Skip to main content
SpringerLink
Log in

Evolutionary Dynamics of Duplicated Microsatellites Shared by Sex Chromosomes

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Segmental duplications on sex chromosomes constitute an important proportion of recent duplications (~30%). Among those, the evolution of duplicated noncoding DNA is still poorly investigated. We focus our work on repeated DNA sequences extensively used in population genetics and evolution: microsatellites. Six duplicated (CA) n microsatellite loci, located on the homologous region of human sex chromosomes, were studied at the intraspecific level in Homo sapiens and by an orthologous comparison in eight primate species. At the intraspecific level, we evaluated the congruence in paralogous divergence between the flanking sequences of the six microsatellites and the ~2.2-kb surrounding sequences and observed that both phylogenies are congruent. At the interspecific level (8 species of primates: 54 individuals), we analyzed the sequence polymorphism and divergence of each orthologous locus for both the flanking sequence and the microsatellite. The results showed a lower divergence of flanking sequences than expected in noncoding DNA and a relative stability of the first nucleotides close to the microsatellite. The location of each CAIII locus in a Low Copy Repeated element containing duplicated VCX/Y genes (~1 kb) suggested that direct or indirect selection could explain these results. Moreover, the substitution rates in the flanking sequences and in the microsatellites were correlated. Thus, the evolutionary dynamics of microsatellites seems closely linked to the variation of spontaneous mutations in the surrounding regions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. SF Altschul W Gish W Miller EW Myers DJ Lipman (1990) ArticleTitleBLAST: Basic local alignment search tool. J Mol Biol 215 IssueID3 403–410 Occurrence Handle10.1006/jmbi.1990.9999 Occurrence Handle1:CAS:528:DyaK3MXitVGmsA%3D%3D Occurrence Handle2231712

    Article  CAS  PubMed  Google Scholar 

  2. N Archidiacono CT Storlazzi C Spalluto AS Ricco R Marzella M Rochi (1998) ArticleTitleEvolution of chromosome Y in primates. Chromosoma 107 241–246 Occurrence Handle10.1007/s004120050303 Occurrence Handle1:CAS:528:DyaK1cXlvF2itLs%3D Occurrence Handle9745049

    Article  CAS  PubMed  Google Scholar 

  3. A Ballabio B Bardoni S Guioli E Basler GA Camerino (1990) ArticleTitleTwo families of low-copy-number repeats are interspersed on Xp22.3: Implications for the high frequency of deletions in this region. Genomics 8 IssueID2 263–270 Occurrence Handle1:CAS:528:DyaK3MXhtFKjtbY%3D Occurrence Handle2249849

    CAS  PubMed  Google Scholar 

  4. WA Bickmore HJ Cooke (1987) ArticleTitleEvolution of homologous sequences on the human X and Y chromosomes, outside of the meiotic pairing segment. Nucleic Acids Res 15 IssueID15 6261–6271 Occurrence Handle1:CAS:528:DyaL2sXlsVygtb0%3D Occurrence Handle3502702

    CAS  PubMed  Google Scholar 

  5. J Brohede H Ellegren (1999) ArticleTitleMicrosatellite evolution: Polarity of substitutions within repeats and neutrality of flanking sequences. Proc R Soc Lond B Biol Sci 266 IssueID1421 825–833 Occurrence Handle10.1098/rspb.1999.0712 Occurrence Handle1:CAS:528:DyaK1MXjsVGnsbk%3D Occurrence Handle10343406

    Article  CAS  PubMed  Google Scholar 

  6. DR Carvalho-Silva SDJ Pena (2000) ArticleTitleMolecular characterization and population study of an X chromosome homolog of the Y-linked microsatellite DYS391. Gene 247 233–240 Occurrence Handle10.1016/S0378-1119(00)00085-8 Occurrence Handle1:CAS:528:DC%2BD3cXisV2kt7g%3D Occurrence Handle10773463

    Article  CAS  PubMed  Google Scholar 

  7. D Casane S Boissinot BHJ Chang LC Shimmin WH Li (1997) ArticleTitleMutation pattern variation among regions of the primate genome. J Mol Evol 45 216–226 Occurrence Handle1:CAS:528:DyaK2sXms1Cru7c%3D Occurrence Handle9302314

    CAS  PubMed  Google Scholar 

  8. FC Chen WH Li (2001) ArticleTitleGenomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am J Hum Genet 68 IssueID2 444–456

    Google Scholar 

  9. I Clisson M Lathuilliere B Crouau-Roy (2000) ArticleTitleConservation and evolution of microsatellite loci in primate taxa. Am J Primatol 50 IssueID3 205–214 Occurrence Handle10.1002/(SICI)1098-2345(200003)50:3<205::AID-AJP3>3.0.CO;2-Y Occurrence Handle1:CAS:528:DC%2BD3cXitVKrtrY%3D Occurrence Handle10711534

