Skip to main content
PMC home page
American Journal of Human Genetics logoLink to American Journal of Human Genetics
. 1998 Dec;63(6):1793–1806. doi: 10.1086/302147

European Y-chromosomal lineages in Polynesians: a contrast to the population structure revealed by mtDNA.

M E Hurles 1, C Irven 1, J Nicholson 1, P G Taylor 1, F R Santos 1, J Loughlin 1, M A Jobling 1, B C Sykes 1
PMCID: PMC1377652  PMID: 9837833

Abstract

We have used Y-chromosomal polymorphisms to trace paternal lineages in Polynesians by use of samples previously typed for mtDNA variants. A genealogical approach utilizing hierarchical analysis of eight rare-event biallelic polymorphisms, seven microsatellite loci, and internal structural analysis of the hypervariable minisatellite, MSY1, has been used to define three major paternal-lineage clusters in Polynesians. Two of these clusters, both defined by novel MSY1 modular structures and representing 55% of the Polynesians studied, are also found in coastal Papua New Guinea. Reduced Polynesian diversity, relative to that in Melanesians, is illustrated by the presence of several examples of identical MSY1 codes and microsatellite haplotypes within these lineage clusters in Polynesians. The complete lack of Y chromosomes having the M4 base substitution in Polynesians, despite their prevalence (64%) in Melanesians, may also be a result of the multiple bottleneck events during the colonization of this region of the world. The origin of the M4 mutation has been dated by use of two independent methods based on microsatellite-haplotype and minisatellite-code diversity. Because of the wide confidence limits on the mutation rates of these loci, the M4 mutation cannot be conclusively dated relative to the colonization of Polynesia, 3,000 years ago. The other major lineage cluster found in Polynesians, defined by a base substitution at the 92R7 locus, represents 27% of the Polynesians studied and, most probably, originates in Europe. This is the first Y-chromosomal evidence of major European admixture with indigenous Polynesian populations and contrasts sharply with the picture given by mtDNA evidence.

