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Low mutation rates of microsatellite loci in Drosophila melanogaster

Abstract

Analysis of variation at microsatellite DNA loci is widely used in studies of parentage1, linkage2 and evolutionary history3–5. The utility of microsatel I ites is primarily due to high levels of allelic diversity, believed to reflect mutation rates orders of magnitude higher than base pair substitutions at single-copy genes. For humans6–14, mice15–16, rats17 and pigs18, microsatellite mutation rates have been estimated at 10−3–10−5. However, a recent study comparing microsatellite variation in humans with non-human primates suggests that microsatellite mutation rates may vary considerably across taxa19–20. We measured mutation rates of 24 microsatellite loci in mutation accumulation lines of Drosophila melanogaster. Surprisingly, only a single mutation was detected after screening 157,680 allele-generations, yielding an estimated average mutation rate per locus of 6.3 × 10−6, a mutation rate considerably lower than reported for various mammals. We propose that the comparatively low mutation rate is primarily a function of short microsatellite repeat lengths in the D. melanogaster genome.

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References

  1. Queller, D.C., Strassmann, J.E. & Hughes, C.R. Microsatellites and kinship. Trends Ecol. Evol. 8, 285–288 (1993).

    Article  CAS  PubMed  Google Scholar 

  2. Hearn, C.M., Ghosh, S. & Todd, J.A. Microsatellite for linkage analysis of genetic traits. Trends Genet. 8, 288–294 (1992).

    Article  Google Scholar 

  3. Goldstein, D.B., Linares, A.R., Cavalli-Sforza, L.L. & Feldman, M.W. Genetic absolute dating based on microsatellites and the origin of modern humans. Proc. Natl. Acad. Sci. USA 92, 6723–6727 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Roy, M.S., Geffen, E., Smith, D., Ostrander, E.A. & Wayne, R.K. Patterns of differentiation and hybridization in North American wolf like canids, revealed by analysis of microsatellite loci. Mol. BioL Evol. 11, 553–570 (1994).

    CAS  PubMed  Google Scholar 

  5. Bowcock, A.M. et al. High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368, 455–457 (1994).

    Article  CAS  PubMed  Google Scholar 

  6. Banchs, I. et al. New alleles at microsatellite loci in CEPH families mainly arise from somatic mutations in the lymphoblastoid cell lines. Hum. Mutat. 3, 365–372 (1994).

    Article  CAS  PubMed  Google Scholar 

  7. Edwards, A., Hammond, H.A., Jin, L., Caskey, C.T. & C hakraborty, R. Genetic variation at five trimeric and tetrameric repeat loci in four human population groups. Genomics 12, 241–253 (1992).

    Article  CAS  PubMed  Google Scholar 

  8. Hastbacka, J. et al. Linkage disequilibrium mapping in isolated founder populations: Diastrophic dysplasia in Finland. Nature Genet. 2, 204–211 (1992).

    Article  CAS  PubMed  Google Scholar 

  9. Kwiatowski, D.I. et al. Construction of a GT polymorphism map of human 9q. Genomics 12, 229–240 (1992).

    Article  Google Scholar 

  10. Bowcock, A. et al. Microsatellite polymorphism linkage map of human chromosome 13q. Genomics 15, 376–386 (1993).

    Article  CAS  PubMed  Google Scholar 

  11. Mahtani, M.M. & Willard, H.F. A polymporphic X-linked tetranucleotide repeat locus displaying a high rate of new mutation: implications for mechanisms of mutation at short tandem repeat loci. Hum. Mol. Genet. 2, 431–437 (1993).

    Article  CAS  PubMed  Google Scholar 

  12. Petrukhin, K.E. et al. A microsatellite genetic linkage map of human chromosome 13. Genomics 15, 76–85 (1993).

    Article  CAS  PubMed  Google Scholar 

  13. Straub, R.E. E. et al. A microsatellite genetic linkage map of human chromosome 18. Genomics 15, 48–56 (1993).

    Article  CAS  PubMed  Google Scholar 

  14. Weber, J.L. & Wong, C. Mutation of human short tandem repeats. Hum. Mol. Genet. 2, 1123–1128 (1993).

    Article  CAS  PubMed  Google Scholar 

  15. Deitrich, W. et al. A genetic map of the mouse suitable for typing intraspecific crosses. Genetics 131, 423–447 (1992).

