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Modifiers of mutation-selection balance: general approach and the evolution of mutation rates

Published online by Cambridge University Press:  14 April 2009

Alexey S. Kondrashov
Alexey S. Kondrashov
Affiliation:
Section of Ecology and Systematics, Corson Hall, Cornell University, Ithaca, NY 14853, USA, Phone: (607) 255-4617, FAX: (607) 255-8088 E-mail: [email protected]
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A general approach is developed to estimate secondary selection at a modifier locus that influences some feature of a population under mutation-selection balance. The approach is based on the assumption that the properties of all available genotypes at this locus are similar. Then mutation-selection balance and weak associations between genotype distributions at selectable loci and the modifier locus are established rapidly. In contrast, changes of frequencies of the modifier genotypes are slow, and lead to only slow and small changes of the other features of the population. Thus, while these changes occur, the population remains in a state of quasi-equilibrium, where the mutation-selection balance and the associations between the selectable loci and the modifier locus are almost invariant. Selection at the modifier locus can be estimated by calculating quasiequilibrium values of these associations. This approach is developed for the situation where distributions of the number of mutations per genome within the individuals with a given modifier genotype are close to Gaussian. The results are used to study the evolution of the mutation rate. Because beneficial mutations are ignored, secondary selection at the modifier locus always diminishes the mutation rate. The coefficient of selection against an allele which increases the mutation rate by υ is approximately υδ2/[U(2−ρ)] = υŝ, where υ is the genomic deleterious mutation rate, δ is the selection differential of the number of mutations per individual in units of the standard deviation of the distribution of this number in the population, ρ is the ratio of variances of the number of mutations after and before selection, and ŝ is the selection coefficient against a mutant allele in the quasiequilibrium population. However, the decline of the mutation rate can be counterbalanced by the cost of fidelity, which can lead to an evolutionary equilibrium mutation rate.

Type
Research Article
Information
Genetics Research , Volume 66 , Issue 1 , August 1995 , pp. 53 - 69
Copyright
Copyright © Cambridge University Press 1995

