Hostname: page-component-7c8c6479df-ph5wq Total loading time: 0 Render date: 2024-03-27T19:19:35.032Z Has data issue: false hasContentIssue false

The rate of polygenic mutation

Published online by Cambridge University Press:  14 April 2009

Michael Lynch
Affiliation:
Department of Ecology, Ethology, and Evolution, Shelford Vivarium, University of Illinois, 606 East Healey St, Champaign, IL 61820
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.

By application of the neutral model of phenotypic evolution, quantitative estimates of the rate of input of genetic variance by polygenic mutation can be extracted from divergence experiments as well as from the response of an inbred base population to selection. The analytical methods are illustrated through a survey of data on a diversity of organisms including Drosophila, Tribolium, mice, and several crop species. The mutational rate of introduction of genetic variance (Vm) scaled by the environmental variance (VE) is shown to vary between populations, species, and characters with a range of approximately 10−4 to 5 × 10−2. Vm/VE for Drosophila viability is somewhat below this range, while hybrid dysgenesis may temporarily inflate Vm/VE beyond 10−1. Potential sources of bias and error in the estimation of Vm are discussed, as are the practical implications of the observed limits to Vm/VE for projecting the long-term response to selection and for testing adaptational hypotheses.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1988

References

Abramowitz, M. & Stegun, I. A. (eds.) (1972). Handbook of Mathematical Functions. New York: Dover.Google Scholar
Bailey, D. W. (1959). Rates of subline divergence in highly inbred strains of mice. Journal of Heredity 50, 2630.CrossRefGoogle Scholar
Barton, N. H. (1986). The maintenance of polygenic variation through a balance between mutation and stabilizing selection. Genetical Research 47, 209216.CrossRefGoogle ScholarPubMed
Barton, N. H. & Turelli, M. (1987). Adaptive landscapes, genetic distance and the evolution of quantitative characters. Genetical Research 49, 157173.CrossRefGoogle ScholarPubMed
Bulmer, M. G. (1972). The genetic variability of polygenic characters under optimizing selection, mutation, and drift. Genetical Research 19, 1725.CrossRefGoogle ScholarPubMed
Bulmer, M. G. (1976). The effect of selection on genetic variability: A simulation study. Genetical Research 28, 101117.CrossRefGoogle ScholarPubMed
Bulmer, M. G. (1980). The Mathematical Theory of Quantitative Genetics. Oxford; Clarendon Press.Google Scholar
Cardellino, R. A. & Mukai, T. (1975). Mutator factors and genetic variance components of viability in Drosophila melanogaster. Genetics 80, 567583.CrossRefGoogle ScholarPubMed
Carpenter, J. R., Gruneberg, H. & Russell, E. S. (1957). Genetical differentiation involving morphological characters in an inbred strain of mice. II. American branches of the C57BL and C57BR strains. Journal of Morphology 100, 377388.CrossRefGoogle Scholar
Chakraborty, R. & Nei, M. (1982). Genetic differentiation of quantitative characters between populations or species. I. Mutation and random drift. Genetical Research 39, 303314.CrossRefGoogle Scholar
Charlesworth, B., Lande, R. & Slatkin, M. (1982). A neo Darwinian commentary on macroevolution. Evolution 36, 474498.Google ScholarPubMed
Clayton, G. A. & Robertson, A. (1955). Mutation and quantitative variation. American Naturalist 89, 151158.CrossRefGoogle Scholar
Clayton, G. A. & Robertson, A. (1964). The effects of X-rays on quantitative characters. Genetical Research 5, 410422.CrossRefGoogle Scholar
