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A high incidence of clustered microsatellite mutations revealed by parent-offspring analysis in the African freshwater snail, Bulinus forskalii (Gastropoda, Pulmonata)

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Abstract

Genotyping of 11 microsatellites in 432 offspring from 28 families of the hermaphroditic, freshwater snail Bulinus forskalii detected 10 de novo mutant alleles. This gave an estimated mutation rate of 1.1 × 10−3 per locus per gamete per generation. There was a trend towards repeat length expansion and, unlike most studies, multi-step mutations predominated, suggesting that the microsatellite mutation process does not conform to a strict stepwise mutation model. Interestingly, the ten mutant alleles appear to have arisen from only six independent germline mutation events within the microsatellite array, with seven of them residing in three mutational clusters. Our results extend observations of clustered microsatellite mutations to another taxonomic group and type of mating system, self-fertile gastropods, and provide compelling evidence of premeiotic germline mutations, a phenomenon that could greatly impact upon our understanding of mutation dynamics but which has received little attention.

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References

  • D.S. Brown (1994) Freshwater Snails of Africa and Their Medical Importance Taylor and Francis Ltd. London

    Google Scholar 

  • R.H. Crozier B. Kaufmann M.E. Carew Y.C. Crozier (1999) ArticleTitleMutability of microsatellites developed for the ant Camponotus consobrinus Mol. Ecol. 8 271–276 Occurrence Handle10.1046/j.1365-294X.1999.00565.x Occurrence Handle1:CAS:528:DyaK1MXjtVOgu7s%3D Occurrence Handle10065542

    Article  CAS  PubMed  Google Scholar 

  • A. Di Rienzo P. Donnelly C. Toomajian B. Sisk A. Hill M.L. Petzl-Erler G.K. Haines D.H. Barch (1998) ArticleTitleHeterogeneity of microsatellite mutations within and between loci, and implications for human demographic histories Genetics 148 1269–1284 Occurrence Handle1:CAS:528:DyaK1cXks1eitLo%3D Occurrence Handle9539441

    CAS  PubMed  Google Scholar 

  • J.H. Edwards (1989) ArticleTitleFamiliarity, recessivity and germline mosaicism Ann. Hum. Genet. 53 33–47 Occurrence Handle2658737

    PubMed  Google Scholar 

  • J.A. Eisen (1999) Mechanistic basis for microsatellite instability D.B. Goldstein C. Schlötterer (Eds) Microsatellites: Evolution and Application Oxford University Press Oxford 34–48

    Google Scholar 

  • H. Ellegren (2000) ArticleTitleHeterogeneous mutation processes in human microsatellite DNA sequences Nat. Genet 24 400–402 Occurrence Handle10.1038/74249 Occurrence Handle1:CAS:528:DC%2BD3cXisVCjtr4%3D Occurrence Handle10742106

    Article  CAS  PubMed  Google Scholar 

  • H. Ellegren (2004) ArticleTitleMicrosatellites: simple sequences with complex evolution Nat. Rev. Genet. 5 435–445 Occurrence Handle10.1038/nrg1348 Occurrence Handle1:CAS:528:DC%2BD2cXktV2rsrg%3D Occurrence Handle15153996

    Article  CAS  PubMed  Google Scholar 

  • N.N. FitzSimmons (1998) ArticleTitleSingle paternity of clutches and sperm storage in the promiscuous green turtle (Chelonia mydas) Mol. Ecol 7 575–584 Occurrence Handle10.1046/j.1365-294x.1998.00355.x Occurrence Handle1:STN:280:DyaK1c3ps1OmtQ%3D%3D Occurrence Handle9633101

    Article  CAS  PubMed  Google Scholar 

  • L. Florea G. Hartzell Z. Zhang G.M. Rubin W. Miller (1998) ArticleTitleA computer program for aligning a cDNA sequence with a genomic DNA sequence Genome Res 8 967–974 Occurrence Handle1:CAS:528:DyaK1cXmsVWnt74%3D Occurrence Handle9750195

    CAS  PubMed  Google Scholar 

  • M.G. Gardner C.M. Bull J.B. Cooper G.A. Duffield (2000) ArticleTitleMicrosatellite mutations in litters of the Australian lizard Egernia stokesii J. Evolution. Biol 13 551–560 Occurrence Handle10.1046/j.1420-9101.2000.00189.x

    Article  Google Scholar 

  • Gow, J.L., L.R. Noble, D. Rollinson, L.-A. Tchuem Tchuente & C.S. Jones. High levels of selfing are revealed by a parent-offspring analysis of the medically important freshwater snail, Bulinus forskalii (Gastropoda, pulmonata). J. Mollus. Stud. (in press)