    Article  CAS  PubMed  Google Scholar 

  10. B Dutrillaux (1979) ArticleTitleChromosomal evolution in Primates: Tentative phylogeny from Microcebus murinus (Prosimian) to man. Hum Genet 48 251–314 Occurrence Handle1:STN:280:CSaB3sfht1A%3D Occurrence Handle112030

    CAS  PubMed  Google Scholar 

  11. I Ebersberger D Metzler C Schwartz S Pääbo (2002) ArticleTitleGenomewide comparsion of DNA sequences between humans and chimpanzees. Am J Hum Genet 70 1490–1497 Occurrence Handle10.1086/340787 Occurrence Handle1:CAS:528:DC%2BD38Xkt1SqsL4%3D Occurrence Handle11992255

    Article  CAS  PubMed  Google Scholar 

  12. JS Farris M Källersjo AG Kluge C Bull (1995) ArticleTitleTesting significance of incongruence. Cladistics 10 315–319 Occurrence Handle10.1006/clad.1994.1021

    Article  Google Scholar 

  13. NN FitzSimmons C Moritz SS Moore (1995) ArticleTitleConservation and dynamics of microsatellite loci over 300 million years of marine turtle evolution. Mol Biol Evol 12 IssueID3 432–440 Occurrence Handle1:CAS:528:DyaK2MXltF2ntbs%3D Occurrence Handle7739385

    CAS  PubMed  Google Scholar 

  14. M Fukami S Kirsch S Schiller A Richter V Benes B Franco K Muroya E Rao S Merker B Niesler A Ballabio W Ansorge T Ogata GA Rappold (2000) ArticleTitleA member of a gene family on Xp223, VCX-A, is deleted in patients with X-linked nonspecific mental retardation. Am J Hum Genet 67 IssueID3 563–573 Occurrence Handle10.1086/303047 Occurrence Handle1:CAS:528:DC%2BD3cXms1Wgsb4%3D Occurrence Handle10903929

    Article  CAS  PubMed  Google Scholar 

  15. D Higgins J Thompson T Gibson JD Thompson DG Higgins TJ Gibson (1994) ArticleTitleCLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 4673–4680 Occurrence Handle7984417

    PubMed  Google Scholar 

  16. LD Hurst JP Randerson (1999) ArticleTitleAn exceptional chromosome. Trends Genet 15 IssueID10 383–385 Occurrence Handle10.1016/S0168-9525(99)01809-0 Occurrence Handle1:CAS:528:DyaK1MXmsVWhsLg%3D Occurrence Handle10498931

    Article  CAS  PubMed  Google Scholar 

  17. T Karafet P de Knijff E Wood J Ragland A Clark MF Hammer (1998) ArticleTitleDifferent patterns of variation at the X- and Y-chromosome linked microsatellite loci DXYS156X and DXYS156Y in human populations. Hum Biol 70 979–992 Occurrence Handle1:STN:280:DyaK1M%2FktlSgsw%3D%3D Occurrence Handle9825590

    CAS  PubMed  Google Scholar 

  18. Y Kashi M Soller (1999) Functional roles of microsatellite and minisatellites. DB Goldstein C Schlötterer (Eds) Microsatellites: Evolution and applications. Oxford University Press Oxford 10–23

    Google Scholar 

  19. S Kumar K Tamura IB Jakobsen M Nei (2001) ArticleTitleMEGA2: Molecular Evolutionary Genetics analysis software. Bioinformatics 17 IssueID12 1244–1245 Occurrence Handle1:CAS:528:DC%2BD38XmtVCktQ%3D%3D Occurrence Handle11751241

    CAS  PubMed  Google Scholar 

  20. BT Lahn DC Page (1999) ArticleTitleFour evolutionary strata on the human X chromosome. Science 286 IssueID5441 964–967 Occurrence Handle10.1126/science.286.5441.964 Occurrence Handle1:CAS:528:DyaK1MXntFaqtrk%3D Occurrence Handle10542153

    Article  CAS  PubMed  Google Scholar 

  21. BT Lahn DC Page (2000) ArticleTitleA human sex-chromosomal gene family expressed in male germ cells and encoding variably charged proteins. Hum Mol Genet 9 IssueID2 311–319 Occurrence Handle10.1093/hmg/9.2.311 Occurrence Handle1:CAS:528:DC%2BD3cXhtVaksb4%3D Occurrence Handle10607842

