Skip to main content
NCBI home page
American Journal of Human Genetics logoLink to American Journal of Human Genetics
. 1997 Sep;61(3):719–733. doi: 10.1086/515500

Differential structuring of human populations for homologous X and Y microsatellite loci.

R Scozzari 1, F Cruciani 1, P Malaspina 1, P Santolamazza 1, B M Ciminelli 1, A Torroni 1, D Modiano 1, D C Wallace 1, K K Kidd 1, A Olckers 1, P Moral 1, L Terrenato 1, N Akar 1, R Qamar 1, A Mansoor 1, S Q Mehdi 1, G Meloni 1, G Vona 1, D E Cole 1, W Cai 1, A Novelletto 1
PMCID: PMC1715969  PMID: 9326337

Abstract

The global pattern of variation at the homologous microsatellite loci DYS413 (Yq11) and DXS8174 and DXS8175 (Xp22) was analyzed by examination of 30 world populations from four continents, accounting for more than 1,100 chromosomes per locus. The data showed discordant patterns of among- and within-population gene diversity for the Y-linked and the X-linked microsatellites. For the Y-linked polymorphism, all groups of populations displayed high FST values (the correlation between random haplotypes within subpopulations, relative to haplotypes of the total population) and showed a general trend for the haplotypes to cluster in a population-specific way. This was especially true for sub-Saharan African populations. The data also indicated that a large fraction of the variation among populations was due to the accumulation of new variants associated with the radiation process. Europeans exhibited the highest level of within-population haplotype diversity, whereas sub-Saharan Africans showed the lowest. In contrast, data for the two X-linked polymorphisms were concordant in showing lower FST values, as compared with those for DYS413, but higher within-population variances, for African versus non-African populations. Whereas the results for the X-linked loci agreed with a model of greater antiquity for the African populations, those for DYS413 showed a confounding pattern that is apparently at odds with such a model. Possible factors involved in this differential structuring for homologous X and Y microsatellite polymorphisms are discussed.

