, Rosenberg NA, Feldman MW (2003) Features of evolution and expansion of modern humans, inferred from genomewide microsatellite markers. Am J Hum Genet 72:1171–1186CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • Cengiz Cinnioğlu
    • 1
    • 4
  • Roy King
    • 2
  • Toomas Kivisild
    • 3
  • Ersi Kalfoğlu
    • 4
  • Sevil Atasoy
    • 4
  • Gianpiero L. Cavalleri
    • 1
  • Anita S. Lillie
    • 1
  • Charles C. Roseman
    • 5
  • Alice A. Lin
    • 1
  • Kristina Prince
    • 1
  • Peter J. Oefner
    • 6
  • Peidong Shen
    • 6
  • Ornella Semino
    • 7
  • L. Luca Cavalli-Sforza
    • 1
  • Peter A. Underhill
    • 1
  1. 1.Department of GeneticsStanford University School of MedicineStanfordUSA
  2. 2.Department of Psychiatry and Behavioral SciencesStanford UniversityStanfordUSA
  3. 3.Estonian Biocentre and Tartu UniversityTartuEstonia
  4. 4.Institute of Forensic Sciences Istanbul University IstanbulTurkey
  5. 5.Anthropological SciencesStanford UniversityStanfordUSA
  6. 6.Stanford Genome Technology CenterPalo AltoUSA
  7. 7.Dipartimento di Genetica e MicrobiologiaUniversità di PaviaPaviaItaly

Personalised recommendations