Tốc độ đột biến tự phát

Genetics - Tập 148 Số 4 - Trang 1667-1686 - 1998
John W. Drake1, Brian Charlesworth2, Deborah Charlesworth2, James F. Crow3
1Laboratory of Molecular Genetics, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina 27709-2233
2Institute of Cell, Animal and Population Biology, University of Edinburgh, Edinburgh EH9 3JT, Scotland, United Kingdom.
3Genetics Department, University of Wisconsin, Madison, Wisconsin 53706

Tóm tắt

Tóm tắt

Tốc độ đột biến tự phát mỗi bộ gen được đo đạc trong phòng thí nghiệm có sự tương đồng đáng kể trong các nhóm sinh vật rộng lớn, nhưng lại có sự khác biệt rõ rệt giữa các nhóm. Tốc độ đột biến ở virus ARN, với bộ gen chứa khoảng 104 base, rơi vào khoảng 1 đột biến cho mỗi bộ gen cho mỗi lần tái tạo đối với virus ly giải, và khoảng 0,1 đột biến cho mỗi bộ gen cho mỗi lần tái tạo đối với virus ngược và một retrotransposon. Tốc độ đột biến ở vi sinh vật với nhiễm sắc thể ADN gần như là 1/300 cho mỗi bộ gen cho mỗi lần tái tạo; trong nhóm này, do đó, tỷ lệ đột biến trên mỗi cặp base thay đổi ngược chiều và rất lớn khi kích thước bộ gen thay đổi từ 6 × 103 đến 4 × 107 base hoặc cặp base. Tốc độ đột biến ở các sinh vật nhân thực bậc cao khoảng từ 0,1 đến 100 cho mỗi bộ gen cho mỗi thế hệ sinh sản, nhưng hiện tại không phân biệt được với 1/300 cho mỗi lần phân chia tế bào cho mỗi bộ gen hiệu dụng (điều này loại trừ phần bộ gen mà phần lớn các đột biến là trung tính). Hiện giờ, chúng ta có thể chỉ ra một số lực tiến hóa hình thành các tốc độ đột biến đa dạng này.

Từ khóa


Tài liệu tham khảo

Ågren, 1993, Outcrossing rate and inbreeding depression in two annual monoecious herbs, Begonia hirsuta and B. semiovata, Evolution, 47, 125, 10.1111/j.1558-5646.1993.tb01204.x

Akiyama, 1995, Mutation frequency in human blood cells increases with age, Mutat. Res., 338, 141, 10.1016/0921-8734(95)00019-3

Ashburner, 1989, Drosophila, A Laboratory Handbook

Auerbach, 1959, Spontaneous mutations in dry spores of Neurospora crassa, Z. Vererbungsl, 90, 335

Baker, 1995, Male mice defective in the DNA mismatch repair gene PMS2 exhibit abnormal chromosome synapsis in meiosis, Cell, 82, 309, 10.1016/0092-8674(95)90318-6

Baker, 1996, Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over, Nature Genet., 13, 336, 10.1038/ng0796-336

Bateman, 1959, The viability of near-normal irradiated chromosomes, Int. J. Radiat. Biol., 1, 170

Benian, 1989, Sequence of an unusually large protein implicated in regulation of myosin activity in C. elegans, Nature, 342, 45, 10.1038/342045a0

Benzer, 1961, On the topography of the genetic fine structure, Proc. Natl. Acad. Sci. USA, 47, 403, 10.1073/pnas.47.3.403

Bird, 1995, Gene number, noise reduction and biological complexity, Trends Genet., 11, 94, 10.1016/S0168-9525(00)89009-5

Blattner, 1997, The complete genome sequence of Escherichia coli K-12, Science, 277, 1453, 10.1126/science.277.5331.1453

Chao, 1983, Competition between high and low mutating strains of Escherichia coli, Evolution, 37, 125, 10.1111/j.1558-5646.1983.tb05521.x

Charlesworth, 1998, The maintenance of genetic variation in life-history traits, Evolutionary Genetics from Molecules to Morphology

