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Mutation-selection balance and the evolutionary advantage of sex and recombination

Published online by Cambridge University Press:  14 April 2009

Brian Charlesworth
Affiliation:
Department of Ecology and Evolution, The University of Chicago, 1103 E. 57th St, Chicago, IL 60637, USA
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Mutation-selection balance in a multi-locus system is investigated theoretically, using a modification of Bulmer's infinitesimal model of selection on a normally-distributed quantitative character, taking the number of mutations per individual (n) to represent the character value. The logarithm of the fitness of an individual with n mutations is assumed to be a quadratic, decreasing function of n. The equilibrium properties of infinitely large asexual populations, random-mating populations lacking genetic recombination, and random-mating populations with arbitrary recombination frequencies are investigated. With ‘synergistic’ epistasis on the scale of log fitness, such that log fitness declines more steeply as n increases, it is shown that equilibrium mean fitness is least for asexual populations. In sexual populations, mean fitness increases with the number of chromosomes and with the map length per chromosome. With ‘diminishing returns’ epistasis, such that log fitness declines less steeply as n increases, mean fitness behaves in the opposite way. Selection on asexual variants and genes affecting the rate of genetic recombination in random-mating populations was also studied. With synergistic epistasis, zero recombination always appears to be disfavoured, but free recombination is disfavoured when the mutation rate per genome is sufficiently small, leading to evolutionary stability of maps of intermediate length. With synergistic epistasis, an asexual mutant is unlikely to invade a sexual population if the mutation rate per diploid genome greatly exceeds unity. Recombination is selectively disadvantageous when there is diminishing returns epistasis. These results are compared with the results of previous theoretical studies of this problem, and with experimental data.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1990