Cox, T. S., Cox, D. J. & Fregy, K. J. (1987). Mutations for polygenic traits in barley under nutrient stress. Euphytica (In the Press.)CrossRefGoogle Scholar
Deaton, W. R., Legg, P. D. & Collins, G. B. (1982). A comparison of burley tobacco doubled-haploid lines with their source cultivars. Theoretical and Applied Genetics 62, 6974.CrossRefGoogle ScholarPubMed
Deol, M. S., Gruneberg, H.Searle, A. G. & Truslove, G. M. (1957). Genetical differentiation involving morphological characters in an inbred strain of mice. I. A British branch of the C57BL strain. Journal of Morphology 100, 345375.CrossRefGoogle Scholar
Durrant, A. & Mather, K. (1954). Heritable variation in a long inbred line of Drosophila. Genetica 27, 97119.CrossRefGoogle Scholar
Enfield, F. D. (1987). Quantitative genetic variation from new mutations in Tribolium. Proceedings of the 3rd World Congress on Genetics Applied to Livestock Productions 12, 144151.Google Scholar
Enfield, F. D., Comstock, R. E. & Braskerud, O. (1966). Selection for pupa weight in Tribolium castaneum. I. Parameters in base populations. Genetics 54, 523533.CrossRefGoogle ScholarPubMed
Falconer, D. S. (1981). Introduction to Quantitative Genetics. New York: Longman.Google Scholar
Felsenstein, J. (1977). Multivariate normal genetic models with a finite number of loci. In Proceedings of the International Conference on Quantitative Genetics (ed. Pollak, E., Kempthorne, O. and Bailey, T. B. Jr.), pp. 227246. Ames, Iowa: Iowa State University Press.Google Scholar
Felsenstein, J. (1981). Continuous-genotype models and assortative mating. Theoretical Population Biology 19, 341357.CrossRefGoogle Scholar
Festing, M. F. W. (1973). A multivariate analysis of subline divergence in the shape of the mandible in C57BL/Gr mice. Genetical Research 21, 121132.CrossRefGoogle ScholarPubMed
Fleming, W. H. (1979). Equilibrium distributions of continuous polygenic traits. SIAM Journal of Applied Mathematics 36, 148168.CrossRefGoogle Scholar
Franklin, I. A. (1980). Evolutionary change in small populations. In Conservation Biology: An Evolutionary Perspective, (ed. Soulé, M. E. and Wilcox, B. A.), pp. 135149. Sunderland, Mass.: Sinauer.Google Scholar
Goodwill, R. & Enfield, F. D. (1971). Heterozygosity in inbred lines of Tribolium castaneum. Theoretical and Applied Genetics 41, 512.CrossRefGoogle Scholar
Gould, S. J. (1980). Is a new and general theory of evolution emerging? Paleobiology 6, 119130.CrossRefGoogle Scholar
Gregory, W. C. (1965). Mutation frequency, magnitude of change, and the probability of improvement in adaptation. Radiation Botany 5, (Suppl.), 429441.Google Scholar
Gruneberg, H. (1955). Genetical studies on the skeleton of the mouse. XV. Relations between major and minor variants. Journal of Genetics 53, 515535.CrossRefGoogle Scholar
Hill, W. G. (1982 a). Rate of change in quantitative traits from fixation of new mutations. Proceedings of the National Academy of Sciences of the USA 79, 142145.CrossRefGoogle ScholarPubMed
Hill, W. G. (1982 b). Predictions of response to artificial selection from new mutations. Genetical Research 40, 255278.CrossRefGoogle ScholarPubMed
Hollingdale, B. & Barker, J. S. F. (1971). Selection for increased abdominal bristle number in Drosophila melanogaster with concurrent irradiation. Theoretical and Applied Genetics 41, 208215.CrossRefGoogle ScholarPubMed
Kacser, H. & Burns, J. A. (1981). The molecular basis of dominance. Genetics 97, 639666.CrossRefGoogle ScholarPubMed
Keightley, P. D. & Hill, W. G. (1983). Effects of linkage on response to directional selection from new mutations. Genetical Research 42, 193206.CrossRefGoogle ScholarPubMed
