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Spontaneous mutations in diploid Saccharomyces cerevisiae: another thousand cell generations

  • DAVID W. HALL (a1) (a2), ROD MAHMOUDIZAD (a1), ANDREW W. HURD (a1) and SARAH B. JOSEPH (a1) (a3)

Summary

Previously we performed a 1012-generation mutation accumulation (MA) study in yeast and found that a surprisingly large proportion of fitness-altering mutations were beneficial. To verify this result and assess the impact of sampling error in our previous study, we have continued the MA experiment for an additional 1050 cell generations and re-estimated mutation parameters. After correcting for biases due to selection, we estimate that 13% of the mutations accumulated during this study are beneficial. We conclude that the high proportions of beneficial mutations observed in this and our previous study cannot be explained by sampling error. We also estimate the genome-wide mutation rate to be 13·7×10−5 mutations per haploid genome per cell generation and the absolute value of the average heterozygous effect of a mutation to be 7·3%.

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Copyright

Corresponding author

*Corresponding author. Department of Genetics, Life Sciences Complex, University of Georgia, Athens, GA 30602, USA. Tel: 706-583-5476. Fax: 706-542-3910. e-mail: davehall@uga.edu

References

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Baer, C. F., Shaw, F., Steding, C., Baumgartner, M., Hawkins, A., Houppert, A., Mason, N., Reed, M., Simonelic, K., Woodard, W. & Lynch, M. (2005). Comparative evolutionary genetics of spontaneous mutations affecting fitness in rhabditid nematodes. Proceedings of the National Academy of Sciences of the USA 102, 57855790.
Bataillon, T. (2000). Estimation of genome–wide mutation rate parameters: whither beneficial mutations? Heredity 84, 497501.
Bateman, K. G. (1959). The viability of near-normal irradiated chromosomes. International Journal of Radiation Biology 2, 170180.
Benjamini, Y. & Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society 57, 289300.
Charlesworth, B., Borthwick, H., Bartolomé, C. & Pignatelli, P. (2004). Estimates of the genomic rate for detrimental alleles in Drosophila melanogaster. Genetics 167, 815826.
Drake, J. W. (1991). A constant rate of spontaneous mutation in DNA-based microbes. Proceedings of the National Academy of Sciences of the USA 88, 71607164.
Drake, J. W., Charlesworth, B., Charlesworth, D. & Crow, J. F. (1998). Rates of spontaneous mutation. Genetics 148, 16671686.
Drost, J. B. & Lee, W. R. (1995). Biological basis of germline mutation: comparisons of spontaneous germline mutation rates among Drosophila, mouse, and human. Environmental and Molecular Mutagenesis 25, 4864.
Estes, S., Phillips, P. C., Denver, D. R., Thomas, W. K. & Lynch, M. (2004). Mutation accumulation in populations of varying size: the distribution of mutational effects for fitness correlates in Caenorhabditis elegans. Genetics 166, 12691279.
Falconer, D. S. & MacKay, T. F. C. (1996). Introduction to Quantitative Genetics, 4th edn. Harlow, Essex, UK: Longman Group Ltd.
Fisher, R. A. (1930). The Genetical Theory of Natural Selection. Oxford: Oxford University Press.
Fry, J. D., Keightley, P. D., Heinsohn, S. L. & Nuzhdin, S. V. (1999). New estimates of the rates and effects of mildly deleterious mutation in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the USA 96, 574579.
Fry, J. D. (2004 a). On the rate and linearity of viability declines in Drosophila mutation-accumulation experiments: genomic mutation rates and synergistic epistasis revisited. Genetics 166, 797806.
Fry, J. D. (2004 b). Estimation of genetic variances and covariances by restricted maximum likelihood using proc mixed. In Genetic Analysis of Complex Traits Using SAS (ed. Saxton, A. M.), pp. 1134. Cary, NC: SAS Institute Inc.
Fry, J. D. (2004 c). How common are overdominant mutations? Genetics 167, 10311032.
Garcia-Dorado, A. (1997). The rate and effects distribution of viability mutation in Drosophila: minimum distance estimation. Evolution 51, 11301139.
Garcia-Dorado, A., Lopez-Fanjul, C. & Caballero, A. (1999). Properties of spontaneous mutations affecting quantitative traits. Genetical Research 74, 341350.
Gordo, I. & Charlesworth, B. (2000). On the speed of Muller's ratchet. Genetics 156, 21372140.
Houle, D., Morikawa, B. & Lynch, M. (1996). Comparing mutational variabilities. Genetics 143, 14671483.
Joseph, S. B. & Hall, D. W. (2004). Spontaneous mutation in Saccharomyces cerevisiae: more beneficial than expected. Genetics 168, 18171825.
Joseph, S. B. & Kirkpatrick, M. (2008). Effects of the [PSI+] prion on rates of adaptation in yeast. Journal of Evolutionary Biology 21, 773780.
Kassen, R. & Bataillon, T. (2006). Distribution of fitness effects among beneficial mutations before selection in experimental populations of bacteria. Nature Genetics 38, 484488.
Keightley, P. D. (1994). The distribution of mutation effects on viability in Drosophila melanogaster. Genetics 138, 13151322.