  • J.L. Gow L.R. Noble D. Rollinson C.S. Jones (2001) ArticleTitlePolymorphic microsatellites in the African freshwater snail, Bulinus forskalii (Gastropoda, Pulmonata) Mol. Ecol. Notes 1 237–240 Occurrence Handle1:CAS:528:DC%2BD38XltVGlug%3D%3D

    CAS  Google Scholar 

  • B. Harr J. Todorova C. Schlötterer (2002) ArticleTitleMismatch repair-driven mutational bias in D. melanogaster Mol. Cell 10 199–205 Occurrence Handle10.1016/S1097-2765(02)00575-0 Occurrence Handle1:CAS:528:DC%2BD38XmtFakur4%3D Occurrence Handle12150919

    Article  CAS  PubMed  Google Scholar 

  • W.E.J. Hoekert H. Neuféglise A.D. Schouten S.B.J. Menken (2002) ArticleTitleMultiple paternity and female-biased mutation at a microsatellite locus in the olive ridley sea turtle (Lepidochelys olivacea) Heredity 89 107–113 Occurrence Handle10.1038/sj.hdy.6800103 Occurrence Handle1:CAS:528:DC%2BD38XlsVKqtL8%3D Occurrence Handle12136412

    Article  CAS  PubMed  Google Scholar 

  • H. Huai R.C. Woodruff (1997) ArticleTitleClusters of identical new mutations can account for the ‘overdispersed’ molecular clock Genetics 147 339–348 Occurrence Handle1:STN:280:ByiH3s3otFc%3D Occurrence Handle9286693

    CAS  PubMed  Google Scholar 

  • A.G. Jones G. Rosenqvist A. Berglund J.C. Avise (1999) ArticleTitleClustered microsatellite mutations in the pipefish Syngnathus typhle Genetics 152 1057–1063 Occurrence Handle1:CAS:528:DyaK1MXltVWnsLk%3D Occurrence Handle10388824

    CAS  PubMed  Google Scholar 

  • G. Levinson G.A. Gutman (1987) ArticleTitleSlipped-strand mispairing: a major mechanism for DNA sequence evolution Mol. Biol. Evol 4 203–221 Occurrence Handle1:CAS:528:DyaL2sXksFejsLw%3D Occurrence Handle3328815

    CAS  PubMed  Google Scholar 

  • M. Mackiewicz D.E. Fletcher S.D. Wilkins J.A. DeWoody J.C. Avise (2002) ArticleTitleA genetic assessment of parentage in a natural population of dollar sunfish (Lepomis marginatus) based on microsatellite markers Mol. Ecol 11 1877–1883 Occurrence Handle10.1046/j.1365-294X.2002.01577.x Occurrence Handle1:CAS:528:DC%2BD38XnvVWht74%3D Occurrence Handle12207736

    Article  CAS  PubMed  Google Scholar 

  • T. Ohta M. Kimura (1973) ArticleTitleThe model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a genetic population Genet. Res 22 201–204 Occurrence Handle4777279

    PubMed  Google Scholar 

  • S. Otto I.M. Hastings (1998) ArticleTitleMutation and selection within the individual Genetics 102–103 507–524

    Google Scholar 

  • J.M. Pemberton J. Slate D.R. Bancroft J.A. Barrett (1995) ArticleTitleNonamplifying alleles at microsatellite loci: a caution for parentage and population studies Mol. Ecol. 4 249–252 Occurrence Handle1:STN:280:ByqB2Mzkslw%3D Occurrence Handle7735527

    CAS  PubMed  Google Scholar 

  • M.D. Schug T.F.C. Mackay C.F. Aquadro (1997) ArticleTitleLow mutation rates of microsatellite loci in Drosophila melanogaster Nat. Genet 15 99–102 Occurrence Handle10.1038/ng0197-99 Occurrence Handle1:CAS:528:DyaK2sXjsFGrug%3D%3D Occurrence Handle8988178

    Article  CAS  PubMed  Google Scholar 

  • E.K. Steinberg K.R. Lindner J. Gallea A. Maxwell J. Meng F.W. Allendorf (2002) ArticleTitleRates and Patterns of microsatellite mutations in pink salmon Mol. Biol. Evol 19 1198–1202 Occurrence Handle1:CAS:528:DC%2BD38Xlt1aktbw%3D Occurrence Handle12082138

    CAS  PubMed  Google Scholar 

  • P. Taberlet S. Griffin B. Goossens S. Questiau V. Manceau N. Escaravage L.P. Waits J. Bouvet (1996) ArticleTitleReliable genotyping of samples with very low DNA quantities using PCR Nucleic Acids Res. 24 3189–3194 Occurrence Handle10.1093/nar/24.16.3189 Occurrence Handle1:CAS:528:DyaK28XlslyrtLs%3D Occurrence Handle8774899