Kimura, M. (1965). A stochastic model concerning the maintenance of genetic variability in quantitative characters. Proceedings of the National Academy of Sciences of the USA 54, 731736.CrossRefGoogle ScholarPubMed
Kitagawa, O. (1967). The effects of x-ray irradiation on selection response in Drosophila melanogaster. Japanese Journal of Genetics 42, 121137.Google Scholar
Lande, R. (1975). The maintenance of genetic variability by mutation in a polygenic character with linked loci. Genetical Research 26, 221235.CrossRefGoogle Scholar
Lande, R. (1976). Natural selection and random genetic drift in phenotypic evolution. Evolution 30, 314334.CrossRefGoogle ScholarPubMed
Lande, R. (1980). The genetic covariance between characters maintained by pleiotropic mutations. Genetics 94, 203215.CrossRefGoogle ScholarPubMed
Lange, W. (1971). Crosses between Hordeum vulgare L. and H. bulbosum L. 1. Production, morphology, and meiosis of hybrids, haploids, and dihaploids. Euphytica 20, 1429.CrossRefGoogle Scholar
Latter, B. D. H. (1970). Selection in finite populations with multiple alleles. II. Centripetal selection, mutation, and isoallelic variation. Genetics 66, 165186.CrossRefGoogle ScholarPubMed
Lynch, M. (1985). Spontaneous mutations for life history characters in an obligate parthenogen. Evolution 39, 804818.Google Scholar
Lynch, M. & Gabriel, W. (1983). Phenotypic evolution and parthenogenesis. American Naturalist 122, 745764.CrossRefGoogle Scholar
Lynch, M. & Hill, W. G. (1986). Phenotypic evolution by neutral mutation. Evolution 40, 915935.CrossRefGoogle ScholarPubMed
Mackay, T. F. C. (1985). Transposable element-induced response to artificial selection in Drosophila melanogaster. Genetics 111, 351374.CrossRefGoogle ScholarPubMed
Mackay, T. F. C. (1986). Transposable element-induced fitness mutations in Drosophila melanogaster. Genetical Research 48, 7787.CrossRefGoogle Scholar
Mackay, T. F. C. (1987). Transposable element-induced polygenic mutations in Drosophila melanogaster. Genetical Research 49, 225233.CrossRefGoogle Scholar
Mackay, T. F. C. (1988). Transposable element-induced quantitative genetic variation in Drosophila. Proceedings of the 2nd International Conference on Quantitative Genetics. (In the Press.)Google Scholar
Mather, K. & Wigan, L. G. (1942). The selection of invisible mutations. Proceedings of the Royal Society of London B 131, 5064.Google Scholar
Moll, R. H., Lindsey, M. F. & Robinson, H. F. (1964). Estimates of genetic variances and level of dominance in maize. Genetics 49, 411423.CrossRefGoogle ScholarPubMed
Mukai, T. (1964). The genetic structure of natural populations of Drosophila melanogaster. I. Spontaneous mutation rate of polygenes controlling viability. Genetics 50, 119.CrossRefGoogle ScholarPubMed
Mukai, T. (1979). Polygenic mutation, p. 177195. In Quantitative Genetic Variation (ed. Thompson, J. N. Jr. and Thoday, J. M.), pp. 177195. New York: Academic Press.CrossRefGoogle Scholar
Mukai, T., Chigusa, S. I. & Kusakaba, S.-I. (1982). The genetic structure of natural populations of Drosophila melanogaster. XV. Nature of developmental homeostasis for viability. Genetics 101, 279300.CrossRefGoogle ScholarPubMed
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, 335355.CrossRefGoogle ScholarPubMed
Mukai, T., Harada, K. & Yoshimaru, H. (1984). Spontaneous mutations modifying the activity of alcohol dehydrogenase (ADH) in Drosophila melanogaster. Genetics 106, 7384.CrossRefGoogle ScholarPubMed
Mukai, T. & Nagano, S. (1983). The genetic structure of natural populations of Drosophila melanogaster. XVI. Excess of additive genetic variance of viability. Genetics 105, 115134.CrossRefGoogle ScholarPubMed