References

Altenberg, L. & Feldman, M. W. (1987). Selection, generalized transmission and the evolution of modifier genes. I. The reduction principle. Genetics 117, 559572.CrossRefGoogle ScholarPubMed
Barton, N. H. & Post, R. J. (1986). Sibling competition and the advantage of mixed families. Journal of Theoretical Biology 120, 381387.CrossRefGoogle Scholar
Bell, G. (1982). The Masterpiece of Nature. London, Croom-Helm.Google Scholar
Brooks, L. D. (1988). The evolution of recombination rates. In The Evolution of Sex (ed. Levin, B. R. and Michod, R. E.), pp. 87106. Sunderland, Mass.: Sinauer.Google Scholar
Bulmer, M. G. (1980). The Mathematical Theory of Quantitative Genetics. Oxford: Oxford University Press.Google Scholar
Cavalier-Smith, T. (1985). The Evolution of Genome Size. Chichester; John Wiley.Google Scholar
Chao, L. (1988). Evolution of sex in RNA viruses. Journal of Theoretical Biology 133, 99112.CrossRefGoogle ScholarPubMed
Charlesworth, B. (1985). Recombination, genome size and chromosome number. In The Evolution of Genome Size (ed. Cavalier-Smith, T.), pp. 489513. Chichester: John Wiley.Google Scholar
Charlesworth, B. (1989). The evolution of sex and recombination. Trends in Ecology and Evolution 4, 264267.CrossRefGoogle ScholarPubMed
Clark, A. G. (1987). A test of multilocus interaction in Drosophila melanogaster. American Naturalist 130, 283299.CrossRefGoogle Scholar
Crow, J. F. (1970). Genetic loads and the cost of natural selection. In Mathematical Topics in Population Genetics (ed. Kojima, K.), pp. 128177. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Crow, J. F. (1988). The importance of recombination. In The Evolution of Sex (ed. Levin, B. R. and Michod, R. E.), pp. 5673. Sunderland, Mass.: Sinauer.Google Scholar
Crow, J. F. & Kimura, M. (1970). An Introduction to Population Genetics Theory. New York: Harper and Row.Google Scholar
Crow, J. F. & Kimura, M. (1979). Efficiency of truncation selection. Proceedings of the National Academy of Sciences USA 76, 396399.CrossRefGoogle ScholarPubMed
Elgen, M. & Schuster, P. (1979). The Hypercycle. Berlin: Springer-Verlag.Google Scholar
Feldman, M. W., Christiansen, F. B. & Brooks, L. D. (1980). Evolution of recombination in a constant environment. Proceedings of the National Academy of Sciences USA 77, 48244827.CrossRefGoogle Scholar
Haigh, J. (1978). The accumulation of deleterious genes in a population. Theoretical Population Biology 14, 251267.CrossRefGoogle ScholarPubMed
Haldane, J. B. S. (1919). The combination of linkage values and the calculation of distance between loci of linked factors. Journal of Genetics 8, 299309.Google Scholar
Hamilton, W. D. (1980). Sex versus non-sex versus parasite. Oikos 35, 282290.CrossRefGoogle Scholar
Hopf, R., Michod, R. E. & Sanderson, M. (1987). On the effect of reproductive system on mutation load and the number of deleterious mutations. Theoretical Population Biology 33, 243265.CrossRefGoogle Scholar
Karlin, S. & McGregor, J. (1974). Towards a theory of the evolution of modifier genes. Theoretical Population Biology 5, 59103.CrossRefGoogle ScholarPubMed
Kelley, S. E., Antonovics, J. & Schmitt, J. (1988). A test of the short-term advantage of sexual reproduction. Nature 331, 714716.CrossRefGoogle Scholar
Kimura, M. & Maruyama, T. (1966). The mutational load with epistatic gene interactions in fitness. Genetics 54, 13031312.CrossRefGoogle ScholarPubMed
Kirkpatrick, M. & Jenkins, C. D. (1989). Genetic segregation and the maintenance of sexual reproduction. Nature 339, 300301.CrossRefGoogle ScholarPubMed
Kondrashov, A. S. (1982). Selection against harmful mutations in large sexual and asexual populations. Genetical Research 40, 325332.CrossRefGoogle ScholarPubMed
Kondrashov, A. S. (1984). Deleterious mutations as an evolutionary factor. I. The advantage of recombination. Genetical Research 44, 199217.CrossRefGoogle Scholar
Kondrashov, A. S. (1985). Deleterious mutations as an evolutionary factor. II. Facultative apomixis and selfing. Genetics 111, 635653.CrossRefGoogle ScholarPubMed
Kondrashov, A. S. (1988). Deleterious mutations and the evolution of sexual reproduction. Nature 336, 435440.CrossRefGoogle ScholarPubMed
Lande, R. S. (1976). Natural selection and random genetic drift in phenotypic evolution. Evolution 30, 314334.CrossRefGoogle ScholarPubMed
Lloyd, D. G. (1980). Benefits and handicaps of sexual reproduction. Evolutionary Biology 13, 69111.CrossRefGoogle Scholar
Maynard Smith, J. (1978). The Evolution of Sex. Cambridge, UK: Cambridge University Press.Google Scholar
Maynard Smith, J. (1983). Models of evolution. Proceedings of the Royal Society of London B219, 315325.Google Scholar
Michod, R. E. & Levin, B. R. (1988). The Evolution of Sex. Sunderland, Mass.: Sinauer.Google Scholar
Morton, N. E. (1955). Sequential tests for the detection of linkage. American Journal of Human Genetics 7, 277318.Google ScholarPubMed
Mukai, T. (1969). The genetic structure of natural populations of Drosophila melanogaster. VII. Synergistic interactions of spontaneous mutant polygenes affecting viability. Genetics 61, 749761.CrossRefGoogle Scholar
Nee, S. (1988). Deleterious mutation and genetic recombination. Nature 331, 308.CrossRefGoogle ScholarPubMed
Nee, S. (1989). On the evolution of sex in RNA viruses. Journal of Theoretical Biology 138, 407412.CrossRefGoogle ScholarPubMed
Nee, S. & Maynard Smith, J. (1990). The evolutionary biology of molecular parasites. Parasitology (in the press).CrossRefGoogle ScholarPubMed
Nowak, M. & Schuster, P. (1989). Error thresholds of replication in a finite population- mutation frequencies and Muller's ratchet. Journal of Theoretical Biology 137, 375398.CrossRefGoogle Scholar
Pressing, J. & Reanney, D. C. (1984). Divided genomes and intrinsic noise. Journal of Molecular Evolution 20, 135146.CrossRefGoogle ScholarPubMed
Redfield, R. J. (1988). Evolution of bacterial transformation: is sex with dead cells ever better than no sex at all? Genetics 119, 213221.CrossRefGoogle ScholarPubMed
Seager, R. D. & Ayala, F. J. (1982). Chromosome interactions in Drosophila melanogaster. I. Viability studies. Genetics 102, 467483.CrossRefGoogle ScholarPubMed
Seager, R. D., Ayala, F. J. & Marks, R. W. (1982). Chromosome interactions in Drosophila melanogaster. II. Total fitness. Genetics 102, 485502.CrossRefGoogle ScholarPubMed
Simmons, M. J. & Crow, J. F. (1977). Mutations affecting fitness in Drosophila populations. Annual Review of Genetics 11, 4978.CrossRefGoogle ScholarPubMed
Stearns, S. C. (1987). The Evolution of Sex and its Consequences. Basel: Birkhaüser.CrossRefGoogle Scholar
Thomson, G. (1977). The effect of a selected locus on linked neutral loci. Genetics 85, 753788.CrossRefGoogle ScholarPubMed
White, M. J. D. (1973). Animal Cytology and Evolution, 3rd edn.Cambridge, UK: Cambridge University Press.Google Scholar