Full Text

The Full Text of this article is available as a PDF (748.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bertranpetit J., Calafell F. Genetic and geographical variability in cystic fibrosis: evolutionary considerations. Ciba Found Symp. 1996;197:97–118. doi: 10.1002/9780470514887.ch6. [DOI] [PubMed] [Google Scholar]
  2. Bianchi N. O., Bailliet G., Bravi C. M., Carnese R. F., Rothhammer F., Martínez-Marignac V. L., Pena S. D. Origin of Amerindian Y-chromosomes as inferred by the analysis of six polymorphic markers. Am J Phys Anthropol. 1997 Jan;102(1):79–89. doi: 10.1002/(SICI)1096-8644(199701)102:1<79::AID-AJPA7>3.0.CO;2-8. [DOI] [PubMed] [Google Scholar]
  3. Bouzekri N., Taylor P. G., Hammer M. F., Jobling M. A. Novel mutation processes in the evolution of a haploid minisatellite, MSY1: array homogenization without homogenization. Hum Mol Genet. 1998 Apr;7(4):655–659. doi: 10.1093/hmg/7.4.655. [DOI] [PubMed] [Google Scholar]
  4. Bravi C. M., Sans M., Bailliet G., Martínez-Marignac V. L., Portas M., Barreto I., Bonilla C., Bianchi N. O. Characterization of mitochondrial DNA and Y-chromosome haplotypes in a Uruguayan population of African ancestry. Hum Biol. 1997 Oct;69(5):641–652. [PubMed] [Google Scholar]
  5. Cooper G., Amos W., Hoffman D., Rubinsztein D. C. Network analysis of human Y microsatellite haplotypes. Hum Mol Genet. 1996 Nov;5(11):1759–1766. doi: 10.1093/hmg/5.11.1759. [DOI] [PubMed] [Google Scholar]
  6. Flint J., Boyce A. J., Martinson J. J., Clegg J. B. Population bottlenecks in Polynesia revealed by minisatellites. Hum Genet. 1989 Oct;83(3):257–263. doi: 10.1007/BF00285167. [DOI] [PubMed] [Google Scholar]
  7. Forster P., Kayser M., Meyer E., Roewer L., Pfeiffer H., Benkmann H., Brinkmann B. Phylogenetic resolution of complex mutational features at Y-STR DYS390 in aboriginal Australians and Papuans. Mol Biol Evol. 1998 Sep;15(9):1108–1114. doi: 10.1093/oxfordjournals.molbev.a026018. [DOI] [PubMed] [Google Scholar]
  8. Goldstein D. B., Zhivotovsky L. A., Nayar K., Linares A. R., Cavalli-Sforza L. L., Feldman M. W. Statistical properties of the variation at linked microsatellite loci: implications for the history of human Y chromosomes. Mol Biol Evol. 1996 Nov;13(9):1213–1218. doi: 10.1093/oxfordjournals.molbev.a025686. [DOI] [PubMed] [Google Scholar]
  9. Hammer M. F. A recent common ancestry for human Y chromosomes. Nature. 1995 Nov 23;378(6555):376–378. doi: 10.1038/378376a0. [DOI] [PubMed] [Google Scholar]
  10. Hammer M. F., Horai S. Y chromosomal DNA variation and the peopling of Japan. Am J Hum Genet. 1995 Apr;56(4):951–962. [PMC free article] [PubMed] [Google Scholar]
  11. Hammer M. F., Karafet T., Rasanayagam A., Wood E. T., Altheide T. K., Jenkins T., Griffiths R. C., Templeton A. R., Zegura S. L. Out of Africa and back again: nested cladistic analysis of human Y chromosome variation. Mol Biol Evol. 1998 Apr;15(4):427–441. doi: 10.1093/oxfordjournals.molbev.a025939. [DOI] [PubMed] [Google Scholar]
  12. Heyer E., Puymirat J., Dieltjes P., Bakker E., de Knijff P. Estimating Y chromosome specific microsatellite mutation frequencies using deep rooting pedigrees. Hum Mol Genet. 1997 May;6(5):799–803. doi: 10.1093/hmg/6.5.799. [DOI] [PubMed] [Google Scholar]
  13. Jobling M. A., Bouzekri N., Taylor P. G. Hypervariable digital DNA codes for human paternal lineages: MVR-PCR at the Y-specific minisatellite, MSY1 (DYF155S1). Hum Mol Genet. 1998 Apr;7(4):643–653. doi: 10.1093/hmg/7.4.643. [DOI] [PubMed] [Google Scholar]
  14. Jobling M. A., Samara V., Pandya A., Fretwell N., Bernasconi B., Mitchell R. J., Gerelsaikhan T., Dashnyam B., Sajantila A., Salo P. J. Recurrent duplication and deletion polymorphisms on the long arm of the Y chromosome in normal males. Hum Mol Genet. 1996 Nov;5(11):1767–1775. doi: 10.1093/hmg/5.11.1767. [DOI] [PubMed] [Google Scholar]
  15. Jobling M. A., Tyler-Smith C. Fathers and sons: the Y chromosome and human evolution. Trends Genet. 1995 Nov;11(11):449–456. doi: 10.1016/s0168-9525(00)89144-1. [DOI] [PubMed] [Google Scholar]
