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The Fundamental Theorem of Neutral Evolution: Rates of Substitution and Mutation Should Factor in Premeiotic Clusters

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Abstract

Mutations do not always arise as single events. Many new mutations actually occur in the cell lineage before germ cell formation or meiosis and are therefore replicated premeiotically. The increased likelihood of substitutions caused by these clusters of new mutant alleles can change the fundamental theorem of neutral evolution.

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References

  • A. Bernards J.J. Gusella (1994) ArticleTitleThe importance of genetic mosaicism in human disease New Engl. J. Med. 331 1447–1449 Occurrence Handle10.1056/NEJM199411243312110 Occurrence Handle7969285

    Article  PubMed  Google Scholar 

  • M. Borgerhoff Mulder (1988) Reproductive success in three Kipsigis cohorts T.H. Clutton-Brock (Eds) Reproductive Success University of Chicago Press Chicago 419–435

    Google Scholar 

  • P.J. Bridges (1994) The Calculation of Genetic Risks The Johns Hopkins University Press Baltimore

    Google Scholar 

  • C.H. Buzin J. Feng J. Yan W. Scaringe Q. Liu L. Dunnen Particleden J.R. Mendell S.S. Sommer (2005) ArticleTitleMutation rates in the dystrophin gene: a hotspot of mutation at a CpG dinucleotide Hum. Mutat. 25 177–188 Occurrence Handle10.1002/humu.20132 Occurrence Handle15643612

    Article  PubMed  Google Scholar 

  • W.E. Castle (1905) ArticleTitleThe mutation theory of organic evolution: from the standpoint of animal breeding Science 21 521–525

    Google Scholar 

  • W.E. Castle (1929) ArticleTitleA mosaic (intense-dilute) coat pattern in the rabbit J. Exp. Zool. 52 471–480 Occurrence Handle10.1002/jez.1400520306

    Article  Google Scholar 

  • F.C. Chen W.H. 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. 68 444–456 Occurrence Handle10.1086/318206 Occurrence Handle11170892

    Article  PubMed  Google Scholar 

  • R.D. Cooper M. Krawczak (1993) Human Gene Mutation Bios Scientific Publishers, Limited Oxford

    Google Scholar 

  • J.F. Crow (1991) Alternative theories of molecular evolution E. C. Dudley (Eds) The Unity of Evolutionary Biology Dioscorides Press Portland 852–864

    Google Scholar 

  • T. Dobzhansky S. Wright (1941) ArticleTitleGenetics of natural populations.V.Relations between mutation rate and accumulation of lethals in populations of Drosophila pseudoobscura Genetics 26 23–51

    Google Scholar 

  • J.W. Drake B. Charlesworth C. Charlesworth J.F. Crow (1998) ArticleTitleRates of spontaneous mutation Genetics 148 1667–1686 Occurrence Handle9560386

    PubMed  Google Scholar 

  • J.B. Drost W.R. Lee (1995) ArticleTitleBiological basis of germline mutation: comparisons of spontaneous germline mutation rates among Drosophila, mouse and human Environ. Mol. Mutagen 25 48–64 Occurrence Handle7789362

    PubMed  Google Scholar 

  • J.B. Drost W.R. Lee (1998) ArticleTitleThe developmental basis for germline mosaicism in mouse and Drosophila melanogaster Genetica 102/103 421–443 Occurrence Handle10.1023/A:1017002221520

    Article  Google Scholar 

  • I. Dupanloup L. Pereira G. Bertorelle R. Calafell M.J. Prata A. Amorim G. Barbujani (2003) ArticleTitleA recent shift from polygyny to monogamy in humans is suggested by the analysis of worldwide Y-chromosome diversity J. Mol. Evol. 57 85–97 Occurrence Handle10.1007/s00239-003-2458-x Occurrence Handle12962309