Full text

PDF
719

Images in this article

721Figure 1
on p.721

Selected References

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

  1. Andreassen R., Egeland T., Olaisen B. Mutation rate in the hypervariable VNTR g3 (D7S22) is affected by allele length and a flanking DNA sequence polymorphism near the repeat array. Am J Hum Genet. 1996 Aug;59(2):360–367. [PMC free article] [PubMed] [Google Scholar]
  2. Armour J. A., Anttinen T., May C. A., Vega E. E., Sajantila A., Kidd J. R., Kidd K. K., Bertranpetit J., Päbo S., Jeffreys A. J. Minisatellite diversity supports a recent African origin for modern humans. Nat Genet. 1996 Jun;13(2):154–160. doi: 10.1038/ng0696-154. [DOI] [PubMed] [Google Scholar]
  3. Bowcock A. M., Kidd J. R., Mountain J. L., Hebert J. M., Carotenuto L., Kidd K. K., Cavalli-Sforza L. L. Drift, admixture, and selection in human evolution: a study with DNA polymorphisms. Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):839–843. doi: 10.1073/pnas.88.3.839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bowcock A. M., Ruiz-Linares A., Tomfohrde J., Minch E., Kidd J. R., Cavalli-Sforza L. L. High resolution of human evolutionary trees with polymorphic microsatellites. Nature. 1994 Mar 31;368(6470):455–457. doi: 10.1038/368455a0. [DOI] [PubMed] [Google Scholar]
  5. Cai W., Filosa S., Martini G. DNA haplotypes in the G6PD gene cluster studied in the Chinese Li population and their relationship to G6PDCanton. Hum Hered. 1994 Sep-Oct;44(5):279–286. doi: 10.1159/000154230. [DOI] [PubMed] [Google Scholar]
  6. Cann R. L., Stoneking M., Wilson A. C. Mitochondrial DNA and human evolution. Nature. 1987 Jan 1;325(6099):31–36. doi: 10.1038/325031a0. [DOI] [PubMed] [Google Scholar]
  7. Ciminelli B. M., Pompei F., Malaspina P., Hammer M., Persichetti F., Pignatti P. F., Palena A., Anagnou N., Guanti G., Jodice C. Recurrent simple tandem repeat mutations during human Y-chromosome radiation in Caucasian subpopulations. J Mol Evol. 1995 Dec;41(6):966–973. doi: 10.1007/BF00173177. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Crow J. F. How much do we know about spontaneous human mutation rates? Environ Mol Mutagen. 1993;21(2):122–129. doi: 10.1002/em.2850210205. [DOI] [PubMed] [Google Scholar]
  10. Deka R., Jin L., Shriver M. D., Yu L. M., DeCroo S., Hundrieser J., Bunker C. H., Ferrell R. E., Chakraborty R. Population genetics of dinucleotide (dC-dA)n.(dG-dT)n polymorphisms in world populations. Am J Hum Genet. 1995 Feb;56(2):461–474. [PMC free article] [PubMed] [Google Scholar]
  11. Deka R., Shriver M. D., Yu L. M., Ferrell R. E., Chakraborty R. Intra- and inter-population diversity at short tandem repeat loci in diverse populations of the world. Electrophoresis. 1995 Sep;16(9):1659–1664. doi: 10.1002/elps.11501601275. [DOI] [PubMed] [Google Scholar]
  12. Di Rienzo A., Wilson A. C. Branching pattern in the evolutionary tree for human mitochondrial DNA. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1597–1601. doi: 10.1073/pnas.88.5.1597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dib C., Fauré S., Fizames C., Samson D., Drouot N., Vignal A., Millasseau P., Marc S., Hazan J., Seboun E. A comprehensive genetic map of the human genome based on 5,264 microsatellites. Nature. 1996 Mar 14;380(6570):152–154. doi: 10.1038/380152a0. [DOI] [PubMed] [Google Scholar]
  14. Dorit R. L., Akashi H., Gilbert W. Absence of polymorphism at the ZFY locus on the human Y chromosome. Science. 1995 May 26;268(5214):1183–1185. doi: 10.1126/science.7761836. [DOI] [PubMed] [Google Scholar]
  15. Edwards A., Hammond H. A., Jin L., Caskey C. T., Chakraborty R. Genetic variation at five trimeric and tetrameric tandem repeat loci in four human population groups. Genomics. 1992 Feb;12(2):241–253. doi: 10.1016/0888-7543(92)90371-x. [DOI] [PubMed] [Google Scholar]
  16. Excoffier L., Smouse P. E., Quattro J. M. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics. 1992 Jun;131(2):479–491. doi: 10.1093/genetics/131.2.479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ferrero G. B., Franco B., Roth E. J., Firulli B. A., Borsani G., Delmas-Mata J., Weissenbach J., Halley G., Schlessinger D., Chinault A. C. An integrated physical and genetic map of a 35 Mb region on chromosome Xp22.3-Xp21.3. Hum Mol Genet. 1995 Oct;4(10):1821–1827. doi: 10.1093/hmg/4.10.1821. [DOI] [PubMed] [Google Scholar]
  18. Figus A., Angius A., Loudianos G., Bertini C., Dessi V., Loi A., Deiana M., Lovicu M., Olla N., Sole G. Molecular pathology and haplotype analysis of Wilson disease in Mediterranean populations. Am J Hum Genet. 1995 Dec;57(6):1318–1324. [PMC free article] [PubMed] [Google Scholar]
