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Mutation accumulation in finite outbreeding and inbreeding populations

  • D. Charlesworth (a1), M. T. Morgan (a1) and B. Charlesworth (a1)

We have carried out an investigation of the effects of various parameters on the accumulation of deleterious mutant alleles in finite diploid populations. Two different processes contribute to mutation accumulation. In random-mating populations of very small size and with tight linkage, fixation of mutant alleles occurs at a high rate, but decreases with extremely tight linkage. With very restricted recombination, the numbers of low-frequency mutant alleles per genome in randommating populations increase over time independently of fixation (Muller's ratchet). Increased population size affects the ratchet less than the fixation process, and the decline in population fitness is dominated by the ratchet in populations of size greater than about 100, especially with high mutation rates. The effects of differences in the selection parameters (strength of selection, dominance coefficient), of multiplicative versus synergistic selection, and of different amounts of inbreeding, are complex, but can be interpreted in terms of opposing effects of selection on individual loci and associations between loci. Stronger selection slows the accumulation of mutations, though a faster decline in mean fitness sometimes results. Increasing dominance tends to have a similar effect to greater strength of selection. High inbreeding slows the ratchet, because the increased homozygous expression of mutant alleles in inbred populations has effects similar to stronger selection, and because with inbreeding there is a higher initial frequency of the least loaded class. Fixation of deleterious mutations is accelerated in highly inbred populations. Even with inbreeding, sexual populations larger than 100 will probably rarely experience mutation accumulation to the point that their survival is endangered because neither fixation nor the ratchet has effects of the magnitude seen in asexual populations. The effects of breeding system and rate of recombination on the rate of molecular evolution by the fixation of slightly deleterious alleles are discussed.