Keightley, P. D. & Bataillon, T. (2000). Multigenerational maximum-likelihood analysis applied to mutation-accumulation experiments in Caenorhabditis elegans. Genetics 154, 11931201.
Keightley, P. D. & Caballero, A. (1997). Genomic mutation rates for lifetime reproductive output and lifespan in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the USA 94, 38233827.
Keightley, P. D. & Ohnishi, O. (1998). EMS-induces polygenic mutation rates for nine quantitative characters in Drosophila melanogaster. Genetics 148, 753766.
Kibota, T. T. & Lynch, M. (1996). Estimate of the genomic mutation rate deleterious to overall fitness in E. coli. Nature 381, 694696.
Korona, R. (1999). Genetic load of the yeast Saccharomyces cerevisiae under diverse environmental conditions. Evolution 53, 19661971.
Li, W.-H. (1997). Molecular Evolution. Sunderland, MA: Sinauer Associates Inc.
Lynch, M. (1988). The rate of polygenic mutation. Genetical Research 51, 137148.
Lynch, M., Blanchard, J., Houle, D., Kibota, T., Schultz, S., Vassilieva, L. & Willis, J. (1999). Perspective: spontaneous deleterious mutation. Evolution 53, 645663.
Mukai, T. (1964). The genetic structure of natural populations of Drosophila melanogaster. I. Spontaneous mutation rate of polygenes controlling viability. Genetics 50, 119.
Mukai, T., Chigusa, S. I., Mettler, L. E. & Crow, J. F. (1972). Mutation rate and dominance of genes affecting viability in Drosophila melanogaster. Genetics 72, 333355.
Ohnishi, O. (1977). Spontaneous and ethyl methanesulfonate-induced mutations controlling viability in Drosophila melanogaster. II. Homozygous effect of polygenic mutations. Genetics 87, 529545.
Otto, S. P. & Orive, M. E. (1995). Evolutionary consequences of mutation and selection within an individual. Genetics 141, 11731187.
Perfeito, L., Fernandes, L., Mota, C. & Gordo, I. (2007). Adaptive mutations in bacteria: high rate and small effects. Science 317, 813815.
Peters, A. D., Halligan, D. L., Whitlock, M. C. & Keightley, P. D. (2003). Dominance and overdominance of mildly deleterious induced mutations for fitness traits in Caenorhabditis elegans. Genetics 165, 589599.
Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution 43, 223225.
Schultz, S. T., Lynch, M. & Willis, J. H. (1999). Spontaneous deleterious mutation in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the USA 96, 1139311398.
Shaw, F. H., Geyer, C. J. & Shaw, R. G. (2002). A comprehensive model of mutations affecting fitness and inferences for Arabidopsis thaliana. Evolution 56, 453463.
Sherman, F. (2002). Getting started with yeast. Methods in Enzymology 350, 341.
Szafraniec, K., Borts, R. & Korona, R. (2001). Environmental stress and mutational load in diploid strains of the yeast Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of the USA 98, 11071112.
Szafraniec, K., Wloch, D. M., Sliwa, P., Borts, R. & Korona, R. (2003). Small fitness effects and weak genetic interactions between deleterious mutations in heterozygous loci of the yeast Saccharomyces cerevisiae. Genetical Research 82, 1931.
Vassilieva, L. L. & Lynch, M. (1999). The rate of spontaneous mutation for life-history traits in Caenorhabditis elegans. Genetics 151, 119129.
Vassilieva, L. L., Hook, A. M. & Lynch, M. (2000). The fitness effects of spontaneous mutations in Caenorhabditis elegans. Evolution 54, 12341246.
Verhoeven, K. J. F., Simonsen, K. L. & McIntyre, L. M. (2005). Implementing the false discovery rate control: increasing your power. Oikos 108, 643647.
Whitlock, M. C. (2000). Fixation of new alleles and the extinction of small populations: Drift load, beneficial alleles, and sexual selection. Evolution 54, 18551861.
Whitlock, M. C., Griswold, C. K. & Peters, A. D. (2003). The critical effective size of a population with deleterious and compensatory mutations. Annales Zoologici Fennici 40, 169183.
Winzeler, E. A., Shoemaker, D. D., Astromoff, A., Liang, H., Anderson, K., Andre, B., Bangham, R., Benito, R., Boeke, J. D., Bussey, H., Chu, A. M., Connelly, C., Davis, K., Dietrich, F., Dow, S. W., El Bakkoury, M., Foury, F., Friend, S. H., Gentalen, E., Giaever, G., Hegemann, J. H., Jones, T., Laub, M., Liao, H., Liebundguth, N., Lockhart, D. J., Lucau-Danila, A., Lussier, M., M'Rabet, N., Menard, P., Mittmann, M., Pai, C., Rebischung, C., Revuelta, J. L., Riles, L., Roberts, C. J., Ross-MacDonald, P., Scherens, B., Snyder, M., Sookhai-Mahadeo, S., Storms, R. K., Véronneau, S., Voet, M., Volckaert, G., Ward, T. R., Wysocki, R., Yen, G. S., Yu, K., Zimmermann, K., Philippsen, P., Johnston, M. & Davis, R. W. (1999). Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285, 901906.
Wloch, D. M., Szafraniec, K., Borts, R. H. & Korona, R. (2001). Direct estimate of the mutation rate and the distribution of fitness effects in the yeast Saccharomyces cerevisiae. Genetics 159, 441452.
Zeyl, C. & DeVisser, J. (2001). Estimates of the rate and distribution of fitness effects of spontaneous mutation in Saccharomyces cerevisiae. Genetics 157, 5361.

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