Charlesworth, 1990, Genetic loads and estimates of mutation rates in very inbred plant populations, Nature, 347, 380, 10.1038/347380a0

Charlesworth, 1995, Quantitative genetics in plants: the effect of breeding system on genetic variability, Evolution, 49, 911, 10.1111/j.1558-5646.1995.tb02326.x

Charlesworth, 1994, Inbreeding depression in two highly inbreeding populations of Leavenworthia, Proc. R. Soc. Lond. Ser. B Biol. Sci., 258, 209, 10.1098/rspb.1994.0164

Christensen, 1985, Conjugation-dependent enhancement of induced and spontaneous mutation in the lacI gene of E. coli, Mol. Gen. Genet., 201, 35, 10.1007/BF00397983

Clark, 1988, The unc-22 (IV) region of Caenorhabditis elegans, Genetics, 119, 345, 10.1093/genetics/119.2.345

Connor, 1991, Effects of tree age on pollen, seed, and seedling characteristics in Great Basin bristlecone pine, Bot. Gaz., 152, 114, 10.1086/337869

Crow, 1993, How much do we know about spontaneous human mutation rates?, Environ. Mol. Mutagen., 21, 122, 10.1002/em.2850210205

Crow, 1995, Spontaneous mutation as a risk factor, Exp. Clin. Immunogenet., 12, 121

Crow, 1997, The high spontaneous mutation rate: is it a health risk?, Proc. Natl. Acad. Sci. USA, 94, 8380, 10.1073/pnas.94.16.8380

Crow, 1983, The mutation load in Drosophila, The Genetics and Biology of Drosophila, 1

Crumpacker, 1967, Genetic loads in maize (Zea mays L.) and other cross-fertilized plants and animals, Evol. Biol., 1, 306

Deng, 1996, Estimation of deleterious-mutation parameters in natural populations, Genetics, 144, 349, 10.1093/genetics/144.1.349

Deng, 1997, Inbreeding depression and inferred deleterious-mutation parameters in Daphnia, Genetics, 147, 147, 10.1093/genetics/147.1.147

de Wind, 1995, Inactivation of the mouse Msh2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination, and predisposition to cancer, Cell, 82, 321, 10.1016/0092-8674(95)90319-4

Drake, 1966, Spontaneous mutations accumulating in bacteriophage T4 in the complete absence of DNA replication, Proc. Natl. Acad. Sci. USA, 55, 738, 10.1073/pnas.55.4.738

Drake, 1991, A constant rate of spontaneous mutation in DNA-based microbes, Proc. Natl. Acad. Sci. USA, 88, 7160, 10.1073/pnas.88.16.7160

Drake, 1993, Rates of spontaneous mutation among RNA viruses, Proc. Natl. Acad. Sci. USA, 90, 4171, 10.1073/pnas.90.9.4171

Drake, 1993, General antimutators are improbable, J. Mol. Biol., 229, 8, 10.1006/jmbi.1993.1002

Drake, 1994, Mutagenesis, Molecular Biology of Bacteriophage T4, 98

Drost, 1995, Biological basis of germline mutation: comparisons of spontaneous germline mutation rates among Drosophila, mouse, and human, Environ. Mol. Mutagen., 26, 48, 10.1002/em.2850250609

Edelmann, 1996, Meiotic pachytene arrest in MLH1-deficient mice, Cell, 85, 1125, 10.1016/S0092-8674(00)81312-4

Eide, 1985, The gene structures of spontaneous mutations affecting a Caenorhabditis elegans myosin heavy chain gene, Genetics, 109, 67, 10.1093/genetics/109.1.67

Fernandez, 1996, Spontaneous mutational variances and covariances for fitness-related traits in Drosophila melanogaster, Genetics, 143, 829, 10.1093/genetics/143.2.829

Finch, 1990, Longevity, Senescence, and the Genome

Finnegan, 1986, Transposable elements in Drosophila melanogaster, Oxf. Surv. Eukaryotic Genes, 3, 1

