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. 1999 Jul;152(3):1057–1063. doi: 10.1093/genetics/152.3.1057

Clustered microsatellite mutations in the pipefish Syngnathus typhle.

A G Jones 1, G Rosenqvist 1, A Berglund 1, J C Avise 1
PMCID: PMC1460651  PMID: 10388824

Abstract

Clustered mutations are copies of a mutant allele that enter a population's gene pool together due to replication from a premeiotic germline mutation and distribution to multiple successful gametes of an individual. Although the phenomenon has been studied in Drosophila and noted in a few other species, the topic has received scant attention despite claims of being of major importance to population genetics theory. Here we capitalize upon the reproductive biology of male-pregnant pipefishes to document the occurrence of clustered microsatellite mutations and to estimate their rates and patterns from family data. Among a total of 3195 embryos genetically screened from 110 families, 40% of the 35 detected de novo mutant alleles resided in documented mutational clusters. Most of the microsatellite mutations appeared to involve small-integer changes in repeat copy number, and they arose in approximately equal frequency in paternal and maternal germlines. These findings extend observations on clustered mutations to another organismal group and motivate a broader critique of the mutation cluster phenomenon. They also carry implications for the evolution of microsatellites with respect to mutational models and homoplasy among alleles.

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Selected References

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  1. 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]
  2. Bunyan D. J., Robinson D. O., Collins A. L., Cockwell A. E., Bullman H. M., Whittaker P. A. Germline and somatic mosaicism in a female carrier of Duchenne muscular dystrophy. Hum Genet. 1994 May;93(5):541–544. doi: 10.1007/BF00202820. [DOI] [PubMed] [Google Scholar]
  3. Dallas J. F. Estimation of microsatellite mutation rates in recombinant inbred strains of mouse. Mamm Genome. 1992;3(8):452–456. doi: 10.1007/BF00356155. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Edwards J. H. Familiarity, recessivity and germline mosaicism. Ann Hum Genet. 1989 Jan;53(Pt 1):33–47. doi: 10.1111/j.1469-1809.1989.tb01120.x. [DOI] [PubMed] [Google Scholar]
  6. Ehling U. H., Neuhäuser-Klaus A. Induction of specific-locus and dominant lethal mutations in male mice by chlormethine. Mutat Res. 1989 Oct;227(2):81–89. doi: 10.1016/0165-7992(89)90002-x. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Giltay J. C., Brunt T., Beemer F. A., Wit J. M., van Amstel H. K., Pearson P. L., Wijmenga C. Polymorphic detection of a parthenogenetic maternal and double paternal contribution to a 46,XX/46,XY hermaphrodite. Am J Hum Genet. 1998 Apr;62(4):937–940. doi: 10.1086/301796. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Green A. J., Barton D. E., Jenks P., Pearson J., Yates J. R. Chimaerism shown by cytogenetics and DNA polymorphism analysis. J Med Genet. 1994 Oct;31(10):816–817. doi: 10.1136/jmg.31.10.816. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Huai H., Woodruff R. C. Clusters of identical new mutations can account for the "overdispersed" molecular clock. Genetics. 1997 Sep;147(1):339–348. doi: 10.1093/genetics/147.1.339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Jones A. G., Avise J. C. Microsatellite analysis of maternity and the mating system in the Gulf pipefish Syngnathus scovelli, a species with male pregnancy and sex-role reversal. Mol Ecol. 1997 Mar;6(3):203–213. doi: 10.1046/j.1365-294x.1997.00173.x. [DOI] [PubMed] [Google Scholar]
  13. Jones A. G., Kvarnemo C., Moore G. I., Simmons L. W., Avise J. C. Microsatellite evidence for monogamy and sex-biased recombination in the Western Australian seahorse Hippocampus angustus. Mol Ecol. 1998 Nov;7(11):1497–1505. doi: 10.1046/j.1365-294x.1998.00481.x. [DOI] [PubMed] [Google Scholar]
  14. Kelly R., Gibbs M., Collick A., Jeffreys A. J. Spontaneous mutation at the hypervariable mouse minisatellite locus Ms6-hm: flanking DNA sequence and analysis of germline and early somatic mutation events. Proc Biol Sci. 1991 Sep 23;245(1314):235–245. doi: 10.1098/rspb.1991.0115. [DOI] [PubMed] [Google Scholar]
  15. Mason J. M., Valencia R., Woodruff R. C., Zimmering S. Genetic drift and seasonal variation in spontaneous mutation frequencies in Drosophila. Environ Mutagen. 1985;7(5):663–676. doi: 10.1002/em.2860070506. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. Schreider E. A new mutant gene possibly carried simultaneously by two distinct gametes. J Med Genet. 1969 Dec;6(4):442–442. doi: 10.1136/jmg.6.4.442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Schug M. D., Mackay T. F., Aquadro C. F. Low mutation rates of microsatellite loci in Drosophila melanogaster. Nat Genet. 1997 Jan;15(1):99–102. doi: 10.1038/ng0197-99. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. Vogel F., Rathenberg R. Spontaneous mutation in man. Adv Hum Genet. 1975;5:223–318. doi: 10.1007/978-1-4615-9068-2_4. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Woodruff R. C., Huai H., Thompson J. N., Jr Clusters of identical new mutation in the evolutionary landscape. Genetica. 1996 Oct;98(2):149–160. doi: 10.1007/BF00121363. [DOI] [PubMed] [Google Scholar]
  25. Zlotogora J. Germ line mosaicism. Hum Genet. 1998 Apr;102(4):381–386. doi: 10.1007/s004390050708. [DOI] [PubMed] [Google Scholar]

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