Human Genetics

, Volume 116, Issue 4, pp 279–291 | Cite as

Signature of recent historical events in the European Y-chromosomal STR haplotype distribution

  • Lutz Roewer
  • Peter J. P. Croucher
  • Sascha Willuweit
  • Tim T. Lu
  • Manfred Kayser
  • Rüdiger Lessig
  • Peter de Knijff
  • Mark A. Jobling
  • Chris Tyler-Smith
  • Michael Krawczak
Original Investigation

Abstract

Previous studies of human Y-chromosomal single-nucleotide polymorphisms (Y-SNPs) established a link between the extant Y-SNP haplogroup distribution and the prehistoric demography of Europe. By contrast, our analysis of seven rapidly evolving Y-chromosomal short tandem repeat loci (Y-STRs) in over 12,700 samples from 91 different locations in Europe reveals a signature of more recent historic events, not previously detected by other genetic markers. Cluster analysis based upon molecular variance yields two clearly identifiable sub-clusters of Western and Eastern European Y-STR haplotypes, and a diverse transition zone in central Europe, where haplotype spectra change more rapidly with longitude than with latitude. This and other observed patterns of Y-STR similarity may plausibly be related to particular historical incidents, including, for example, the expansion of the Franconian and Ottoman Empires. We conclude that Y-STRs may be capable of resolving male genealogies to an unparalleled degree and could therefore provide a useful means to study local population structure and recent demographic history.

