Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-30T20:19:55.408Z Has data issue: false hasContentIssue false
  • English
  • Français

Mutation accumulation in finite outbreeding and inbreeding populations

Published online by Cambridge University Press:  14 April 2009

D. Charlesworth ,
M. T. Morgan  and
B. Charlesworth
D. Charlesworth*
Affiliation:
Department of Ecology and Evolution, University of Chicago, 1101 E 57th St., Chicago, IL 60637
M. T. Morgan
Affiliation:
Department of Ecology and Evolution, University of Chicago, 1101 E 57th St., Chicago, IL 60637
B. Charlesworth
Affiliation:
Department of Ecology and Evolution, University of Chicago, 1101 E 57th St., Chicago, IL 60637
*
* Corresponding author.
Rights & Permissions [Opens in a new window]

Summary

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

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.

Type
Research Article
Information
Genetics Research , Volume 61 , Issue 1 , February 1993 , pp. 39 - 56
Copyright
Copyright © Cambridge University Press 1993

References

Attwood, K. C, Schneider, L. K. & Ryan, F. J. (1951). Selective mechanisms in bacteria. Cold Spring Harbor Symposium on Quantitative Biology 16, 345–355.CrossRefGoogle Scholar
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, 1530–1533.CrossRefGoogle ScholarPubMed
Bell, G. (1988). Recombination and the immortality of the germ line. Journal of Evolutionary Biology 1, 67–82.CrossRefGoogle Scholar
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, 6414–6418.CrossRefGoogle ScholarPubMed
Chao, L., Tran, T. & Matthews, C. (1992). Muller's ratchet and the advantage of sex in the RNA virus f6. Evolution 46, 289–299.Google Scholar
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, 5618–5622.CrossRefGoogle Scholar
Charlesworth, B. (1992). Evolutionary rates in partially selffertilizing species. American Naturalist 140, 126–148.Google Scholar
Charlesworth, B., Morgan, M. T. & Charlesworth, D. (1991). Multilocus models of inbreeding depression with synergistic selection and partial self-fertilisation. Genetical Research (Cambridge) 57, 177–194.Google Scholar
Charlesworth, B., Morgan, M. T. & Charlesworth, D. (1992). The effect of deleterious mutations on neutral molecular variation. In preparation.Google Scholar
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, 1469–1489.CrossRefGoogle Scholar
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, 49–61.Google Scholar
Crow, J. F. (1948). Alternative hypotheses for hybrid vigor. Genetics 33, 477–487.CrossRefGoogle ScholarPubMed
Crow, J. F. (1970). Genetic loads and the cost of natural selection. In Mathematical Models in Population Genetics (ed. Kojima, K.-I.), pp. 128–177. Berlin: Springer-Verlag.CrossRefGoogle Scholar
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. 1–35. London: Academic Press.Google Scholar
Felsenstein, J. (1974). The evolutionary advantage of recombination. Genetics 78, 737–756.Google Scholar
Fisher, R. A. (1949). The Theory of Inbreeding. London: Oliver & Boyd.Google Scholar
Fraser, A. S. & Burnell, D. (1970). Computer Models in Genetics. New York: McGraw- Hill.Google Scholar
Gillespie, J. H. (1991). The Causes of Molecular Evolution. Oxford: Oxford University Press.Google Scholar
Haigh, J. (1978). The accumulation of deleterious genes in a population. Theoretical Population Biology 14, 251–267.CrossRefGoogle ScholarPubMed
Haldane, J. B. S. (1950). The association of characters as a result of inbreeding and linkage. Annals of Eugenics 15, 15–23.Google Scholar
Heller, J. & Maynard, Smith J. (1979). Does Muller's ratchet work with selfing? Genetical Research (Cambridge) 32, 289–293.CrossRefGoogle Scholar
Hill, W. G. & Robertson, A. (1966). The effect of linkage on limits to artificial selection. Genetical Research (Cambridge) 8, 269–294.CrossRefGoogle ScholarPubMed
Houle, D., Hoffmaster, D. K., Assimacopoulos, S., and Charlesworth, B. (1992). The genomic rate of mutation for fitness in Drosophila. Nature 359, 58–60.CrossRefGoogle ScholarPubMed
Kimura, M. & Maruyama, T. (1966). The mutational load with epistatic gene interactions in fitness. Genetics 54, 1337–1351.CrossRefGoogle ScholarPubMed
Kimura, M., Maruyama, T. & Crow, J. F. (1963). The mutational load in small populations. Genetics 48, 1303–1312.CrossRefGoogle ScholarPubMed
Kondrashov, A. S. (1985). Deleterious mutation as an evolutionary factor. II. Facultative apomixis and selfing. Genetics HI, 635–653.CrossRefGoogle ScholarPubMed
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, 801–811.Google Scholar
Li, W.-H. (1987). Models of nearly neutral mutations with particular implications for nonrandom usage of synonymous codons. Journal of Molecular Evolution 24, 337–345.Google Scholar
Lynch, M. & Gabriel, W. (1990). Mutation load and the survival of small population. Evolution 44, 1725–1737.CrossRefGoogle Scholar
Manning, J. T. (1983). The consequences of mutation in multi-clonal asexual species. Heredity 50, 15–19.Google Scholar
Maynard, Smith J. (1978). The Evolution of Sex. Cambridge: Cambridge University Press.Google Scholar
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. 106–125. Sunderland, MA: Sinauer.Google Scholar
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, 649–655.Google Scholar
Mukai, T., Chigusa, S. I., Mettler, L. E. & Crow, J. F. (1972). Mutation rate and dominance of genes affecting viability. Genetics 72, 335–355.Google Scholar
Muller, H. J. (1964). The relation of recombination to mutational advance. Mutation Research 1, 2–9.CrossRefGoogle Scholar
Nei, M. (1970). Accumulation of nonfunctional genes on sheltered chromosomes. American Naturalist 104, 311–322.Google Scholar
Ohta, T. (1976). Role of very slightly deleterious mutations in molecular evolution and polymorphism. Theoretical Population Biology 10, 254–275.Google Scholar
Pamilo, P., Nei, M. & Li, W.-H. (1987). Accumulation of mutations in sexual and asexual populations. Genetical Research (Cambridge) 43, 135–146.Google Scholar
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, 348–352.Google Scholar
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, 279–286.CrossRefGoogle ScholarPubMed
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, 119–128.Google Scholar
Vrijenhoek, R. C, Angus, R. A. & Schultz, R. J. (1977). Variation and heterozygosity in sexually versus clonally reproducing populations of Poeciliopsis. Evolution 31, 767–781.Google Scholar
Vrijenhoek, R. C. (1979). Factors affecting clonal diversity and coexistence. American Zoologist 19, 787–797.CrossRefGoogle Scholar