    Article  CAS  PubMed  Google Scholar 

  • J.N. Thompson SuffixJr. R.C. Woodruff H. Huai (1998) ArticleTitleMutation rate: a simple concept has become complex Environ. Mol. Mutagen. 32 292–300 Occurrence Handle10.1002/(SICI)1098-2280(1998)32:4<292::AID-EM2>3.0.CO;2-V Occurrence Handle1:CAS:528:DyaK1MXhvV2ksg%3D%3D Occurrence Handle9882003

    Article  CAS  PubMed  Google Scholar 

  • F. Vogel R. Rathenberg (1975) Spontaneous mutations in man H. Harris K. Hirschhorn (Eds) Advances in Human Genetics Plenum Press New York 223–318

    Google Scholar 

  • R. Wattier C.R. Engel P. Saumitou-Laprade M. Valero (1998) ArticleTitleShort allele dominance as a source of heterozygote deficiency at microsatellite loci: experimental evidence at the dinucleotide locus Gv1CT in Gracilaria gracilis (Rhodophyta) Mol. Ecol. 7 1569–1573 Occurrence Handle10.1046/j.1365-294x.1998.00477.x Occurrence Handle1:CAS:528:DyaK1cXnsFSgtLk%3D

    Article  CAS  Google Scholar 

  • J.L. Weber C. Wong (1993) ArticleTitleMutation of human short tandem repeats Hum. Mol. Genet. 2 1123–1128 Occurrence Handle1:CAS:528:DyaK3sXmsValsrY%3D Occurrence Handle8401493

    CAS  PubMed  Google Scholar 

  • J. Weissenbach G. Gyapay C. Dib A. Vignal J. Morissette P. Millasseau G. Vaysseix M. Lathrop (1992) ArticleTitleA second-generation linkage map of the human genome Nature 359 794–801 Occurrence Handle10.1038/359794a0 Occurrence Handle1:CAS:528:DyaK38XmsVKnuro%3D Occurrence Handle1436057

    Article  CAS  PubMed  Google Scholar 

  • M. Wierdl M. Dominska T.D. Petes (1997) ArticleTitleMicrosatellite instability in yeast: dependence on the length of the microsatellite Nature 146 769–779 Occurrence Handle1:CAS:528:DyaK2sXmsVartLw%3D

    CAS  Google Scholar 

  • R.C. Woodruff H. Huai J.N. Thompson (1996) ArticleTitleClusters of identical new mutation in the evolutionary landscape Genetica 98 149–160 Occurrence Handle10.1007/BF00121363 Occurrence Handle1:STN:280:ByiC3s%2FisVY%3D Occurrence Handle8976063

    Article  CAS  PubMed  Google Scholar 

  • R.C. Woodruff J.N. Thompson (1992) ArticleTitleHave premeiotic clusters of mutation been overlooked in evolutionary theory? J. Evolution. Biol 5 457–464 Occurrence Handle10.1046/j.1420-9101.1992.5030457.x

    Article  Google Scholar 

  • R.C. Woodruff J.N. Thompson S. Gu (1992) ArticleTitlePremeiotic clusters of mutation and the cost of natural selection J. Hered. 95 277–283 Occurrence Handle10.1093/jhered/esh048

    Article  Google Scholar 

  • N.A. Yamada G.A. Smith A. Castro C.N. Roques J.C. Boyer R.A. Farber (2002) ArticleTitleRelative rates of insertion and deletion mutations in dinucleotide repeats of various lengths in mismatch repair proficient mouse and mismatch repair deficient human cells Mutat. Res. – Fund. Mol. M. 499 213–225 Occurrence Handle1:CAS:528:DC%2BD38XhtVKltbw%3D

    CAS  Google Scholar 

  • G.H. Yue P. Beckmann H. Geldermann (2002) ArticleTitleMutation rate at swine microsatellite loci Genetica 114 113–119 Occurrence Handle10.1023/A:1015189921578 Occurrence Handle1:CAS:528:DC%2BD38XksFSktL0%3D Occurrence Handle12041824

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Jennifer L. Gow.

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Gow, J.L., Noble, L.R., Rollinson, D. et al. A high incidence of clustered microsatellite mutations revealed by parent-offspring analysis in the African freshwater snail, Bulinus forskalii (Gastropoda, Pulmonata). Genetica 124, 77–83 (2005). https://doi.org/10.1007/s10709-005-0204-6

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