References

  1. Ammerman AJ, Cavalli-Sforza LL (1984) The neolithic transition and the genetics of populations in Europe. Princeton University Press, PrincetonGoogle Scholar
  2. Banniard M (1989) Genèse culturelle de l’Europe - Ve au VIII siècle. Le Seuil, ParisGoogle Scholar
  3. Barbujani G (1987) Autocorrelation of gene frequencies under isolation by distance. Genetics 117:777–782Google Scholar
  4. Barbujani G, Chikhi L (2000) Genetic population structure of Europeans inferred from nuclear and mitochondrial DNA polymorphisms. In: Renfrew C, Boyle K (eds) Archaeogenetics: DNA and the population prehistory of Europe. McDonald Institute for Archaeological Research, Cambridge, pp 119–129Google Scholar
  5. Bartlett R (1994) The making of Europe: conquest, colonization, and cultural change, 950-1350. Princeton University Press, PrincetonGoogle Scholar
  6. Boyd R, Silk JB (1997) How humans evolved. WW Norton, New YorkGoogle Scholar
  7. Chikhi L, Nichols RA, Barbujani G, Beaumont MA (2002) Y genetic data support the Neolithic demic diffusion model. Proc Natl Acad Sci U S A 99:11008–11013CrossRefGoogle Scholar
  8. Cooper DN, Krawczak M (1993) Human gene mutation. BIOS Scientific Publishers, OxfordGoogle Scholar
  9. Ewens WJ (1972) The sampling theory of selectively neutral alleles. Theor Popul Biol 3:87–112CrossRefGoogle Scholar
  10. Excoffier L, Smouse PE (1994) Using allele frequencies and geographic subdivision to reconstruct gene trees within a species: molecular variance parsimony. Genetics 136:343–359PubMedGoogle Scholar
  11. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among mtDNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  12. Gieysztor A, Kieniewicz S, Rostworowski E, Tazbir J, Wereszycki H (1979) History of Poland. Polish Scientific Publishers, WarsawGoogle Scholar
  13. Gill P, Brenner C, Brinkmann B, Budowle B, Carracedo A, Jobling MA, de Knijff P, Kayser M, Krawczak M, Mayr W, Morling N, Olaisen B, Pascali VL, Prinz M, Roewer L, Schneider PM, Sajantila A, Tyler-Smith C (2001) DNA commission of the international society of forensic genetics: recommendations on forensic analysis using Y chromosome STRs. Int J Legal Med 114:305–309CrossRefPubMedGoogle Scholar
  14. Gimbutas M (1971) The slavs. Thames & Hudson, LondonGoogle Scholar
  15. Helgason A, Sigurdadottir S, Nicholson J, Sykes B, Hill EW, Bradley DG, Bosnes V, Gulcher JR, Ward R, Stefansson K (2000) Estimating Scandinavian and gaelic ancestry in the male settlers of Iceland. Am J Hum Genet 67:697–717PubMedGoogle Scholar
  16. Jobling MA, Tyler-Smith C (2003) The human Y chromosome: an evolutionary marker comes of age. Nat Rev Genet 4:598–612CrossRefPubMedGoogle Scholar
  17. Jobling MA, Hurles M, Tyler-Smith C (2004) Human evolutionary genetics. Garland Science, New YorkGoogle Scholar
  18. Kayser M, Cagliá A, Corach D, Fretwell N, Gehrig C, Graziosi G, Heidorn F, Herrmann S, Herzog B, Hidding M, Honda K, Jobling M, Krawczak M, Leim K, Meuser S, Meyer E, Oesterreich W, Pandya A, Parson W, Piccinini A, Perez-Lezaun A, Prinz M, Schmitt C, Schneider PM, Szibor R, Teifel-Greding J, Weichhold G, de Knijff P, Roewer L (1997) Evaluation of Y chromosomal STRs: a multicenter study. Int J Leg Med 110:125–133CrossRefGoogle Scholar
  19. Kayser M, Roewer L, Hedman M, Henke L, Henke J, Brauer S, Krüger C, Krawczak M, Nagy M, Dobosz T, Szibor R, de Knijff P, Stoneking M, Sajantila A (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 66:1580–1588CrossRefPubMedGoogle Scholar
  20. Kayser M, Krawczak M, Excoffier L, Dieltjes P, Corach D, Pascali V, Gehrig C, Bernini LF, Jespersen J, Bakker E, Roewer L, de Knijff P (2001) Extensive analysis of chromosome Y microsatellite haplotypes from globally dispersed human populations. Am J Hum Genet 68:990–1018CrossRefPubMedGoogle Scholar
  21. Kittler R, Erler A, Brauer S, Stoneking M, Kayser M (2003) Apparent intrachromosomal exchange on the human Y chromosome explained by population history. Eur J Hum Genet 11:304–314CrossRefGoogle Scholar
  22. 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
  23. Lessig R, Edelmann J, Krawczak M (2001) Population genetics of Y-chromosomal microsatellites in Baltic males. Forensic Sci Int 118:153–157CrossRefGoogle Scholar
  24. Lessig R, Edelmann J, Zoledziewska M, Dobosz T, Fahr K, Kostrzewa M (2004) SNP-genotyping on human Y-chromosome for forensic purposes—comparison of two different methods. In: Progress in forensic genetics, vol 10, Elsevier, Amsterdam, pp 334–336Google Scholar
  25. Merriman J (1996) A history of modern Europe. WW Norton, New YorkGoogle Scholar
  26. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  27. Oota H, Settheetham-Ishida W, Tiwawech D, Ishida T, Stoneking M (2001) Human mtDNA and Y-chromosome variation is correlated with matrilocal versus patrilocal residence. Nat Genet 29:20–21CrossRefGoogle Scholar
  28. Ploski R, Wozniak M, Pawlowski R, Monies DM, Branicki W, Kupiec T, Kloostermann A, Dobosz T, Bosch E, Nowak E, Lessig R, Jobling MA, Roewer L, Kayser M (2002) Homogeneity and distinctiveness of Polish paternal lineages revealed by Y chromosome microsatellite haplotype analysis. Hum Genet 110:592–600CrossRefGoogle Scholar
