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. 1999 Jan;151(1):285–296. doi: 10.1093/genetics/151.1.285

Multiple levels of single-strand slippage at cetacean tri- and tetranucleotide repeat microsatellite loci.

P J Palsbøll 1, M Bérubé 1, H Jørgensen 1
PMCID: PMC1460447  PMID: 9872967

Abstract

Between three and six tri- and tetranucleotide repeat microsatellite loci were analyzed in 3720 samples collected from four different species of baleen whales. Ten of the 18 species/locus combinations had imperfect allele arrays, i.e., some alleles differed in length by other than simple integer multiples of the basic repeat length. The estimate of the average number of alleles and heterozygosity was higher at loci with imperfect allele arrays relative to those with perfect allele arrays. Nucleotide sequences of 23 different alleles at one tetranucleotide repeat microsatellite locus in fin whales, Balaenoptera physalus, and humpback whales, Megaptera novaeangliae, revealed sequence changes including perfect repeats only, multiple repeats, and partial repeats. The relative rate of the latter two categories of mutation was estimated at 0.024 of the mutation rate involving perfect repeats only. It is hypothesized that single-strand slippage of partial repeats may provide a mechanism for counteracting the continuous expansion of microsatellite loci, which is the logical consequence of recent reports demonstrating directional mutations. Partial-repeat mutations introduce imperfections in the repeat array, which subsequently could reduce the rate of single-strand slippage. Limited computer simulations confirmed this predicted effect of partial-repeat mutations.