  19. Freimer N. B., Slatkin M. Microsatellites: evolution and mutational processes. Ciba Found Symp. 1996;197:51–72. doi: 10.1002/9780470514887.ch4. [DOI] [PubMed] [Google Scholar]
  20. Goldstein D. B., Ruiz Linares A., Cavalli-Sforza L. L., Feldman M. W. An evaluation of genetic distances for use with microsatellite loci. Genetics. 1995 Jan;139(1):463–471. doi: 10.1093/genetics/139.1.463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Gyapay G., Morissette J., Vignal A., Dib C., Fizames C., Millasseau P., Marc S., Bernardi G., Lathrop M., Weissenbach J. The 1993-94 Généthon human genetic linkage map. Nat Genet. 1994 Jun;7(2 Spec No):246–339. doi: 10.1038/ng0694supp-246. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Hammer M. F., Spurdle A. B., Karafet T., Bonner M. R., Wood E. T., Novelletto A., Malaspina P., Mitchell R. J., Horai S., Jenkins T. The geographic distribution of human Y chromosome variation. Genetics. 1997 Mar;145(3):787–805. doi: 10.1093/genetics/145.3.787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Horai S., Hayasaka K., Kondo R., Tsugane K., Takahata N. Recent African origin of modern humans revealed by complete sequences of hominoid mitochondrial DNAs. Proc Natl Acad Sci U S A. 1995 Jan 17;92(2):532–536. doi: 10.1073/pnas.92.2.532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Huoponen K., Torroni A., Wickman P. R., Sellitto D., Gurley D. S., Scozzari R., Wallace D. C. Mitochondrial DNA and Y chromosome-specific polymorphisms in the Seminole Tribe of Florida. Eur J Hum Genet. 1997 Jan-Feb;5(1):25–34. [PubMed] [Google Scholar]
  27. Jakubiczka S., Arnemann J., Cooke H. J., Krawczak M., Schmidtke J. A search for restriction fragment length polymorphism on the human Y chromosome. Hum Genet. 1989 Dec;84(1):86–88. doi: 10.1007/BF00210680. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Jorde L. B., Bamshad M. J., Watkins W. S., Zenger R., Fraley A. E., Krakowiak P. A., Carpenter K. D., Soodyall H., Jenkins T., Rogers A. R. Origins and affinities of modern humans: a comparison of mitochondrial and nuclear genetic data. Am J Hum Genet. 1995 Sep;57(3):523–538. doi: 10.1002/ajmg.1320570340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kidd J. R., Black F. L., Weiss K. M., Balazs I., Kidd K. K. Studies of three Amerindian populations using nuclear DNA polymorphisms. Hum Biol. 1991 Dec;63(6):775–794. [PubMed] [Google Scholar]
  31. Konotey-Ahulu F. I. Male procreative superiority index (MPSI): the missing coefficient in African anthropogenetics. Br Med J. 1980 Dec 20;281(6256):1700–1702. doi: 10.1136/bmj.281.6256.1700. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Long J. C. The allelic correlation structure of Gainj- and Kalam-speaking people. I. The estimation and interpretation of Wright's F-statistics. Genetics. 1986 Mar;112(3):629–647. doi: 10.1093/genetics/112.3.629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Lucotte G., Hazout S. Y-chromosome DNA haplotypes in Basques. J Mol Evol. 1996 Apr;42(4):472–475. doi: 10.1007/BF02498642. [DOI] [PubMed] [Google Scholar]
  34. Malaspina P., Ciminelli B. M., Viggiano L., Jodice C., Cruciani F., Santolamazza P., Sellitto D., Scozzari R., Terrenato L., Rocchi M. Characterization of a small family (CAIII) of microsatellite-containing sequences with X-Y homology. J Mol Evol. 1997 Jun;44(6):652–659. doi: 10.1007/pl00006189. [DOI] [PubMed] [Google Scholar]
  35. Malaspina P., Persichetti F., Novelletto A., Iodice C., Terrenato L., Wolfe J., Ferraro M., Prantera G. The human Y chromosome shows a low level of DNA polymorphism. Ann Hum Genet. 1990 Oct;54(Pt 4):297–305. doi: 10.1111/j.1469-1809.1990.tb00385.x. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Meroni G., Franco B., Archidiacono N., Messali S., Andolfi G., Rocchi M., Ballabio A. Characterization of a cluster of sulfatase genes on Xp22.3 suggests gene duplications in an ancestral pseudoautosomal region. Hum Mol Genet. 1996 Apr;5(4):423–431. doi: 10.1093/hmg/5.4.423. [DOI] [PubMed] [Google Scholar]
  38. Michalakis Y., Excoffier L. A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics. 1996 Mar;142(3):1061–1064. doi: 10.1093/genetics/142.3.1061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Monckton D. G., Neumann R., Guram T., Fretwell N., Tamaki K., MacLeod A., Jeffreys A. J. Minisatellite mutation rate variation associated with a flanking DNA sequence polymorphism. Nat Genet. 1994 Oct;8(2):162–170. doi: 10.1038/ng1094-162. [DOI] [PubMed] [Google Scholar]