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Attwood K. C, Schneider L. K. & Ryan F. J. (1951). Selective mechanisms in bacteria. Cold Spring Harbor Symposium on Quantitative Biology 16, 345355.
Avise J. C, Trexler J. C, Travis J. & Nelson W. S. (1991). Poecilia mexicana is the female parent of the unisexual fish. P. formosa. Evolution 45, 15301533.
Bell G. (1988). Recombination and the immortality of the germ line. Journal of Evolutionary Biology 1, 6782.
Birky C. W. & Walsh J. B. (1988). Effects of linkage on rates of molecular evolution. Proceedings of the National Academy of Sciences of the USA 85, 64146418.
Chao L., Tran T. & Matthews C. (1992). Muller's ratchet and the advantage of sex in the RNA virus f6. Evolution 46, 289299.
Charlesworth B. (1978). A model for the evolution of Y chromosomes and dosage compensation. Proceedings of the National Academy of Sciences of the USA 75, 56185622.
Charlesworth B. (1992). Evolutionary rates in partially selffertilizing species. American Naturalist 140, 126148.
Charlesworth B., Morgan M. T. & Charlesworth D. (1991). Multilocus models of inbreeding depression with synergistic selection and partial self-fertilisation. Genetical Research (Cambridge) 57, 177194.
Charlesworth B., Morgan M. T. & Charlesworth D. (1992). The effect of deleterious mutations on neutral molecular variation. In preparation.
Charlesworth D., Morgan M. T. & Charlesworth B. (1990). Inbreeding depression, genetic load and the evolution of outcrossing rates in a multi-locus system with no linkage. Evolution 44, 14691489.
Charlesworth D., Morgan M. T. & Charlesworth B. (1992). The effect of linkage and population size on inbreeding depression due to mutational load. Genetical Research (Cambridge) 59, 4961.
Crow J. F. (1948). Alternative hypotheses for hybrid vigor. Genetics 33, 477487.
Crow J. F. (1970). Genetic loads and the cost of natural selection. In Mathematical Models in Population Genetics (ed. Kojima K.-I.), pp. 128177. Berlin: Springer-Verlag.
Crow J. F. & Simmons M. J. (1983). The mutation load in Drosophila. In The Genetics and Biology of Drosophila (ed. Ashburner M., Carson H. L. & Thompson J. N.), pp. 135. London: Academic Press.
Felsenstein J. (1974). The evolutionary advantage of recombination. Genetics 78, 737756.
Fisher R. A. (1949). The Theory of Inbreeding. London: Oliver & Boyd.
Fraser A. S. & Burnell D. (1970). Computer Models in Genetics. New York: McGraw- Hill.
Gillespie J. H. (1991). The Causes of Molecular Evolution. Oxford: Oxford University Press.
Haigh J. (1978). The accumulation of deleterious genes in a population. Theoretical Population Biology 14, 251267.
Haldane J. B. S. (1950). The association of characters as a result of inbreeding and linkage. Annals of Eugenics 15, 1523.
Heller J. & Maynard Smith J. (1979). Does Muller's ratchet work with selfing? Genetical Research (Cambridge) 32, 289293.
Hill W. G. & Robertson A. (1966). The effect of linkage on limits to artificial selection. Genetical Research (Cambridge) 8, 269294.
Houle D., Hoffmaster D. K., Assimacopoulos S., and Charlesworth B. (1992). The genomic rate of mutation for fitness in Drosophila. Nature 359, 5860.
Kimura M. & Maruyama T. (1966). The mutational load with epistatic gene interactions in fitness. Genetics 54, 13371351.
Kimura M., Maruyama T. & Crow J. F. (1963). The mutational load in small populations. Genetics 48, 13031312.
Kondrashov A. S. (1985). Deleterious mutation as an evolutionary factor. II. Facultative apomixis and selfing. Genetics HI, 635653.
Leslie J. F., and Vrijenhoek R. C. (1978). Genetic dissection of the clonally inherited genome of Poeciliopsis. I. Linkage and preliminary assessment of genetic loads. Genetics 90, 801811.
Li W.-H. (1987). Models of nearly neutral mutations with particular implications for nonrandom usage of synonymous codons. Journal of Molecular Evolution 24, 337345.
Lynch M. & Gabriel W. (1990). Mutation load and the survival of small population. Evolution 44, 17251737.
Manning J. T. (1983). The consequences of mutation in multi-clonal asexual species. Heredity 50, 1519.
Maynard Smith J. (1978). The Evolution of Sex. Cambridge: Cambridge University Press.
Maynard Smith J. (1988). The evolution of recombination. In The Evolution of Sex: an Examination of Current Ideas (ed. Michod R. E. & Levin B. R.), pp. 106125. Sunderland, MA: Sinauer.
Melzer A. L. & Koeslag J. H. (1991). Mutations do not accumulate in asexual isolates capable of growth and extinction: Muller's ratchet re-examined. Evolution 45, 649655.
Mukai T., Chigusa S. I., Mettler L. E. & Crow J. F. (1972). Mutation rate and dominance of genes affecting viability. Genetics 72, 335355.
Muller H. J. (1964). The relation of recombination to mutational advance. Mutation Research 1, 29.
Nei M. (1970). Accumulation of nonfunctional genes on sheltered chromosomes. American Naturalist 104, 311322.
Ohta T. (1976). Role of very slightly deleterious mutations in molecular evolution and polymorphism. Theoretical Population Biology 10, 254275.
Pamilo P., Nei M. & Li W.-H. (1987). Accumulation of mutations in sexual and asexual populations. Genetical Research (Cambridge) 43, 135146.
Quattro J. M., Avise J. C. & Vrijenhoek R. C. (1992). An ancient clonal lineage in the fish Poeciliopsis (Atheriniformes: Poeciliidae). Proceedings of the National Academy of Sciences of the USA 89, 348352.
Spinella D. C. & Vrijenhoek R. C. (1982). Genetic dissection of the clonally inherited genome of Poeciliopsis. II. Investigation of a silent carboxylesterase allele. Genetics 100, 279286.
Sved J. & Wilton A. N. (1989). Inbreeding depression and the maintenance of deleterious genes by mutation: model of a Drosophila chromosome. Genetical Research (Cambridge) 54, 119128.
Vrijenhoek R. C, Angus R. A. & Schultz R. J. (1977). Variation and heterozygosity in sexually versus clonally reproducing populations of Poeciliopsis. Evolution 31, 767781.
Vrijenhoek R. C. (1979). Factors affecting clonal diversity and coexistence. American Zoologist 19, 787797.
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