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • M.J. Edwards R.J. Wenstrup P.H. Byers D.H. Cohn (1992) ArticleTitleRecurrence of lethal osteogenesis imperfecta due to a parental mosaicism for a mutation in the COL1A2 gene of type I collagen: the mosaic parent exhibits phenotypic features of a mild form of the disease Hum. Mut. 1 47–54 Occurrence Handle10.1002/humu.1380010108 Occurrence Handle1301191

    Article  PubMed  Google Scholar 

  • A. Eyre-Walker P.D. Keightley (1999) ArticleTitleHigh genomic deleterious mutation rates in hominids Nature 397 344–346 Occurrence Handle10.1038/16915 Occurrence Handle9950425

    Article  PubMed  Google Scholar 

  • D.S. Falconer (1951) ArticleTitleTwo new mutants, ‘trembler’ and ‘reeler’, with neurological actions in the house mouse (Mus musculus L.) J. Genet 50 192–201

    Google Scholar 

  • R.A. Fisher (1930) The Genetical Theory of Natural Selection Clarendon Press Oxford

    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 Handle9633101

    Article  PubMed  Google Scholar 

  • R.A. Fisher (1930a) ArticleTitleNote on a tricolour (mosaic) mouse J. Genet 23 77–81

    Google Scholar 

  • Y.X. Fu H. Huai (2003) ArticleTitleEstimating mutation rate: how to count mutations? Genetics 164 797–805 Occurrence Handle12807798

    PubMed  Google Scholar 

  • F. Giannelli T.P.M. Anagnostopoulos Green (1999) ArticleTitleMutation rates in humans. II. Sporadic mutation-specific rates and rate of detrimental human mutations inferred from Hemophilia B Am. J. Hum. Genet. 65 1580–1587 Occurrence Handle10.1086/302652 Occurrence Handle10577911

    Article  PubMed  Google Scholar 

  • J.B.S. Haldane (1935) ArticleTitleThe rate of spontaneous mutation of a human gene J. Genet. 31 317–326

    Google Scholar 

  • J.B.S. Haldane (1947) ArticleTitleThe mutation rate of the gene for haemophilia and its segregation rations in males and females Ann. Eugenics 13 262–271

    Google Scholar 

  • J.G. Hall (1988) ArticleTitleSomatic mosaicism: observations related to clinical genetics Am. J. Hum. Genet. 43 355–363 Occurrence Handle3052049

    PubMed  Google Scholar 

  • D.L. Hartl (1971) ArticleTitleRecurrence risks for germinal mosaics Am. J. Hum. Genet 23 124–134 Occurrence Handle5092478

    PubMed  Google Scholar 

  • W.E.J. Hoekert H. Neufeglise A.D. Schouten S.B.J. Menden (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 Handle12136412

    Article  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 Handle9286693

    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 Handle10388824

    PubMed  Google Scholar 

  • A.G. Jones J.C. Avise (2001) ArticleTitleMating systems and sexual selection in male-pregnant pipefishes and seahorses: Insights from microsatellite-based studies of maternity J. Hered. 92 150–158 Occurrence Handle10.1093/jhered/92.2.150 Occurrence Handle11396573

    Article  PubMed  Google Scholar 

  • M. Kimura (1968) ArticleTitleEvolutionary rate at the molecular level Nature 217 624–626 Occurrence Handle5637732

    PubMed  Google Scholar 

  • M. Kimura (1983) The Neutral Theory of Molecular Evolution Cambridge University Press Cambridge

    Google Scholar 

  • A.S. Kondrashov (2002) ArticleTitleDirect estimates of human per nucleotide mutation rates at 20 loci causing Mendelian diseases Hum. Mut. 21 12–27 Occurrence Handle10.1002/humu.10147

    Article  Google Scholar 

  • M. Leur J. Oldenburg J. Lavergne M. Ludwig A. Fregin A. Eigel R. Ljung A. Goodeve I. Peake K. Olek (2001) ArticleTitleSomatic mosaicism in hemophilia A: a fairly common event Am. J. Hum. Genet. 69 75–87 Occurrence Handle10.1086/321285 Occurrence Handle11410838