  40. Primmer C. R., Saino N., Møller A. P., Ellegren H. Directional evolution in germline microsatellite mutations. Nat Genet. 1996 Aug;13(4):391–393. doi: 10.1038/ng0896-391. [DOI] [PubMed] [Google Scholar]
  41. Rogers A. R., Jorde L. B. Ascertainment bias in estimates of average heterozygosity. Am J Hum Genet. 1996 May;58(5):1033–1041. [PMC free article] [PubMed] [Google Scholar]
  42. Ruiz Linares A., Nayar K., Goldstein D. B., Hebert J. M., Seielstad M. T., Underhill P. A., Lin A. A., Feldman M. W., Cavalli Sforza L. L. Geographic clustering of human Y-chromosome haplotypes. Ann Hum Genet. 1996 Sep;60(Pt 5):401–408. doi: 10.1111/j.1469-1809.1996.tb00438.x. [DOI] [PubMed] [Google Scholar]
  43. Schaefer L., Ferrero G. B., Grillo A., Bassi M. T., Roth E. J., Wapenaar M. C., van Ommen G. J., Mohandas T. K., Rocchi M., Zoghbi H. Y. A high resolution deletion map of human chromosome Xp22. Nat Genet. 1993 Jul;4(3):272–279. doi: 10.1038/ng0793-272. [DOI] [PubMed] [Google Scholar]
  44. Scozzari R., Cruciani F., Santolamazza P., Parra E., Sellitto D., Modiano D., Meloni G., Cai W., Moral P. Novel tetranucleotide repeat polymorphism in the human adenosine deaminase gene: interethnic comparison of three major human groups. Hum Biol. 1996 Apr;68(2):315–320. [PubMed] [Google Scholar]
  45. Scozzari R., Cruciani F., Santolamazza P., Sellitto D., Cole D. E., Rubin L. A., Labuda D., Marini E., Succa V., Vona G. mtDNA and Y chromosome-specific polymorphisms in modern Ojibwa: implications about the origin of their gene pool. Am J Hum Genet. 1997 Jan;60(1):241–244. [PMC free article] [PubMed] [Google Scholar]
  46. Semino O., Passarino G., Brega A., Fellous M., Santachiara-Benerecetti A. S. A view of the neolithic demic diffusion in Europe through two Y chromosome-specific markers. Am J Hum Genet. 1996 Oct;59(4):964–968. [PMC free article] [PubMed] [Google Scholar]
  47. Shimmin L. C., Chang B. H., Li W. H. Male-driven evolution of DNA sequences. Nature. 1993 Apr 22;362(6422):745–747. doi: 10.1038/362745a0. [DOI] [PubMed] [Google Scholar]
  48. Slatkin M. A measure of population subdivision based on microsatellite allele frequencies. Genetics. 1995 Jan;139(1):457–462. doi: 10.1093/genetics/139.1.457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Spurdle A. B., Hammer M. F., Jenkins T. The Y Alu polymorphism in southern African populations and its relationship to other Y-specific polymorphisms. Am J Hum Genet. 1994 Feb;54(2):319–330. [PMC free article] [PubMed] [Google Scholar]
  50. 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]
  51. Terrenato L., Ulizzi L., San Martini A. The effects of demographic transition on the opportunity for selection: changes during the last century in Italy. Ann Hum Genet. 1979 Jan;42(3):391–399. doi: 10.1111/j.1469-1809.1979.tb00671.x. [DOI] [PubMed] [Google Scholar]
  52. Tishkoff S. A., Dietzsch E., Speed W., Pakstis A. J., Kidd J. R., Cheung K., Bonné-Tamir B., Santachiara-Benerecetti A. S., Moral P., Krings M. Global patterns of linkage disequilibrium at the CD4 locus and modern human origins. Science. 1996 Mar 8;271(5254):1380–1387. doi: 10.1126/science.271.5254.1380. [DOI] [PubMed] [Google Scholar]
  53. Torroni A., Semino O., Scozzari R., Sirugo G., Spedini G., Abbas N., Fellous M., Santachiara Benerecetti A. S. Y chromosome DNA polymorphisms in human populations: differences between Caucasoids and Africans detected by 49a and 49f probes. Ann Hum Genet. 1990 Oct;54(Pt 4):287–296. doi: 10.1111/j.1469-1809.1990.tb00384.x. [DOI] [PubMed] [Google Scholar]
  54. 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]
  55. Vigilant L., Stoneking M., Harpending H., Hawkes K., Wilson A. C. African populations and the evolution of human mitochondrial DNA. Science. 1991 Sep 27;253(5027):1503–1507. doi: 10.1126/science.1840702. [DOI] [PubMed] [Google Scholar]
  56. Wainscoat J. S., Hill A. V., Boyce A. L., Flint J., Hernandez M., Thein S. L., Old J. M., Lynch J. R., Falusi A. G., Weatherall D. J. Evolutionary relationships of human populations from an analysis of nuclear DNA polymorphisms. Nature. 1986 Feb 6;319(6053):491–493. doi: 10.1038/319491a0. [DOI] [PubMed] [Google Scholar]
  57. Wallace D. C. 1994 William Allan Award Address. Mitochondrial DNA variation in human evolution, degenerative disease, and aging. Am J Hum Genet. 1995 Aug;57(2):201–223. [PMC free article] [PubMed] [Google Scholar]
  58. 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]
  59. 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]

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

RESOURCES