    Google Scholar 

  16. Dallas, J.F. Estimation of microsatellite mutation rates in recombinant inbred strains of mouse. Mamm. Genome 3, 452–456 (1992).

    Article  CAS  PubMed  Google Scholar 

  17. Serikawa, T. et al. Rat gene mapping using PCR-analyzed microsatellites. Genetics 131, 701–721 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Ellegren, H. Mutation rates at porcine microsatellite loci. Mamm. Genome 6, 376–377 (1995).

    Article  CAS  PubMed  Google Scholar 

  19. Rubensztein, D.C. et al. Microsatellite evolution - evidence for directionality and variation in rate between species. Nature Genet. 10, 337–343 (1995).

    Article  Google Scholar 

  20. Dover, G. Slippery DNA runs on and on and on. Nature Genet. 10, 254–256 (1995).

    Article  CAS  PubMed  Google Scholar 

  21. Goldstein, D.B. & Clark, A.G. Microsatellite variation in North American populations of Drosophila melanogaster. Nucl. Acids Res. 23, 3882–3886 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. England, P.R., Briscoe, D.A. & Frankham, R. Microsatellite polymorphisms in a wild population of Drosophila melanogaster. Genet. Res. Camb. 67, 285–290 (1996).

    Article  CAS  Google Scholar 

  23. Kreitman, M. Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature 304, 412–417 (1983).

    Article  CAS  PubMed  Google Scholar 

  24. Singh, R.S. Population genetics and evolution of species related to Drosophila melanogaster. Annu. Rev. Genet. 23, 425–453 (1989).

    Article  CAS  PubMed  Google Scholar 

  25. Takahata, N., Satta, Y. & Klein, J. Divergence time and population size in the lineage leading to modern humans. Theor. Pop. Biol. 48, 198–221 (1995).

    Article  CAS  Google Scholar 

  26. Strand, M., Prolla, T.A., Liskay, R.M. & Petes, T.D. Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature 365, 274–275 (1993).

    Article  CAS  PubMed  Google Scholar 

  27. Mackay, T.F.C., Fry, J.D., Lyman, R.F. & Nuzhdin, S.V. Polygenic mutation in Drosophila melanogaster: estimates from response to selection of inbred strains. Genetics 136, 937–951 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Mackay, T.F.C., Lyman, R.T. & Hill, W.G. Polygenic mutation in Drosophila melanogaster:non-linear divergence among unselected strains. Genetics 139, 849–859 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Nuzhdin, S.V. & Mackay, T.F.C. Direct determination of retrotransposon transposition rates in Drosophila melanogaster. Genet. Res. Camb. 63, 139–144 (1994).

    Article  CAS  Google Scholar 

  30. Chang, H.-J., Shimmin, L.C., Shyue, S.-K., Hewett-Emmet, D. & Li, W.-H. Weak male-driven molecular evolution in rodents. Proc. Natl. Acad. Sci. USA 91, 827–831 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Lin, H. & Spradling, A.C. Germline stem cell division and egg chamber development in transplanted Drosophila germaria. Dev. Biol. 159, 140–152 (1993).

    Article  CAS  PubMed  Google Scholar 

  32. Mahowald, A.P. & Kambysellis, M. Oogenesis in The Genetics and Biology of Drosophila. 141–225 (Volume 2d. Academic Press, New York, 1980).

    Google Scholar 

  33. Cooper, K.W. Normal spermatogenesis in Drosophila. in The Biology of Drosophila. (ed. Demerec, M.) 1–61 (John Wiley & Sons, Inc. New York, 1950).

  34. Sonnenblick, B.P. The early embryology of Drosophila melanogaster in The Biology of Drosophila. (ed. Demerec, M.) 62–167 (John Wiley & Sons, Inc. New York, 1950).

  35. Weber, J.L. Informativeness of human (dC-dA)n. (dG-dT)n polymorphisms. Genomics 7, 524–530 (1990).

    Article  CAS  PubMed  Google Scholar 

  36. Gloor, G.B. et al. Type I repressers of P element mobility. Genetics 135, 81–95 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Casella, G. & Berger, R.L. Statistical Inference.(Duxbury Press, Belmont, California 1992).

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Schug, M., Mackay, T. & Aquadro, C. Low mutation rates of microsatellite loci in Drosophila melanogaster. Nat Genet 15, 99–102 (1997). https://doi.org/10.1038/ng0197-99

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