    Article  PubMed  Google Scholar 

  • J.W. MacCluer J.V. Neel N.A. Chagnon (1971) ArticleTitleDemographic structure of a primitive population: a simulation Am. J. Phys. Anthropol. 35 193–207 Occurrence Handle5120561

    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) basesd on microsatellite markers Mol. Ecol. 11 1877–1883 Occurrence Handle10.1046/j.1365-294X.2002.01577.x Occurrence Handle12207736

    Article  PubMed  Google Scholar 

  • T.H. Morgan C.B. Bridges A.H. Sturtevant (1925) The Genetics of Drosophila M. Nijhoff s-Gravenhage

    Google Scholar 

  • M. Mottes M.M.G. Lira M. Valli G. Scarano F. Lonardo A. Forlino G. Cetta P.F. Pignatti (1993) ArticleTitlePaternal mosaicism for a COL1A1 dominant mutation (α1 Ser-415) causes recurrent osteogenesis imperfecta Hum. Mut. 2 196–204 Occurrence Handle10.1002/humu.1380020308 Occurrence Handle8364588

    Article  PubMed  Google Scholar 

  • H.J. Muller (1920) ArticleTitleFurther changes in the white-eye series of Drosophila and their bearing on the manner of occurrence of mutation J. Exp. Zool. 31 443–472 Occurrence Handle10.1002/jez.1400310405

    Article  Google Scholar 

  • H.J. Muller (1956) ArticleTitleFurther studies bearing on the load of mutations in man Acta Genetica et Statistica Medica 6 157–168 Occurrence Handle13410478

    PubMed  Google Scholar 

  • H.J. Muller I.I. Oster & Zimmering (1963) Are chronic and acute gamma irradiation equally mutagenic in Drosophila? F.H. Sobels (Eds) Repair from Genetic Radiation Damage and Differential Radiosensitivity in Germ Cells Pergamon Press Oxford 275–311

    Google Scholar 

  • N.W. Nachman S.L. Crowell (2000) ArticleTitleEstimate of the mutation rate per nucleotide in humans Genetics 156 297–304 Occurrence Handle10978293

    PubMed  Google Scholar 

  • N.W. Namikawa K. Suzumori Y. Kukushima M. Sasaki A. Hata (1995) ArticleTitleRecurrence of osteogenesis imperfecta because of paternal mosaicism: Gly862−>Ser substitution in a type I collagen gene (COL1A1) Hum. Genet 95 666–670 Occurrence Handle10.1007/BF00209484 Occurrence Handle7789952

    Article  PubMed  Google Scholar 

  • J.V. Neel (1993) Human consanguinity effects revisited: why is the measurable impact of inbreeding so small? C.F. Sing C.L. Manis (Eds) Genetics of Cellular, Individual, Family and Population Variability, Hanis Oxford University Press New York 58–82

    Google Scholar 

  • J.V. Neel (1998) ArticleTitleReappraisal of studies concerning the genetic effects of the radiation of humans, mice, and Drosophila Environ. Mol. Mutagen 31 4–10 Occurrence Handle10.1002/(SICI)1098-2280(1998)31:1<4::AID-EM2>3.0.CO;2-O Occurrence Handle9464310

    Article  PubMed  Google Scholar 

  • J.V. Neel E.D. Rothman (1978) ArticleTitleIndirect estimates of mutation rates in tribal Amerindians Proc. Nat. Acad. Sci. USA 75 5585–5588 Occurrence Handle281707

    PubMed  Google Scholar 

  • J.V. Neel C. Satoh K. Goriki M. Fujita N. Takahashi J. Asakawa R. Hazama (1986) ArticleTitleThe rate with which spontaneous mutations alter the electrophoretic mobility of polypeptides Proc. Nat. Acad. Sci. USA 83 389–393 Occurrence Handle3455776

    PubMed  Google Scholar 

  • J.V. Neel C. Satoh K. Goriki J. Asakawa M. Fujita N. Takahashi T. Kageoka R. Hazama (1988) ArticleTitleSearch for mutations altering protein charge and/or function in children of atomic bomb survivors: final report Am. J. Hum. Genet. 42 663–676 Occurrence Handle3358419