  16. Kwok C., Tyler-Smith C., Mendonca B. B., Hughes I., Berkovitz G. D., Goodfellow P. N., Hawkins J. R. Mutation analysis of the 2 kb 5' to SRY in XY females and XY intersex subjects. J Med Genet. 1996 Jun;33(6):465–468. doi: 10.1136/jmg.33.6.465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lum J. K., Cann R. L., Martinson J. J., Jorde L. B. Mitochondrial and nuclear genetic relationships among Pacific Island and Asian populations. Am J Hum Genet. 1998 Aug;63(2):613–624. doi: 10.1086/301949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lum J. K., Rickards O., Ching C., Cann R. L. Polynesian mitochondrial DNAs reveal three deep maternal lineage clusters. Hum Biol. 1994 Aug;66(4):567–590. [PubMed] [Google Scholar]
  19. Mathias N., Bayés M., Tyler-Smith C. Highly informative compound haplotypes for the human Y chromosome. Hum Mol Genet. 1994 Jan;3(1):115–123. doi: 10.1093/hmg/3.1.115. [DOI] [PubMed] [Google Scholar]
  20. Melton T., Peterson R., Redd A. J., Saha N., Sofro A. S., Martinson J., Stoneking M. Polynesian genetic affinities with Southeast Asian populations as identified by mtDNA analysis. Am J Hum Genet. 1995 Aug;57(2):403–414. [PMC free article] [PubMed] [Google Scholar]
  21. Redd A. J., Takezaki N., Sherry S. T., McGarvey S. T., Sofro A. S., Stoneking M. Evolutionary history of the COII/tRNALys intergenic 9 base pair deletion in human mitochondrial DNAs from the Pacific. Mol Biol Evol. 1995 Jul;12(4):604–615. doi: 10.1093/oxfordjournals.molbev.a040240. [DOI] [PubMed] [Google Scholar]
  22. Reed P. W., Davies J. L., Copeman J. B., Bennett S. T., Palmer S. M., Pritchard L. E., Gough S. C., Kawaguchi Y., Cordell H. J., Balfour K. M. Chromosome-specific microsatellite sets for fluorescence-based, semi-automated genome mapping. Nat Genet. 1994 Jul;7(3):390–395. doi: 10.1038/ng0794-390. [DOI] [PubMed] [Google Scholar]
  23. Spurdle A. B., Woodfield D. G., Hammer M. F., Jenkins T. The genetic affinity of Polynesians: evidence from Y chromosome polymorphisms. Ann Hum Genet. 1994 Jul;58(Pt 3):251–263. doi: 10.1111/j.1469-1809.1994.tb01889.x. [DOI] [PubMed] [Google Scholar]
  24. Spurdle A., Jenkins T. The search for Y chromosome polymorphism is extended to negroids. Hum Mol Genet. 1992 Jun;1(3):169–170. doi: 10.1093/hmg/1.3.169. [DOI] [PubMed] [Google Scholar]
  25. Sykes B., Leiboff A., Low-Beer J., Tetzner S., Richards M. The origins of the Polynesians: an interpretation from mitochondrial lineage analysis. Am J Hum Genet. 1995 Dec;57(6):1463–1475. [PMC free article] [PubMed] [Google Scholar]
  26. Underhill P. A., Jin L., Lin A. A., Mehdi S. Q., Jenkins T., Vollrath D., Davis R. W., Cavalli-Sforza L. L., Oefner P. J. Detection of numerous Y chromosome biallelic polymorphisms by denaturing high-performance liquid chromatography. Genome Res. 1997 Oct;7(10):996–1005. doi: 10.1101/gr.7.10.996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Underhill P. A., Jin L., Zemans R., Oefner P. J., Cavalli-Sforza L. L. A pre-Columbian Y chromosome-specific transition and its implications for human evolutionary history. Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):196–200. doi: 10.1073/pnas.93.1.196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Veitia R., Ion A., Barbaux S., Jobling M. A., Souleyreau N., Ennis K., Ostrer H., Tosi M., Meo T., Chibani J. Mutations and sequence variants in the testis-determining region of the Y chromosome in individuals with a 46,XY female phenotype. Hum Genet. 1997 May;99(5):648–652. doi: 10.1007/s004390050422. [DOI] [PubMed] [Google Scholar]
  29. Whitfield L. S., Sulston J. E., Goodfellow P. N. Sequence variation of the human Y chromosome. Nature. 1995 Nov 23;378(6555):379–380. doi: 10.1038/378379a0. [DOI] [PubMed] [Google Scholar]
  30. Zerjal T., Dashnyam B., Pandya A., Kayser M., Roewer L., Santos F. R., Schiefenhövel W., Fretwell N., Jobling M. A., Harihara S. Genetic relationships of Asians and Northern Europeans, revealed by Y-chromosomal DNA analysis. Am J Hum Genet. 1997 May;60(5):1174–1183. [PMC free article] [PubMed] [Google Scholar]
  31. de Knijff P., Kayser M., Caglià A., Corach D., Fretwell N., Gehrig C., Graziosi G., Heidorn F., Herrmann S., Herzog B. Chromosome Y microsatellites: population genetic and evolutionary aspects. Int J Legal Med. 1997;110(3):134–149. doi: 10.1007/s004140050052. [DOI] [PubMed] [Google Scholar]

Articles from American Journal of Human Genetics are provided here courtesy of American Society of Human Genetics

RESOURCES