Fisher, 1930, The Genetical Theory of Natural Selection, 10.5962/bhl.title.27468

Foster, 1997, Nonadaptive mutations occur on the F′ episome during adaptive mutation conditions in Escherichia coli, J. Bacteriol., 179, 1550, 10.1128/jb.179.5.1550-1554.1997

Gabriel, 1996, Replication infidelity during a single cycle of Ty1 retrotransposition, Proc. Natl. Acad. Sci. USA, 93, 7767, 10.1073/pnas.93.15.7767

Garcia-Dorado, 1997, The rate and effects distribution of viability mutations in Drosophila: minimum distance estimation, Evolution, 51, 1130

Gillespie, 1981, Mutation modification in a random environment, Evolution, 35, 468, 10.1111/j.1558-5646.1981.tb04910.x

Gillespie, 1981, Evolution of the mutation rate at a heterotic locus, Proc. Natl. Acad. Sci. USA, 78, 2452, 10.1073/pnas.78.4.2452

Goelet, 1982, Nucleotide sequence of tobacco mosaic virus RNA, Proc. Natl. Acad. Sci. USA, 79, 5818, 10.1073/pnas.79.19.5818

Goffeau, 1996, Life with 6000 genes, Science, 274, 546, 10.1126/science.274.5287.546

Greenwald, 1980, unc-93(e1500): a behavioral mutant of Caenorhabditis elegans that defines a gene with a wild-type null phenotype, Genetics, 96, 147, 10.1093/genetics/96.1.147

Gross, 1981, Incidence of mutator strains in Escherichia coli and coliforms in nature, Mutat. Res., 91, 107, 10.1016/0165-7992(81)90081-6

Hall, 1984, Generation of genetic diversity in herpes simplex virus: an antimutator phenotype maps to the DNA polymerase locus, Virology, 132, 26, 10.1016/0042-6822(84)90088-6

Haldane, 1927, A mathematical theory of natural and artificial selection. Part V. Selection and mutation, Proc. Camb. Philos. Soc., 23, 838, 10.1017/S0305004100015644

Haldane, 1937, The effect of variation on fitness, Am. Nat., 71, 337, 10.1086/280722

Holland, 1990, Mutation frequencies at defined single codonsites in vesicular stomatitis virus and poliovirus can be increased only slightly by chemical mutagenesis, J. Virol., 64, 3960, 10.1128/jvi.64.8.3960-3962.1990

Houle, 1992, Comparing evolvability and variability of quantitative traits, Genetics, 130, 195, 10.1093/genetics/130.1.195

Howe, 1997, Intron self-complementarity enforces exon inclusion in yeast pre-mRNA, Proc. Natl. Acad. Sci. USA, 94, 12467, 10.1073/pnas.94.23.12467

Hughes, 1995, The inbreeding decline and average dominance of genes affecting male life-history characters in Drosophila melanogaster, Genet. Res., 65, 41, 10.1017/S0016672300032997

Ishii, 1989, Evolutionarily stable mutation rate in a periodically changing environment, Genetics, 121, 163, 10.1093/genetics/121.1.163

Jacobs, 1997, Rates of spontaneous mutation in an Archaeon from geothermal environments, J. Bacteriol., 179, 3298, 10.1128/jb.179.10.3298-3303.1997

Johnston, 1995, Mutation rates and dominance levels of genes affecting total fitness in two angiosperm species, Science, 267, 226, 10.1126/science.267.5195.226

Jyssum, 1960, Observations on two types of genetic instability in Escherichia coli, Acta Path. Microbiol. Scand., 48, 113, 10.1111/j.1699-0463.1960.tb04747.x

Karn, 1983, Protein structural domains in the Caenorhabditis elegans unc-54 myosin heavy chain gene are not separated by introns, Proc. Natl. Acad. Sci. USA, 80, 4253, 10.1073/pnas.80.14.4253

Kearney, 1993, Low level of genetic drift in foreign sequences replicating in a RNA virus in plants, Virology, 192, 11, 10.1006/viro.1993.1002