Mukai, T. & Yamazaki, T. (1964). Position effect of spontaneous mutant polygenes controlling viability in Drosophila melanogaster. Proceedings of the Japan Academy 40, 840845.CrossRefGoogle Scholar
Mukai, T. & Yamazaki, T. (1968). The genetic structure of natural populations of Drosophila melanogaster. V. Coupling–repulsion effect of spontaneous mutant polygenes controlling viability. Genetics 59, 513535.CrossRefGoogle ScholarPubMed
Ohnishi, O. (1977 a). Spontaneous and ethyl methane-sulfonate-induced mutations controlling viability in Drosophila melanogaster. II. Homozygous effect of polygenic mutations. Genetics 87, 529545.CrossRefGoogle Scholar
Ohnishi, O. (1977 b). Spontaneous and ethyl methane-sulfonate-induced mutations controlling viability in Drosophila melanogaster. III. Heterozygous effect of polygenic mutations. Genetics 87, 547556.CrossRefGoogle Scholar
Oka, H. I., Hayashi, J. & Shiojiri, I. (1958). Induced mutations of polygenes for quantitative characters in rice. Journal of Heredity. 49, 1114.CrossRefGoogle Scholar
Paxman, G. J. (1957). A study of spontaneous mutation in Drosophila melanogaster. Genetica 29, 3957.CrossRefGoogle Scholar
Reyment, R. A. (1983). Phenotypic evolution in microfossils. Evolutionary Biology 16, 209254.CrossRefGoogle Scholar
Robertson, A. (1952). The effect of inbreeding on the variation due to recessive genes. Genetics 37, 189207.CrossRefGoogle ScholarPubMed
Robertson, A. (1962). Selection for heterozygotes in small populations. Genetics 47, 12911300.CrossRefGoogle ScholarPubMed
Russell, W. A., Sprague, G. F. & Penny, H. L. (1963). Mutations affecting quantitative characters in long-time inbred lines of maize. Crops Science 3, 175178.CrossRefGoogle Scholar
Sakai, K. I. & Suzuki, A. (1964). Induced mutation and pleiotropy of genes responsible for quantitative characters in rice. Radiation Botany 4, 141151.CrossRefGoogle Scholar
Sprague, G. F., Russell, W. A. & Penny, L. H. (1960). Mutations affecting quantitative traits in the selfed progeny of doubled monoploid maize stocks. Genetics 45, 855866.CrossRefGoogle ScholarPubMed
Turelli, M. (1984). Heritable genetic variation via mutation selection balance: Lerch's zeta meets the abdominal bristle. Theoretical Population Biology 25, 138193.CrossRefGoogle Scholar
Turelli, M. (1985). Effects of pleiotropy on predictions concerning mutation-selection balance for polygenic traits. Genetics 111, 165195.CrossRefGoogle ScholarPubMed
Turelli, M. (1986). Gaussian versus non-Gaussian genetic analyses of polygenic mutation-selection balance. In Evolutionary Processes and Theory (ed. Karlin, S. and Nevo, E.). pp. 607628. New York: Academic Press.CrossRefGoogle Scholar
Turelli, M. (1987). Population genetic models for polygenic variation and evolution. Proceedings of the 2nd International Conference on Quantitative Genetics. (In the Press.)Google Scholar
Wallace, B. (1956). Studies on irradiated populations of Drosophila melanogaster. Journal of Genetics 54, 280293.CrossRefGoogle Scholar
Yong, H.-S. (1972). Is sub-line differentiation a continuing process in inbred strains of mice? Genetical Research 19, 5359.Google Scholar
Yoshimaru, H. & Mukai, T. (1985). Relationship between the polygenes affecting the rate of development and viability in Drosophila melanogaster. Japanese Journal of Genetics 60, 307334.Google Scholar
Yukuhiro, K., Harada, K. & Mukai, T. (1985). Viability mutations induced by the P elements in Drosophila melanogaster. Japanese Journal of Genetics 60, 531537.Google Scholar
Zeng, Z.-B. & Hill, W. G. (1986). The selection limit due to the conflict between truncation and stabilizing selection with mutation. Genetics 114, 13131328.CrossRefGoogle Scholar