References

Altenberg, L., & Feldman, M. W., (1987). Selection, generalized transmission and the evolution of modifier genes. I. The reduction principle. Genetics 117, 559–572.CrossRefGoogle ScholarPubMed
Barrett, S. C. H., & Husband, B. C., (1990). Variation in outcrossing rates in Eichhornia paniculata: the role of demographic and reproductive factors. Plant Species Biology 5, 41–55.CrossRefGoogle Scholar
Berg, R. L., (1941). Role of small mutations in the evolution of mutability. Doklady Akademii Nauk SSSR 32, 71–74.Google Scholar
Berg, R. L., (1942). Mutability as dependent on the degree of isolation of populations of Drosophila melanogaster. Doklady Akademii Nauk SSSR 36, 71–75.Google Scholar
Berg, R. L., (1948). On relationship between mutability and selection in natural populations of Drosophila melanogaster. Zhurnal Obshchej Biologii 9, 299–313 (in Russian).Google Scholar
Bodmer, W. F., & Felsenstein, J., (1967). Linkage and selection: theoretical analysis of the deterministic two locus random mating model. Genetics 57, 237–265.CrossRefGoogle ScholarPubMed
Brooks, L. D., (1988). The evolution of recombination rates. In The Evolution of Sex: an Examination of Current Ideas (ed. Michod, R. E. and Levin, B. R.), pp. 87–105.Google Scholar
Charlesworth, B., (1990). Mutation-selection balance and the evolutionary advantage of sex and recombination. Genetical Research 55, 199–221.CrossRefGoogle ScholarPubMed
Charlesworth, B., (1993). Directional selection and the evolution of sex and recombination. Genetical Research 61, 205–224.CrossRefGoogle ScholarPubMed
Charlesworth, B., Morgan, M. T., & Charlesworth, D., (1991). Multilocus models of inbreeding depression with synergistic selection and partial self-fertilization. Genetical Research 57, 177–194.CrossRefGoogle Scholar
Crow, J. F., & Kimura, M., (1970). An Introduction to Population Theory. Harper and Row, New York.Google Scholar
Crow, J. F., & Simmons, M. J., (1983). The mutation load in Drosophila. In The Genetics and Biology of Drosophila, Vol. 3c (ed. Ashburner, M., Carson, H. L. and Thompson, J. N. Jr), pp. 1–35. Academic Press, London.Google Scholar
Demerec, M., (1937). Frequency of spontaneous mutations in certain stocks of Drosophila melanogaster. Genetics 22, 469–478.CrossRefGoogle ScholarPubMed
Dobzhansky, T., (1951). Genetics and the Origin of Species. New York, Columbia University Press (3rd edn).Google Scholar
Drake, J. W., (1991). A constant rate of spontaneous mutation in DNA-based microbes. Proceedings of the National Academy of Sciences USA 88, 7160–7164.CrossRefGoogle ScholarPubMed
Dubinin, N. P., Geptner, M. A., Demidova, Z. A., & Dyachkova, L. I., (1936). Genetic constitution and gene dynamics of wild populations of Drosophila melanogaster. Biologicheskij Zhurnal 5, 939–976.Google Scholar
Dubovskij, N. V., (1935). On the question of the comparative mutability of stocks of Drosophila melanogaster of different origin. Comptes Rendus (Doklady) le l'academie des Sciences de I'URSS 4, 95–97.Google Scholar
Eshel, I., (1973). Clone selection and the evolution of modifying features. Theoretical Population Biology 4, 196–208.CrossRefGoogle Scholar
Feldman, M. W., Christiansen, F. B., & Brooks, L. D., (1980). Evolution of recombination in constant environment. Proceedings of the National Academy of Sciences USA 77, 4838–4841.CrossRefGoogle ScholarPubMed
Gillespie, J. H., (1981). Mutation modification in a random environment. Evolution 35, 468–476.CrossRefGoogle Scholar
Gillespie, J. H., (1981). Evolution of the mutation rate at a heterotic locus. Proceedings of the National Academy of Sciences USA 78, 2452–2454.CrossRefGoogle Scholar
Hebert, P. D. N., Beaton, M. J., Schwartz, S. S., & Stanton, D. J., (1989). Polyphiletic origins of asexuality in Daphnia pulex. I. Breeding-system variation and levels of clonal diversity. Evolution 43, 1004–1015.Google Scholar
Holsinger, K. E., & Feldman, M. W., (1983). Modifiers of mutation rate: evolutionary optimum with complete selfing. Proceedings of the National Academy of Sciences USA 80, 6732–6734.CrossRefGoogle ScholarPubMed
Holsinger, K. E., Feldman, M. W., & Altenberg, L., (1986). Selection for increased mutation rates with fertility differences between matings. Genetics 112, 909–922.CrossRefGoogle ScholarPubMed
Houle, D., Hoffmaster, D. K., Assimacopoulos, S., & Charlesworth, B., (1992). The genomic mutation rate for fitness in Drosophila. Nature 359, 58–60.CrossRefGoogle ScholarPubMed
Ishii, K., Matsuda, H., Iwasa, Y., & Sasaki, A., (1989). Evolutionary stable mutation rate in a periodically changing environment. Genetics 121, 163–174.CrossRefGoogle Scholar
Ives, P. T., (1950). The importance of mutation rate genes in evolution. Evolution 4, 236–252.CrossRefGoogle Scholar
Iwasa, Y., Pomiankowski, A., & Nee, S., (1991). The evolution of costly mate preferences. II. The “handicap” principle. Evolution 45, 1431–1442.Google ScholarPubMed
Karlin, S., & McGregor, J., (1974). Towards a theory of the evolution of modifier genes. Theoretical Population Biology 5, 59–103.CrossRefGoogle ScholarPubMed
Kimura, M., (1960). Optimum mutation rate and degree of dominance as determined by the principle of minimum genetic load. Journal of Genetics 57, 21–34.CrossRefGoogle Scholar
Kimura, M., (1967). On the evolutionary adjustment of spontaneous mutation rates. Genetical Research 9, 23–34.CrossRefGoogle Scholar
Kimura, M., & Maruyama, T., (1966). The mutation load with epistatic gene interactions in fitness. Genetics 54, 1337–1351.CrossRefGoogle ScholarPubMed
Kirkwood, T. B. L., Rosenberger, R. F., & Galas, D. J., (1986). Accuracy in Molecular Processes. Chapman and Hall, London.CrossRefGoogle Scholar