Keightley, 1994, The distribution of mutation effects on viability in Drosophila melanogaster, Genetics, 138, 1, 10.1093/genetics/138.4.1315

Keightley, 1996, The nature of deleterious mutation load in Drosophila, Genetics, 144, 1993, 10.1093/genetics/144.4.1993

Keightley, 1997, Genomic mutation rate for fitness in Caenorhabditis elegans, Proc. Natl. Acad. Sci. USA, 94, 3823, 10.1073/pnas.94.8.3823

Khush, 1967, Studies on the linkage map of chromosome 4 of the tomato and on the transmission of induced deficiencies, Genetica, 38, 74, 10.1007/BF01507450

Kibota, 1996, Estimate of the genomic mutation rate deleterious to overall fitness in E. coli, Nature, 381, 694, 10.1038/381694a0

Kimble, 1988, Germ-line development and fertilization, The Nematode Caenorhabditis elegans, 191

Kimura, 1960, Optimum mutation rate and degree of dominance as determined by the principle of minimum genetic load, J. Genet., 57, 21, 10.1007/BF02985336

Kimura, 1967, On the evolutionary adjustment of spontaneous mutation rates, Genet. Res., 9, 23, 10.1017/S0016672300010284

Kimura, 1983, The Neutral Theory of Molecular Evolution, 10.1017/CBO9780511623486

Kimura, 1983, Rare variant alleles in the light of the neutral theory, Mol. Biol. Evol., 1, 84

Kimura, 1966, The mutation load with epistatic gene interactions in fitness, Genetics, 54, 1337, 10.1093/genetics/54.6.1337

Kimura, 1971, Theoretical Topics in Population Genetics

Kirkwood, 1986, Accuracy in Molecular Processes, 10.1007/978-94-009-4097-0

Klekowski, 1973, Genetic load in Osmunda regalis populations, Am. J. Bot., 60, 146, 10.1002/j.1537-2197.1973.tb10211.x

Klekowski, 1988, Mutation, Developmental Selection, and Plant Evolution, 10.7312/klek92068

Klekowski, 1992, Mutation rates in diploid annuals—are they immutable?, Int. J. Plant Sci., 153, 462, 10.1086/297052

Klekowski, 1989, Aging and mutation in plants: a comparison of woody mangroves and herbaceous annuals, Nature, 340, 389, 10.1038/340389a0

Klekowski, 1994, Mangrove genetics. II. Outcrossing and lower spontaneous mutation rates in Puerto Rican Rhizophora, Int. J. Plant Sci., 155, 373, 10.1086/297174

Knight, 1957, Fitness as a measurable character in Drosophila, Genetics, 42, 524, 10.1093/genetics/42.4.524

Kohler, 1991, Spectra of spontaneous and mutagen-induced mutations in the lacI gene in transgenic mice, Proc. Natl. Acad. Sci. USA, 88, 7958, 10.1073/pnas.88.18.7958

Kondrashov, 1984, Deleterious mutations as an evolutionary factor. I. The advantage of recombination, Genet. Res., 44, 325, 10.1017/S0016672300026392

Kondrashov, 1988, Deleterious mutations and the evolution of sexual reproduction, Nature, 336, 435, 10.1038/336435a0

Kondrashov, 1993, A classification of hypotheses on the advantage of amphimixis, J. Hered., 84, 372, 10.1093/oxfordjournals.jhered.a111358

Kondrashov, 1995, Modifiers of mutation-selection balance: general approach and the evolution of mutation rates, Genet. Res., 66, 53, 10.1017/S001667230003439X

Kondrashov, 1993, A molecular approach to estimating the human deleterious mutation rate, Hum. Mutat., 2, 229, 10.1002/humu.1380020312

Kondrashov, 1994, Genotype-environment interaction and the estimation of the genomic mutation rate in Drosophila melanogaster, Proc. R. Soc. Lond. Ser. B Biol. Sci., 258, 221, 10.1098/rspb.1994.0166

Kunz, 1983, The infidelity of conjugal DNA transfer in Escherichia coli, Genetics, 105, 489, 10.1093/genetics/105.3.489