    PubMed  Google Scholar 

  • H. Ochman A.C. Wilson. (1987) ArticleTitleEvolution in bacteria: evidence for a universal substitution rate in cellular genomes J. Mol. Evol 26 74–86 Occurrence Handle10.1007/BF02111283 Occurrence Handle3125340

    Article  PubMed  Google Scholar 

  • L.B. Russell W.L. Russell (1996) ArticleTitleSpontaneous mutations recovered as mosaics in the mouse specific-locus test Proc. Natl. Acad. Sci. USA 93 13072–13077 Occurrence Handle10.1073/pnas.93.23.13072 Occurrence Handle8917546

    Article  PubMed  Google Scholar 

  • E.S. Sachs M.G. Jahoda F.J. Los L. Pijpers J.W. Wladimiroff (1990) ArticleTitleTrisomy 21 mosaicism in gonads with unexpectedly high recurrence risks Am. J. Hum. Genet. 7 186–188

    Google Scholar 

  • Selby, P.B., 1998a. Discovery of numerous clusters of spontaneous mutations, pp. 463–487 R.C. Woodruff & J.N. Thompson jr. Kluwer Academic Publishers, Dordrecht, The Netherlands.

  • P.B. Selby (1998b) Major impacts of gonadal mosaicism on hereditary risk estimation, origin of hereditary diseases, and evolution R.C. Woodruff J.N. Thompson (Eds) Mutation and Evolution Kluwer Academic Publishers Dordrecht, The Netherlands 445–462

    Google Scholar 

  • S.S. Sommer R.P. Ketterling (1996) ArticleTitleThe factor IX gene as a model for analysis of human germline mutations: an update Hum. Mol. Genet. 5 1505–1514 Occurrence Handle8875257

    PubMed  Google Scholar 

  • S.S. Sommer W.A. Scaringe Hill K.A. (2001) ArticleTitleHuman germline mutation in the factor IX gene Mutat. Res. 487 1–17 Occurrence Handle11595404

    PubMed  Google Scholar 

  • W. Spencer C. Stern (1948) ArticleTitleExperiments to test the validity of the linear R-dose/mutation frequency relation in Drosophila at low dosage Genetics 33 43–74

    Google Scholar 

  • G. Stamatoyannopoulos P.E. Nute (1982) ArticleTitleDe novo mutations producing unstable Hbs or Hbs M Hum. Genet. 60 181–188 Occurrence Handle10.1007/BF00569709 Occurrence Handle7076259

    Article  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 Handle12082138

    PubMed  Google Scholar 

  • C. Stern (1968) Genetic Mosaics and Other Essays Harvard University Press Cambridge

    Google Scholar 

  • B.I. Strassmann B. Gillispie (2002) ArticleTitleLife-history theory, fertility and reproductive success in humans Proc. R. Soc. Lond. B 269 553–562 Occurrence Handle10.1098/rspb.2001.1912

    Article  Google Scholar 

  • J.N. Thompson 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 Handle9882003

    Article  PubMed  Google Scholar 

  • R. Thompson J.K. Pritchard P. Shen P.J. Oefner M.W. Feldman (2000) ArticleTitleRecent common ancestry of human Y chromosomes: evidence from DNA sequence data Proc. Nat. Acad. Sci. USA 97 7360–7365 Occurrence Handle10.1073/pnas.97.13.7360 Occurrence Handle10861004

    Article  PubMed  Google Scholar 

  • InstitutionalAuthorNameUNSCEAR (United Nations Scientific Committee on the Effects of Atomic Radiation). (2001) Heredity Effects of Radiation: Scientific Annex United Nations, New York