Kondrashov, A. S., (1984). Deleterious mutations as an evolutionary factor. I. The advantage of recombination. Genetical Research 44, 199–214.CrossRefGoogle Scholar
Kondrashov, A. S., (1988). Deleterious mutations and the evolution of sexual reproduction. Nature 336, 435–440.CrossRefGoogle ScholarPubMed
Kondrashov, A. S., (1993). Classification of hypotheses on the advantage of amphimixis. J. of Heredity 84, 372–387.CrossRefGoogle ScholarPubMed
K-95 = Kondrashov, A. S., (1995). Dynamics of unconditionally deleterious mutations: Gaussian approximation and soft selection. Genetical Research 65, 113–121.CrossRefGoogle ScholarPubMed
Kondrashov, A. S., & Turelli, M., (1992). Deleterious mutations, apparent stabilizing selection and the maintenance of quantitative variation. Genetics 132, 603–618.CrossRefGoogle ScholarPubMed
Korol, A. B., Preigel, I. A., & Preigel, S. I., (1990). Variability of crossing-over in higher organisms. Kishinev, Shtiinca (in Russian).Google Scholar
Leigh, E. G., (1970). Natural selection and mutability. American Naturalist 104, 301–305.CrossRefGoogle Scholar
Leigh, E. G., (1973). The evolution of mutation rates. Genetics (Supplement) 73, 1–18.Google ScholarPubMed
Levins, R., (1967). Theory of fitness in a heterogeneous environment. VI. The adaptive significance of mutation. Genetics 56, 163–178.CrossRefGoogle Scholar
Lewontin, R. C., (1974). The Genetic Basis of Evolutionary Change. Harvard University Press, Cambridge.Google Scholar
Liberman, U., & Feldman, M. W., (1986). Modifiers of mutation rate: a general reduction principle. Theoretical Population Biology 30, 125–142.CrossRefGoogle ScholarPubMed
Lindahl, T., (1993). Instability and decay of the primary structure of DNA. Nature 362, 709–715.CrossRefGoogle ScholarPubMed
Mishchenko, E. F., & Rozov, N. Kh. (1980). Differential Equations with Small Parameters and Relaxation Oscillations. Plenum Press, New York.CrossRefGoogle Scholar
Mohrenweiser, H., (1994). Impact of the molecular spectrum of mutational lesions on estimates of germinal genemutation rates. Mutation Research 304, 119–137.CrossRefGoogle ScholarPubMed
Morgan, M. T., & Barrett, S. C. H., (1990). Outcrossing rates and correlated mating within a population of Eichhornia paniculata (Pontederiaceae). Heredity 64, 271–280.CrossRefGoogle Scholar
Muller, H. J., (1928). The measurement of gene mutation rate in Drosophila, its high variability, and its dependence upon temperature. Genetics 13, 279–357.CrossRefGoogle ScholarPubMed
Nagylaki, T., (1993). The evolution of multilocus systems under weak selection. Genetics 134, 627–647.CrossRefGoogle ScholarPubMed
Nei, M., & Li, W.-H., (1980). Non-random association between electromorphs and inversion chromosomes in finite populations. Genetical Research 35, 65–83.CrossRefGoogle ScholarPubMed
Njiokou, F., Bellec, C., Berrebi, P., Delay, B., & Jarne, P., (1993). Do self-fertilization and genetic drift promote a very low genetic variability in allotetraploid Bulinus truncatus (Gastropoda: Planorbidae) populations? Genetical Research 62, 89–100.CrossRefGoogle Scholar
Nothel, H., (1987). Adaptation of Drosophila melanogaster populations to high mutation pressure: evolutionary adjustment of mutation rates. Proceedings of the National Academy of Sciences USA 84, 1045–1048.CrossRefGoogle ScholarPubMed
Painter, P. R., (1975). Clone selection and the mutation rate. Theoretical Population Biology 8, 74–80.CrossRefGoogle ScholarPubMed
Passekov, V. P., & Singh, D. K., (1991). Weak selection in a logistic model of density-dependent genotype fitnesses. Zhurnal Obshchej Biologii 54, 509–520 (in Russian).Google Scholar
Poinar, G. O., (1993). Recovery of antediluvian DNA. Nature 365, 700.CrossRefGoogle Scholar
Redfield, R. J., (1994). Male mutation rates and the cost of sex for females. Nature 369, 145–147.CrossRefGoogle ScholarPubMed
Sasaki, A., (1994). Evolution of antigen drift/switching: continuously evading pathogens. Journal of Theoretical Biology 168, 291–308.CrossRefGoogle ScholarPubMed
Semenov, M. A., & Terkel, D. A., (1985). On the evolution of the mechanisms of genetic variability by indirect action of selection. Zhurnal Obshchej Biologii 46, 271–277 (in Russian).Google Scholar
Shapiro, N. I., (1938). The mutation process as an adaptive character of a species. Zoologicheskij Zhurnal 17, 592–601 (in Russian).Google Scholar
Shapiro, N. I., & Ignatiev, M. V., (1945). Evolution of mutability. Uspekhi Sovremennoj Biologii 20, 325–344 (in Russian).Google Scholar
Slatkin, M., (1972). On treating the chromosome as the unit of selection. Genetics 72, 157–168.CrossRefGoogle ScholarPubMed
Sturtevant, A. H., (1937). Essays on evolution. I. On the effects of selection on mutation rate. Quarterly Review of Biology 12, 464–467.CrossRefGoogle Scholar
Twomey, M. J., & Feldman, M. W., (1990). Mutation modification with multiplicative fertility selection. Theoretical Population Biology 37, 320–342.CrossRefGoogle ScholarPubMed
Uyenoyama, M. K., & Waller, D. M., (1991). Coevolution of self-fertilization and inbreeding depression. III. Homozygous lethal mutations at multiple loci. Theoretical Population Biology 40, 173–210.CrossRefGoogle ScholarPubMed
Wiener, P., & Feldman, M. W., (1993). The effects of the mating systems on the evolution of migration in a spatially heterogeneous population. Evolutionary Ecology 7, 251–269.CrossRefGoogle Scholar
Woodruff, R. C., Thompson, J. N., Seeger, M. A., & Spivey, W. E., (1984). Variation in spontaneous mutation and repair in natural population lines of Drosophila melanogaster. Heredity 53, 223–234.CrossRefGoogle Scholar