  29. Richards M, Macaulay V, Torroni A, Bandelt HJ (2002) In search of geographical patterns in European mitochondrial DNA. Am J Hum Genet 71:1168–1174CrossRefGoogle Scholar
  30. Roewer L, Kayser M, Dieltjes P, Nagy M, Bakker E, Krawczak M, de Knijff P (1996) Analysis of molecular variance (AMOVA) of Y-chromosome specific microsatellites in two closely related human populations. Hum Mol Genet 5:1029–1033 (Erratum in Hum Mol Genet 6:828 1997)Google Scholar
  31. Roewer L, Kayser M, de Knijff P, Anslinger K, Cagliá A, Corach D, Füredi S, Henke L, Hidding M, Kärgel H-J, Lessig R, Nagy M, Pascali VL, Parson W, Rolf B, Schmitt C, Szibor R, Teifel-Greding J, Krawczak M (2000) A new method for the evaluation of matches in non-recombining genomes: application to Y-chromosomal short tandem repeat (STR) haplotypes in European males. Forensic Sci Int 114:31–43CrossRefGoogle Scholar
  32. Roewer L, Krawczak M, Willuweit S, Nagy M, Alves C, Amorim A, Anslinger K, Augustin C, Betz A, Bosch E, Cagliá A, Carracedo A, Corach D, Dekairelle AF, Dobosz T, Dupuy BM, Füredi S, Gehrig C, Gusmao L, Henke J, Henke L, Hidding M, Hohoff C, Hoste B, Jobling MA, Kärgel HJ, de Knijff P, Lessig R, Liebeherr E, Lorente M, Martínez-Jarreta B, Nievas P, Nowak M, Parson W, Pascali VL, Penacino G, Ploski R, Rolf B, Sala A, Schmidt U, Schmitt C, Schneider PM, Szibor R, Teifel-Greding J, Kayser M (2001) Online reference database of European Y-chromosomal short tandem repeat (STR) haplotypes. Forensic Sci Int 118:106–113CrossRefPubMedGoogle Scholar
  33. 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 6:583–588CrossRefGoogle Scholar
  34. Rosser ZH, Zerjal T, Hurles ME, Adojaan M, Alavantic D, Amorim A, Amos W, Armenteros M, Arroyo E, Barbujani G, Beckman L, Bertranpetit J, Bosch E, Bradley DG, Brede G, Cooper GC, Corte-Real H, de Knijff P, Decorte R, Dubrova YE, Evgravov O, Gilissen A, Glisic S, Gölge M, Hill EW, Jeziorovska A, Kalaydijeva L, Kayser M, Kravcenko SA, Lavinha J, Livshits LA, Maria S, McElreavey K, Meitinger TA, Melegh B, Mitchell RJ, Nicholson J, Norby S, Noveletto A, Pandya A, Parik J, Patsalis PC, Pereira L, Peterlin B, Pielberg G, Prata MJ, Previderé C, Rajczy K, Roewer L, Rootsi S, Rubinsztein DC, Saillard J, Santos FR, Shlumukova M, Stefanescu G, Sykes BC, Tolun A, Villems R, Tyler-Smith C, Jobling MA (2000) Y-chromosomal diversity within Europe is clinal and influenced primarily by geography rather than language. Am J Hum Genet 67:1526–1543CrossRefGoogle Scholar
  35. Schneider S, Roessli D, Excoffier L (2000) Arlequin: A software for population genetics data analysis, version 2.000. Genetics and Biometry Lab, Dept. of Anthropology, University of GenevaGoogle Scholar
  36. Seielstad MT, Minch E, Cavalli-Sforza LL (1998) Genetic evidence for a higher female migration rate in humans. Nat Genet 20:278–180CrossRefGoogle Scholar
  37. 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 290:1155–1159CrossRefPubMedGoogle Scholar
  38. Shriver MD, Jin L, Chakraborty R, Boerwinkle E (1993) VNTR allele frequency distributions under the stepwise mutation model: a computer simulation approach. Genetics134:983–993Google Scholar
  39. Sokal RR, Oden NL (1978) Spatial autocorrelation in biology. 1. Methodology. Biol J Linn Soc 10:199–228Google Scholar
  40. 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 109:659-674CrossRefGoogle Scholar
  41. Weale ME, Weiss DA, Jager RF, Bradman N, Thomas MG (2002) Y chromosome evidence for Anglo-Saxon mass migration. Mol Biol Evol 19:1008–1021PubMedGoogle Scholar
  42. Wells RS, Yuldasheva N, Ruzibakiev R, Underhill PA, Evseeva I, Blue-Smith J, Jin L, Su B, Pitchappan R, Shanmugalakshmi S, Balakrishnan K, Read M, Pearson NM, Zerjal T, Webster MT, Zholoshvili I, Jamarjashvili E, Gambarov S, Nikbin B, Dostiev A, Aknazarov O, Zalloua P, Tsoy I, Kitaev M, Mirrakhimov M, Chariev A, Bodmer WF (2001) The Eurasian heartland: a continental perspective on Y-chromosome diversity. Proc Natl Acad Sci U S A 98:10244–10249CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Lutz Roewer
    • 1
  • Peter J. P. Croucher
    • 2
    • 3
  • Sascha Willuweit
    • 1
  • Tim T. Lu
    • 3
  • Manfred Kayser
    • 4
    • 5
  • Rüdiger Lessig
    • 6
  • Peter de Knijff
    • 7
  • Mark A. Jobling
    • 8
  • Chris Tyler-Smith
    • 9
  • Michael Krawczak
    • 3
  1. 1.Institute of Legal MedicineHumboldt-UniversityBerlinGermany
  2. 2.First Department of MedicineChristian-Albrechts-UniversityKielGermany
  3. 3.Institute of Medical Informatics and StatisticsChristian-Albrechts-UniversityKielGermany
  4. 4.Max-Planck-Institute for Evolutionary AnthropologyLeipzigGermany
  5. 5.Department of Forensic Molecular BiologyErasmus UniversityRotterdamThe Netherlands
  6. 6.Institute of Legal MedicineUniversity of LeipzigGermany
  7. 7.Forensic Laboratory for DNA ResearchLeiden UniversityThe Netherlands
  8. 8.Department of GeneticsUniversity of LeicesterUK
  9. 9.The Wellcome Trust Sanger InstituteHinxtonUK

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