    Google Scholar 

  • A.J. Essen Particlevan S. Abbs M. Baiget E. Bakker C. Boileau C. Broeckhoven Particlevan D. Bushby A. Clarke M. Claustres A.E. Covone M. Ferrari A. Ferlini G. Galluzzi T. Grimm C. Grubben M. Jeanpierre H. Kaariainen S. Liechti-Gallati M.A. Melis G.-J.B. Ommen Particlevan J.E. Pocin H. Scheffer M. Schwartz A. Speer M. Stuhrmann C. Verellen-Dumoulin D.E. Wilcox L.P. ten Kate (1992) ArticleTitleParental origin and germline mosaicism of deletions and duplications of the dystrophin gene: a European study Hum. Genet 88 249–257 Occurrence Handle1733826

    PubMed  Google Scholar 

  • F. Vogel A.G. Motulsky (1997) Human Genetics: Problems and Approaches Springer Berlin

    Google Scholar 

  • E.M. Wijsman (1991) ArticleTitleRecurrence risk of a new dominant mutation in children of unaffected parents Am J Hum Genet 48 654–661 Occurrence Handle2014793

    PubMed  Google Scholar 

  • J.A. Wilder Z. Mobasher M.F. Hammer (2004) ArticleTitleGenetic evidence for unequal effective population sizes of human females and males Mol. Biol. Evol. 21 2047–2057 Occurrence Handle10.1093/molbev/msh214 Occurrence Handle15317874

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • R.C. Woodruff H. Huai J.N. Thompson (1996) ArticleTitleClusters of new mutations in the evolutionary landscape Genetica 98 149–160 Occurrence Handle10.1007/BF00121363 Occurrence Handle8976063

    Article  PubMed  Google Scholar 

  • R.C. Woodruff J.N. Thompson (2003) ArticleTitleThe role of somatic and germline mutations in aging and a mutation interaction model of aging J. Anti-Aging Med 6 29–39 Occurrence Handle10.1089/109454503765361560 Occurrence Handle12941181

    Article  PubMed  Google Scholar 

  • R.C. Woodruff J.N. Thompson S. Gu (2004) ArticleTitlePremeiotic clusters of mutation and the cost of natural selection J. Hered 95 277–283 Occurrence Handle10.1093/jhered/esh048 Occurrence Handle15247306

    Article  PubMed  Google Scholar 

  • F.E., Wurgler F.H. Sobels E. Vogel (1984) Drosophila as an assay system for detecting genetic changes B.J. Kilbey M. Legator W. Nichols C. Ramel (Eds) in Handbook of Mutagenicity Test Procedures, edited by Elsevier Science Publishers Amsterdam 555–601

    Google Scholar 

  • H.P. Yang A.Y. Tanikawa A.S. Kondrashov (2001) ArticleTitleMolecular nature of 11 spontaneous de novo mutations in Drosophila melanogaster Genetics 157 1285–1292 Occurrence Handle11238412

    PubMed  Google Scholar 

  • S.R. Yoon L. Dubeau M. Young Particlede N.S. Wexler N. Arnheim (2003) ArticleTitleHuntington disease expansion mutations in humans can occur before meiosis is completed Proc. Nat. Acad. Sci. USA 100 8834–8838 Occurrence Handle10.1073/pnas.1331390100 Occurrence Handle12857955

    Article  PubMed  Google Scholar 

  • D. Young (1991) Introduction to Risk Calculation in Genetic Counseling Oxford University Press Oxford

    Google Scholar 

  • J. Zlotogora (1998) ArticleTitleGerm line mosaicism Hum. Genet. 102 381–386 Occurrence Handle10.1007/s004390050708 Occurrence Handle9600231

    Article  PubMed  Google Scholar 

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  1. Department of Biological Sciences, Bowling Green State University, Bowling Green, OH, 43403, USA

    R.C. Woodruff

  2. Department of Zoology, University of Oklahoma, Norman, OK, 73019, USA

    J.N. Thomson

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Woodruff, R., Thomson, J. The Fundamental Theorem of Neutral Evolution: Rates of Substitution and Mutation Should Factor in Premeiotic Clusters. Genetica 125, 333–339 (2005). https://doi.org/10.1007/s10709-005-4982-7

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