Kutter, 1994, Genomic map of bacteriophage T4, Molecular Biology of Bacteriophage T4, 491

Laird, 1971, Chromatid structure: relationship between DNA content and nucleotide sequence diversity, Chromosoma, 32, 378, 10.1007/BF00285251

Lande, 1985, The evolution of self fertilization and inbreeding depression in plants. I. Genetic models, Evolution, 39, 24

LeClerc, 1996, High mutation frequencies among Escherichia coli and Salmonella pathogens, Science, 274, 1208, 10.1126/science.274.5290.1208

Leigh, 1970, Natural selection and mutability, Am. Nat., 104, 301, 10.1086/282663

Leigh, 1973, The evolution of mutation rates, Genetics Suppl., 73, 1

Levin, 1992, The Caenorhabditis elegans unc-93 gene encodes a putative transmembrane protein that regulates muscle contraction, J. Cell Biol., 117, 143, 10.1083/jcb.117.1.143

Liu, 1996, Interaction between a putative mechanosensory membrane channel and a collagen, Science, 273, 361, 10.1126/science.273.5273.361

Mansky, 1994, Lower mutation rate of bovine leukemia virus relative to spleen necrosis virus, J. Virol., 68, 494, 10.1128/jvi.68.1.494-499.1994

Mansky, 1995, Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase, J. Virol., 69, 5087, 10.1128/jvi.69.8.5087-5094.1995

Mao, 1997, Proliferation of mutators in a cell population, J. Bacteriol., 179, 417, 10.1128/jb.179.2.417-422.1997

Matic, 1997, Highly variable mutation rates in commensal and pathogenic Escherichia coli, Science, 277, 1833, 10.1126/science.277.5333.1833

Maynard Smith, 1991, The population genetics of bacteria, Proc. R. Soc. Lond. Ser. B Biol. Sci., 245, 37, 10.1098/rspb.1991.0085

McGeoch, 1988, The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1, J. Gen. Virol., 69, 1531, 10.1099/0022-1317-69-7-1531

McKnight, 1980, The nucleotide sequence and transcript map of the herpes simplex virus thymidine kinase gene, Nucleic Acids Res., 8, 5949, 10.1093/nar/8.24.5949

McVean, 1997, Evidence for a selectively favorable reduction in the mutation rate of the X chromosome, Nature, 386, 388, 10.1038/386388a0

Moxon, 1994, Adaptive evolution of highly mutable loci in pathogenic bacteria, Curr. Biol., 4, 23, 10.1016/S0960-9822(00)00005-1

Mukai, 1964, The genetic structure of natural populations of Drosophila melanogaster. I. Spontaneous mutation rate of polygenes controlling viability, Genetics, 50, 1, 10.1093/genetics/50.1.1

Mukai, 1969, The genetic structure of natural populations of Drosophila melanogaster. VII. Synergistic interaction of spontaneous mutant polygenes controlling viability, Genetics, 61, 749, 10.1093/genetics/61.3.749

Mukai, 1977, Spontaneous mutation rates at enzyme loci in Drosophila melanogaster, Proc. Natl. Acad. Sci. USA, 74, 2514, 10.1073/pnas.74.6.2514

Mukai, 1972, Mutation rate and dominance of genes affecting viability in Drosophila melanogaster, Genetics, 72, 335, 10.1093/genetics/72.2.335

Mukai, 1974, The genetic variance for viability and its components in a local population of Drosophila melanogaster, Genetics, 78, 1195, 10.1093/genetics/78.4.1195

Muller, 1928, The measurement of gene mutation rate in Drosophila, its high variability, and its dependence on temperature, Genetics, 13, 279, 10.1093/genetics/13.4.279

Muller, 1952, The standard error of the frequency of mutants some of which are of common origin, Genetics, 37, 608

Narayanan, 1997, Elevated levels of mutation in multiple tissues of mice deficient in the DNA mismatch repair gene Pms2, Proc. Natl. Acad. Sci. USA, 94, 3122, 10.1073/pnas.94.7.3122