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Selected References

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

  1. Amos W., Sawcer S. J., Feakes R. W., Rubinsztein D. C. Microsatellites show mutational bias and heterozygote instability. Nat Genet. 1996 Aug;13(4):390–391. doi: 10.1038/ng0896-390. [DOI] [PubMed] [Google Scholar]
  2. Angers B., Bernatchez L. Complex evolution of a salmonid microsatellite locus and its consequences in inferring allelic divergence from size information. Mol Biol Evol. 1997 Mar;14(3):230–238. doi: 10.1093/oxfordjournals.molbev.a025759. [DOI] [PubMed] [Google Scholar]
  3. Augusteyn R. C., Hum T. P., Putilin T. P., Thomson J. A. The location of sulphydryl groups in alpha-crystallin. Biochim Biophys Acta. 1987 Sep 2;915(1):132–139. doi: 10.1016/0167-4838(87)90133-6. [DOI] [PubMed] [Google Scholar]
  4. Bérubé M., Aguilar A., Dendanto D., Larsen F., Notarbartolo di Sciara G., Sears R., Sigurjónsson J., Urban-R J., Palsbøll P. J. Population genetic structure of North Atlantic, Mediterranean Sea and Sea of Cortez fin whales, Balaenoptera physalus (Linnaeus 1758): analysis of mitochondrial and nuclear loci. Mol Ecol. 1998 May;7(5):585–599. doi: 10.1046/j.1365-294x.1998.00359.x. [DOI] [PubMed] [Google Scholar]
  5. Bérubé M., Palsbøll P. Identification of sex in cetaceans by multiplexing with three ZFX and ZFY specific primers. Mol Ecol. 1996 Apr;5(2):283–287. doi: 10.1111/j.1365-294x.1996.tb00315.x. [DOI] [PubMed] [Google Scholar]
  6. Chakraborty R., Kimmel M., Stivers D. N., Davison L. J., Deka R. Relative mutation rates at di-, tri-, and tetranucleotide microsatellite loci. Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):1041–1046. doi: 10.1073/pnas.94.3.1041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chakraborty R., Weiss K. M. Genetic variation of the mitochondrial DNA genome in American Indians is at mutation-drift equilibrium. Am J Phys Anthropol. 1991 Dec;86(4):497–506. doi: 10.1002/ajpa.1330860405. [DOI] [PubMed] [Google Scholar]
  8. Di Rienzo A., Peterson A. C., Garza J. C., Valdes A. M., Slatkin M., Freimer N. B. Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3166–3170. doi: 10.1073/pnas.91.8.3166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Duyao M., Ambrose C., Myers R., Novelletto A., Persichetti F., Frontali M., Folstein S., Ross C., Franz M., Abbott M. Trinucleotide repeat length instability and age of onset in Huntington's disease. Nat Genet. 1993 Aug;4(4):387–392. doi: 10.1038/ng0893-387. [DOI] [PubMed] [Google Scholar]
  10. Eldridge G. D., St Lawrence J. S., Little C. E., Shelby M. C., Brasfield T. L. Barriers to condom use and barrier method preferences among low-income African-American women. Women Health. 1995;23(1):73–89. doi: 10.1300/J013v23n01_05. [DOI] [PubMed] [Google Scholar]
  11. Ellegren H., Primmer C. R., Sheldon B. C. Microsatellite 'evolution': directionality or bias? Nat Genet. 1995 Dec;11(4):360–362. doi: 10.1038/ng1295-360. [DOI] [PubMed] [Google Scholar]
  12. Estoup A., Tailliez C., Cornuet J. M., Solignac M. Size homoplasy and mutational processes of interrupted microsatellites in two bee species, Apis mellifera and Bombus terrestris (Apidae). Mol Biol Evol. 1995 Nov;12(6):1074–1084. doi: 10.1093/oxfordjournals.molbev.a040282. [DOI] [PubMed] [Google Scholar]
  13. Garza J. C., Freimer N. B. Homoplasy for size at microsatellite loci in humans and chimpanzees. Genome Res. 1996 Mar;6(3):211–217. doi: 10.1101/gr.6.3.211. [DOI] [PubMed] [Google Scholar]
  14. Garza J. C., Slatkin M., Freimer N. B. Microsatellite allele frequencies in humans and chimpanzees, with implications for constraints on allele size. Mol Biol Evol. 1995 Jul;12(4):594–603. doi: 10.1093/oxfordjournals.molbev.a040239. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Grimaldi M. C., Crouau-Roy B. Microsatellite allelic homoplasy due to variable flanking sequences. J Mol Evol. 1997 Mar;44(3):336–340. doi: 10.1007/pl00006151. [DOI] [PubMed] [Google Scholar]
  17. Gyllensten U. B., Erlich H. A. Generation of single-stranded DNA by the polymerase chain reaction and its application to direct sequencing of the HLA-DQA locus. Proc Natl Acad Sci U S A. 1988 Oct;85(20):7652–7656. doi: 10.1073/pnas.85.20.7652. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hudson R. R., Kaplan N. L. On the divergence of alleles in nested subsamples from finite populations. Genetics. 1986 Aug;113(4):1057–1076. doi: 10.1093/genetics/113.4.1057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jin L., Macaubas C., Hallmayer J., Kimura A., Mignot E. Mutation rate varies among alleles at a microsatellite locus: phylogenetic evidence. Proc Natl Acad Sci U S A. 1996 Dec 24;93(26):15285–15288. doi: 10.1073/pnas.93.26.15285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kimmel M., Chakraborty R., King J. P., Bamshad M., Watkins W. S., Jorde L. B. Signatures of population expansion in microsatellite repeat data. Genetics. 1998 Apr;148(4):1921–1930. doi: 10.1093/genetics/148.4.1921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kimmel M., Chakraborty R. Measures of variation at DNA repeat loci under a general stepwise mutation model. Theor Popul Biol. 1996 Dec;50(3):345–367. doi: 10.1006/tpbi.1996.0035. [DOI] [PubMed] [Google Scholar]
