Abstract
It is widely held that each gene typically affects many characters, and that each character is affected by many genes. Moreover, strong stabilizing selection cannot act on an indefinitely large number of independent traits. This makes it likely that heritable variation in any one trait is maintained as a side effect of polymorphisms which have nothing to do with selection on that trait. This paper examines the idea that variation is maintained as the pleiotropic side effect of either deleterious mutation, or balancing selection. If mutation is responsible, it must produce alleles which are only mildly deleterious (s & 10(-3)), but nevertheless have significant effects on the trait. Balancing selection can readily maintain high heritabilities; however, selection must be spread over many weakly selected polymorphisms if large responses to artificial selection are to be possible. In both classes of pleiotropic model, extreme phenotypes are less fit, giving the appearance of stabilizing selection on the trait. However, it is shown that this effect is weak (of the same order as the selection on each gene): the strong stabilizing selection which is often observed is likely to be caused by correlations with a limited number of directly selected traits. Possible experiments for distinguishing the alternatives are discussed.
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Selected References
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- Barton N. H., Turelli M. Adaptive landscapes, genetic distance and the evolution of quantitative characters. Genet Res. 1987 Apr;49(2):157–173. doi: 10.1017/s0016672300026951. [DOI] [PubMed] [Google Scholar]
- Bulmer M. G. The maintenance of the genetic variability of polygenic characters by heterozygous advantage. Genet Res. 1973 Aug;22(1):9–12. [PubMed] [Google Scholar]
- Davies R. W. The genetic relationship of two quantitative characters in Drosophila melanogaster. II. Location of the effects. Genetics. 1971 Nov;69(3):363–375. doi: 10.1093/genetics/69.3.363. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dobzhansky T, Holz A M. A Re-Examination of the Problem of Manifold Effects of Genes in Drosophila Melanogaster. Genetics. 1943 Jul;28(4):295–303. doi: 10.1093/genetics/28.4.295. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fisher R A, Immer F R, Tedin O. The Genetical Interpretation of Statistics of the Third Degree in the Study of Quantitative Inheritance. Genetics. 1932 Mar;17(2):107–124. doi: 10.1093/genetics/17.2.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gillespie J. H. Pleiotropic overdominance and the maintenance of genetic variation in polygenic characters. Genetics. 1984 Jun;107(2):321–330. doi: 10.1093/genetics/107.2.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gillespie J. H., Turelli M. Genotype-environment interactions and the maintenance of polygenic variation. Genetics. 1989 Jan;121(1):129–138. doi: 10.1093/genetics/121.1.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hill W. G. Predictions of response to artificial selection from new mutations. Genet Res. 1982 Dec;40(3):255–278. doi: 10.1017/s0016672300019145. [DOI] [PubMed] [Google Scholar]
- Kearsey M. U., Barnes B. W. Variation for metrical characters in Drosophila populations. II. Natural selection. Heredity (Edinb) 1970 Feb;25(1):11–21. doi: 10.1038/hdy.1970.2. [DOI] [PubMed] [Google Scholar]
- Keightley P. D., Hill W. G. Effects of linkage on response to directional selection from new mutations. Genet Res. 1983 Oct;42(2):193–206. doi: 10.1017/s0016672300021650. [DOI] [PubMed] [Google Scholar]
- Keightley P. D., Hill W. G. Quantitative genetic variability maintained by mutation-stabilizing selection balance in finite populations. Genet Res. 1988 Aug;52(1):33–43. doi: 10.1017/s0016672300027282. [DOI] [PubMed] [Google Scholar]
- Kimura M. A stochastic model concerning the maintenance of genetic variability in quantitative characters. Proc Natl Acad Sci U S A. 1965 Sep;54(3):731–736. doi: 10.1073/pnas.54.3.731. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kimura M., Crow J. F. Effect of overall phenotypic selection on genetic change at individual loci. Proc Natl Acad Sci U S A. 1978 Dec;75(12):6168–6171. doi: 10.1073/pnas.75.12.6168. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lande R. The Genetic Covariance between Characters Maintained by Pleiotropic Mutations. Genetics. 1980 Jan;94(1):203–215. doi: 10.1093/genetics/94.1.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lewontin R. C., Ginzburg L. R., Tuljapurkar S. D. Heterosis as an explanation for large amounts of genic polymorphism. Genetics. 1978 Jan;88(1):149–169. doi: 10.1093/genetics/88.1.149. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Linney R., Barnes B. W., Kearsey M. J. Variation for metrical characters in drosophila populations. 3. The nature of selection. Heredity (Edinb) 1971 Oct;27(2):163–174. doi: 10.1038/hdy.1971.82. [DOI] [PubMed] [Google Scholar]
- Lynch M. The rate of polygenic mutation. Genet Res. 1988 Apr;51(2):137–148. doi: 10.1017/s0016672300024150. [DOI] [PubMed] [Google Scholar]
- Mukai T., Nagano S. The Genetic Structure of Natural Populations of DROSOPHILA MELANOGASTER. Xvi. Excess of Additive Genetic Variance of Viability. Genetics. 1983 Sep;105(1):115–134. doi: 10.1093/genetics/105.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Simmons M. J., Crow J. F. Mutations affecting fitness in Drosophila populations. Annu Rev Genet. 1977;11:49–78. doi: 10.1146/annurev.ge.11.120177.000405. [DOI] [PubMed] [Google Scholar]
- Slatkin M. Frequency- and density-dependent selection on a quantitative character. Genetics. 1979 Nov;93(3):755–771. doi: 10.1093/genetics/93.3.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smith J. M. The genetics of stasis and punctuation. Annu Rev Genet. 1983;17:11–25. doi: 10.1146/annurev.ge.17.120183.000303. [DOI] [PubMed] [Google Scholar]
- Sved J. A., Reed T. E., Bodmer W. F. The number of balanced polymorphisms that can be maintained in a natural population. Genetics. 1967 Mar;55(3):469–481. doi: 10.1093/genetics/55.3.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tachida H., Cockerham C. C. Variance components of fitness under stabilizing selection. Genet Res. 1988 Feb;51(1):47–53. doi: 10.1017/s0016672300023934. [DOI] [PubMed] [Google Scholar]
- Turelli M. Heritable genetic variation via mutation-selection balance: Lerch's zeta meets the abdominal bristle. Theor Popul Biol. 1984 Apr;25(2):138–193. doi: 10.1016/0040-5809(84)90017-0. [DOI] [PubMed] [Google Scholar]
- Wagner G. P. Multivariate mutation-selection balance with constrained pleiotropic effects. Genetics. 1989 May;122(1):223–234. doi: 10.1093/genetics/122.1.223. [DOI] [PMC free article] [PubMed] [Google Scholar]