Nee, 1987, The evolution of multicompartmental genomes in viruses, J. Mol. Evol., 25, 277, 10.1007/BF02603110

Ninio, 1991, Transient mutators: a semiquantitative analysis of the influence of translation and transcription errors on mutation rates, Genetics, 129, 957, 10.1093/genetics/129.3.957

Nöthel, 1987, Adaptation of Drosophila melanogaster populations to high mutation pressure: evolutionary adjustment of mutation rates, Proc. Natl. Acad. Sci. USA, 84, 1045, 10.1073/pnas.84.4.1045

Ohnishi, 1977, Spontaneous and ethyl methanesulfonate-induced mutations controlling viability in Drosophila melanogaster. II. Homozygous effects of polygenic mutations, Genetics, 87, 529, 10.1093/genetics/87.3.529

Ohnishi, 1982, Population genetics of cultivated buckwheat, Fagopyrum esculentum Moench. I. Frequency of chlorophyll-deficient mutants in Japanese populations, Jpn. J. Genet., 57, 623, 10.1266/jjg.57.623

Ohta, 1974, Detrimental genes with partial selfing and effects on a neutral locus, Genet. Res., 23, 191, 10.1017/S0016672300014816

Orr, 1995, Somatic mutation favors the evolution of diploidy, Genetics, 139, 1441, 10.1093/genetics/139.3.1441

Parsons, 1995, Mismatch repair deficiency in phenotypically normal human cells, Science, 268, 738, 10.1126/science.7632227

Parthasarathi, 1995, Genetic rearrangements occurring during a single cycle of murine leukemia virus vector replication: characterization and implications, J. Virol., 69, 7991, 10.1128/jvi.69.12.7991-8000.1995

Pathak, 1990, Broad spectrum of in vivo forward mutations, hypermutations, and mutational hotspots in a retroviral shuttle vector after a single replication cycle: substitutions, frameshifts, and hypermutations, Proc. Natl. Acad. Sci. USA, 87, 6019, 10.1073/pnas.87.16.6019

Peterson, 1995, Genetic map of the Mycoplasma genitalium chromosome, J. Bacteriol., 177, 3199, 10.1128/jb.177.11.3199-3204.1995

Pressing, 1984, Divided genomes and intrinsic noise, J. Mol. Evol., 20, 135, 10.1007/BF02257374

Quiñones, 1985, Isolation and characterization of Escherichia coli antimutators, Mol. Gen. Genet., 201, 315, 10.1007/BF00425677

Ratner, 1985, Complete nucleotide sequence of the AIDS virus, HTLV-III, Nature, 313, 277, 10.1038/313277a0

Reha-Krantz, 1993, Bacteriophage T4 DNA polymerase mutations that confer sensitivity to the PPi analog phosphonoacetic acid, J. Virol., 67, 60, 10.1128/jvi.67.1.60-66.1993

Reitmair, 1995, MSH2 deficient mice are viable and susceptible to lymphoid tumours, Nature Genet., 11, 64, 10.1038/ng0995-64

Risch, 1987, Spontaneous mutation and parental age in humans, Am. J. Hum. Genet., 41, 218

Rosenbluth, 1983, Mutagenesis in Caenorhabditis elegans. I. A rapid eukaryotic mutagen test system using the reciprocal translocation eT1(III; V), Mutat. Res., 119, 39, 10.1016/0027-5107(83)90016-7

Russell, 1996, Spontaneous mutations recovered as mosaics in the mouse specific-locus test, Proc. Natl. Acad. Sci. USA, 93, 13072, 10.1073/pnas.93.23.13072

Sagata, 1985, Complete nucleotide sequence of the genome of bovine leukemia virus: its evolutionary relationship to other retroviruses, Proc. Natl. Acad. Sci. USA, 82, 677, 10.1073/pnas.82.3.677

Sapienza, 1994, Parental origin effects, genome imprinting, and sex-ratio distortion: double or nothing?, Am. J. Hum. Genet., 55, 1073

Sasaki, 1994, Evolution of antigen drift/switching: continuously evading pathogens, J. Theor. Biol., 168, 291, 10.1006/jtbi.1994.1110

Schalet A , 1960  A study of spontaneous visible mutations in Drosophila melanogaster. Ph.D. Thesis, Indiana University, Bloomington.