  22. Kimmel M., Chakraborty R., Stivers D. N., Deka R. Dynamics of repeat polymorphisms under a forward-backward mutation model: within- and between-population variability at microsatellite loci. Genetics. 1996 May;143(1):549–555. doi: 10.1093/genetics/143.1.549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kuhner M. K., Yamato J., Felsenstein J. Maximum likelihood estimation of population growth rates based on the coalescent. Genetics. 1998 May;149(1):429–434. doi: 10.1093/genetics/149.1.429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Levinson G., Gutman G. A. High frequencies of short frameshifts in poly-CA/TG tandem repeats borne by bacteriophage M13 in Escherichia coli K-12. Nucleic Acids Res. 1987 Jul 10;15(13):5323–5338. doi: 10.1093/nar/15.13.5323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Messier W., Li S. H., Stewart C. B. The birth of microsatellites. Nature. 1996 Jun 6;381(6582):483–483. doi: 10.1038/381483a0. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Moran P. A. Wandering distributions and the electrophoretic profile. Theor Popul Biol. 1975 Dec;8(3):318–330. doi: 10.1016/0040-5809(75)90049-0. [DOI] [PubMed] [Google Scholar]
  28. Ortí G., Pearse D. E., Avise J. C. Phylogenetic assessment of length variation at a microsatellite locus. Proc Natl Acad Sci U S A. 1997 Sep 30;94(20):10745–10749. doi: 10.1073/pnas.94.20.10745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Palsbøll P. J., Bérubé M., Larsen A. H., Jørgensen H. Primers for the amplification of tri- and tetramer microsatellite loci in baleen whales. Mol Ecol. 1997 Sep;6(9):893–895. doi: 10.1111/j.1365-294x.1997.tb00146.x. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. Rubinsztein D. C., Amos W., Leggo J., Goodburn S., Jain S., Li S. H., Margolis R. L., Ross C. A., Ferguson-Smith M. A. Microsatellite evolution--evidence for directionality and variation in rate between species. Nat Genet. 1995 Jul;10(3):337–343. doi: 10.1038/ng0795-337. [DOI] [PubMed] [Google Scholar]
  32. Schlötterer C., Tautz D. Slippage synthesis of simple sequence DNA. Nucleic Acids Res. 1992 Jan 25;20(2):211–215. doi: 10.1093/nar/20.2.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Shriver M. D., Jin L., Boerwinkle E., Deka R., Ferrell R. E., Chakraborty R. A novel measure of genetic distance for highly polymorphic tandem repeat loci. Mol Biol Evol. 1995 Sep;12(5):914–920. doi: 10.1093/oxfordjournals.molbev.a040268. [DOI] [PubMed] [Google Scholar]
  34. Shriver M. D., Jin L., Chakraborty R., Boerwinkle E. VNTR allele frequency distributions under the stepwise mutation model: a computer simulation approach. Genetics. 1993 Jul;134(3):983–993. doi: 10.1093/genetics/134.3.983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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]
  36. Talbot C. C., Jr, Avramopoulos D., Gerken S., Chakravarti A., Armour J. A., Matsunami N., White R., Antonarakis S. E. The tetranucleotide repeat polymorphism D21S1245 demonstrates hypermutability in germline and somatic cells. Hum Mol Genet. 1995 Jul;4(7):1193–1199. doi: 10.1093/hmg/4.7.1193. [DOI] [PubMed] [Google Scholar]
  37. Tautz D. Hypervariability of simple sequences as a general source for polymorphic DNA markers. Nucleic Acids Res. 1989 Aug 25;17(16):6463–6471. doi: 10.1093/nar/17.16.6463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Valdes A. M., Slatkin M., Freimer N. B. Allele frequencies at microsatellite loci: the stepwise mutation model revisited. Genetics. 1993 Mar;133(3):737–749. doi: 10.1093/genetics/133.3.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Valsecchi E., Palsbøll P., Hale P., Glockner-Ferrari D., Ferrari M., Clapham P., Larsen F., Mattila D., Sears R., Sigurjonsson J. Microsatellite genetic distances between oceanic populations of the humpback whale (Megaptera novaeangliae). Mol Biol Evol. 1997 Apr;14(4):355–362. doi: 10.1093/oxfordjournals.molbev.a025771. [DOI] [PubMed] [Google Scholar]
  40. Weber J. L., May P. E. Abundant class of human DNA polymorphisms which can be typed using the polymerase chain reaction. Am J Hum Genet. 1989 Mar;44(3):388–396. [PMC free article] [PubMed] [Google Scholar]
  41. Weber J. L., Wong C. Mutation of human short tandem repeats. Hum Mol Genet. 1993 Aug;2(8):1123–1128. doi: 10.1093/hmg/2.8.1123. [DOI] [PubMed] [Google Scholar]
  42. Zhivotovsky L. A., Feldman M. W. Microsatellite variability and genetic distances. Proc Natl Acad Sci U S A. 1995 Dec 5;92(25):11549–11552. doi: 10.1073/pnas.92.25.11549. [DOI] [PMC free article] [PubMed] [Google Scholar]

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