    Article  CAS  PubMed  Google Scholar 

  22. B Lambson NA Affara M Mitchell MA Ferguson-Smith (1992) ArticleTitleEvolution of DNA sequence homologies between the sex chromosomes in primate species. Genomics 14 IssueID4 1032–1040 Occurrence Handle1:CAS:528:DyaK3sXhs1ahtrw%3D Occurrence Handle1478645

    CAS  PubMed  Google Scholar 

  23. D Liao (1999) ArticleTitleConcerted evolution: Molecular mechanism and biological implications. Am J Hum Genet 64 IssueID1 24–30 Occurrence Handle1:CAS:528:DyaK1MXht1emu7k%3D Occurrence Handle9915939

    CAS  PubMed  Google Scholar 

  24. P Malaspina BM Ciminelli L Viggiano C Jodice F Cruciani P Santolamazza D Sellitto R Scozzari L Terrenato M Rocchi A Novelletto (1997) ArticleTitleCharacterization of a small family (CAIII) of microsatellite-containing sequences with X-Y homology. J Mol Evol 44 IssueID6 652–659 Occurrence Handle1:CAS:528:DyaK2sXjslKjtro%3D Occurrence Handle9169558

    CAS  PubMed  Google Scholar 

  25. JA Marshall Graves ML Delbridge (2001) ArticleTitleThe X-a sexy chromosome. BioEssays 23 1091–1094 Occurrence Handle10.1002/bies.10026 Occurrence Handle11746227

    Article  PubMed  Google Scholar 

  26. HC Mefford BJ Trask (2002) ArticleTitleThe complex structure and dynamic evolution of human subtelomeres. Nat Rev Genet 3 IssueID2 91–102 Occurrence Handle1:CAS:528:DC%2BD38XhsV2ntrY%3D Occurrence Handle11836503

    CAS  PubMed  Google Scholar 

  27. W Messier SH Li CB Stewart (1996) ArticleTitleThe birth of microsatellites. Nature 381 483 Occurrence Handle1:CAS:528:DyaK28XjsVWis7o%3D Occurrence Handle8632820

    CAS  PubMed  Google Scholar 

  28. S Ohno (1970) Evolution by gene duplication. Springer-Verlag Berlin

    Google Scholar 

  29. RDM Page, (1996) ArticleTitleTREEVIEW: An application to display phylogenetic trees on personal computers. Comput Appl Biosci 12 357–358 Occurrence Handle1:STN:280:ByiD2MfgtlA%3D Occurrence Handle8902363

    CAS  PubMed  Google Scholar 

  30. C Rico I Rico G Hewitt (1996) ArticleTitle470 million years of conservation of microsatellite loci among fish species. Proc R Soc Lond B Biol Sci 263 IssueID1370 549–557 Occurrence Handle1:CAS:528:DyaK28XktlChsr4%3D Occurrence Handle8677258

    CAS  PubMed  Google Scholar 

  31. RV Samonte EE Eichler (2002) ArticleTitleSegmental duplications and the evolution of the primate genome. Nat Rev Genet 3 IssueID1 65–72 Occurrence Handle10.1038/nrg705 Occurrence Handle1:CAS:528:DC%2BD38XhsV2gt7s%3D Occurrence Handle11823792

    Article  CAS  PubMed  Google Scholar 

  32. MF Santibañez-Koref R Gangeswaran JM Hancock (2001) ArticleTitleA relationship between lengths of microsatellites and nearby substitution rates in mammalian genomes. Mol Biol Evol 18 IssueID11 2119–2123 Occurrence Handle11606708

    PubMed  Google Scholar 

  33. C Schlötterer (2000) ArticleTitleEvolutionary dynamics of microsatellite DNA. Chromosoma 109 IssueID6 365–371

    Google Scholar 

  34. DL Swofford (1998) PAUP*: Phylogenetic analysis using parsimony (*and other methods), Beta version 4.0. Sinauer Sunderland, MA

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire Evolution et Diversité Biologique, UMR 5174 Bat. IV R3, Université Paul Sabatier, 118 route de Narbonne, 31062 Toulouse Cedex 4, France

    Patricia Balaresque & Brigitte Crouau-Roy

  2. Laboratoire d’Anthropologie Biologique CNRS FRE2292, Musée de l’Homme, 17 place du Trocadéro, 75116 Paris, France

    Patricia Balaresque, Bruno Toupance & Evelyne Heyer

Authors
  1. Patricia Balaresque
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bruno Toupance
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Evelyne Heyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Brigitte Crouau-Roy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Patricia Balaresque.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Balaresque, P., Toupance, B., Heyer, E. et al. Evolutionary Dynamics of Duplicated Microsatellites Shared by Sex Chromosomes . J Mol Evol 57 (Suppl 1), S128–S137 (2003). https://doi.org/10.1007/s00239-003-0018-z

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-003-0018-z

Keywords

Search

Navigation