Schnell, 1996, The minimal conserved transcription stop-start signal promotes stable expression of a foreign gene in vesicular stomatitis virus, J. Virol., 70, 2318, 10.1128/jvi.70.4.2318-2323.1996

Shiang, 1994, Mutations in the transmembrane domain of FGFR3 cause the most common genetic form of dwarfism, achondroplasia, Cell, 78, 335, 10.1016/0092-8674(94)90302-6

Simmons, 1978, Heterozygous effects on fitness of EMS-treated chromosomes in Drosophila melanogaster, Genetics, 88, 575, 10.1093/genetics/88.3.575

Sniegowski, 1997, Evolution of high mutation rates in experimental populations of E. coli, Nature, 387, 703, 10.1038/42701

Stadler, 1929, Chromosome number and the mutation rate in Avena and Triticum, Proc. Natl. Acad. Sci. USA, 15, 876, 10.1073/pnas.15.12.876

Stadler, 1930, The frequency of mutation of specific genes in maize (Abstr.), Anat. Rec., 47, 381

Steponkus, 1993, An optimized procedure for the cryopreservation of Drosophila melanogaster embryos, Cryo Lett., 14, 375

Sturtevant, 1937, Essays on evolution. I. On the effects of selection on the mutation rate, Q. Rev. Biol., 12, 464, 10.1086/394543

Sulston, 1974, The DNA of Caenorhabditis elegans, Genetics, 77, 95, 10.1093/genetics/77.1.95

Sved, 1975, Fitness of third chromosome homozygotes in Drosophila melanogaster, Genet. Res., 25, 197, 10.1017/S0016672300015603

Taddei, 1995, Mutation rate of the F episome, Science, 269, 288, 10.1126/science.269.5222.288.c

Taddei, 1997, Role of mutator alleles in adaptive evolution, Nature, 387, 700, 10.1038/42696

Takano, 1987, The genetic structure of natural populations of Drosophila melanogaster. XX. Comparisons of genotype-environment interaction in viability between a northern and southern population, Genetics, 117, 245, 10.1093/genetics/117.2.245

Torkelson, 1997, Genome-wide hypermutation in a subpopulation of stationary-phase cells underlies recombination-dependent adaptive mutation, EMBO J., 16, 3303, 10.1093/emboj/16.11.3303

Tröbner, 1984, Selection against hypermutability in Escherichia coli during long term evolution, Mol. Gen. Genet., 198, 177, 10.1007/BF00328720

Vogel, 1997, Human Genetics: Problems and Approaches, 3, 10.1007/978-3-662-03356-2

Walker, 1984, Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli, Microbiol. Rev., 48, 60, 10.1128/mr.48.1.60-93.1984

Wallace, 1952, The estimation of adaptive values of experimental populations, Evolution, 6, 333, 10.1111/j.1558-5646.1952.tb01429.x

Wallace, 1956, Studies on irradiated populations of Drosophila melanogaster, J. Genet., 54, 280, 10.1007/BF02982782

Wijsman, 1984, The effect of mutagenesis on competitive ability in Drosophila, Evolution, 38, 571, 10.1111/j.1558-5646.1984.tb00323.x

Willetts, 1987, Structure and function of the F factor and mechanism of conjugation, Escherichia coli and Salmonella typhimurium, 1110

Woodruff, 1984, Variation in spontaneous mutation rates in natural population lines of Drosophila melanogaster, Heredity, 53, 223, 10.1038/hdy.1984.78

Woodruff, 1997, Clusters of new mutation in the evolutionary landscape, Genetica, 98, 149, 10.1007/BF00121363

Yamaguchi, 1974, Variation of spontaneous occurrence rates of chromosomal aberrations in the second chromosomes of Drosophila melanogaster, Genetics, 78, 1209, 10.1093/genetics/78.4.1209