Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1996 Jul;143(3):1467–1483. doi: 10.1093/genetics/143.3.1467

Comparing Mutational Variabilities

D Houle 1, B Morikawa 1, M Lynch 1
PMCID: PMC1207413  PMID: 8807316

Abstract

We have reviewed the available data on V(M), the amount of genetic variation in phenotypic traits produced each generation by mutation. We use these data to make several qualitative tests of the mutation-selection balance hypothesis for the maintenance of genetic variance (MSB). To compare V(M) values, we use three dimensionless quantities: mutational heritability, V(M)/V(E); the mutational coefficient of variation, CV(M); and the ratio of the standing genetic variance to V(M), V(G)/V(M). Since genetic coefficients of variation for life history traits are larger than those for morphological traits, we predict that under MSB, life history traits should also have larger CV(M). This is confirmed; life history traits have a median CV(M) value more than six times higher than that for morphological traits. V(G)/V(M) approximates the persistence time of mutations under MSB in an infinite population. In order for MSB to hold, V(G)/V(M) must be small, substantially less than 1000, and life history traits should have smaller values than morphological traits. V(G)/V(M) averages about 50 generations for life history traits and 100 generations for morphological traits. These observations are all consistent with the predictions of a mutation-selection balance model.

Full Text

The Full Text of this article is available as a PDF (5.1 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Barton N. H. Pleiotropic models of quantitative variation. Genetics. 1990 Mar;124(3):773–782. doi: 10.1093/genetics/124.3.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barton N. H., Turelli M. Evolutionary quantitative genetics: how little do we know? Annu Rev Genet. 1989;23:337–370. doi: 10.1146/annurev.ge.23.120189.002005. [DOI] [PubMed] [Google Scholar]
  3. CROW J. F. Some possibilities for measuring selection intensities in man. Hum Biol. 1958 Feb;30(1):1–13. [PubMed] [Google Scholar]
  4. Caballero A., Keightley P. D., Hill W. G. Accumulation of mutations affecting body weight in inbred mouse lines. Genet Res. 1995 Apr;65(2):145–149. doi: 10.1017/s0016672300033152. [DOI] [PubMed] [Google Scholar]
  5. Cardellino R. A., Mukai T. Mutator factors and genetic variance components of viability in Drosophila melanogaster. Genetics. 1975 Jul;(3):567–583. doi: 10.1093/genetics/80.3.567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cowley D. E., Atchley W. R., Rutledge J. J. Quantitative Genetics of DROSOPHILA MELANOGASTER. I. Sexual Dimorphism in Genetic Parameters for Wing Traits. Genetics. 1986 Oct;114(2):549–566. doi: 10.1093/genetics/114.2.549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Coyne J. A., Beecham E. Heritability of two morphological characters within and among natural populations of Drosophila melanogaster. Genetics. 1987 Dec;117(4):727–737. doi: 10.1093/genetics/117.4.727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Crow J. F. Minor viability mutants in Drosophila. Genetics. 1979 May;92(1 Pt 1 Suppl):s165–s172. [PubMed] [Google Scholar]
  9. DURRANT A., MATHER K. Heritable variation in a long inbred line of Drosophila. Genetica. 1954;27(1-2):97–119. doi: 10.1007/BF01664156. [DOI] [PubMed] [Google Scholar]
  10. Falconer D. S. Replicated selection for body weight in mice. Genet Res. 1973 Dec;22(3):291–321. doi: 10.1017/s0016672300013094. [DOI] [PubMed] [Google Scholar]
  11. Festing M. A multivariate analysis of subline divergence in the shape of the mandible in C57BL-Gr mice. Genet Res. 1973 Apr;21(2):121–132. doi: 10.1017/s0016672300013306. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. Houle D. Comparing evolvability and variability of quantitative traits. Genetics. 1992 Jan;130(1):195–204. doi: 10.1093/genetics/130.1.195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Houle D., Hughes K. A., Hoffmaster D. K., Ihara J., Assimacopoulos S., Canada D., Charlesworth B. The effects of spontaneous mutation on quantitative traits. I. Variances and covariances of life history traits. Genetics. 1994 Nov;138(3):773–785. doi: 10.1093/genetics/138.3.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Keightley P. D., Mackay T. F., Caballero A. Accounting for bias in estimates of the rate of polygenic mutation. Proc Biol Sci. 1993 Sep 22;253(1338):291–296. doi: 10.1098/rspb.1993.0116. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Kondrashov A. S., Turelli M. Deleterious mutations, apparent stabilizing selection and the maintenance of quantitative variation. Genetics. 1992 Oct;132(2):603–618. doi: 10.1093/genetics/132.2.603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Leamy L. Heritability of osteometric traits in a randombred population of mice. J Hered. 1974 Mar-Apr;65(2):109–120. doi: 10.1093/oxfordjournals.jhered.a108469. [DOI] [PubMed] [Google Scholar]
  21. Li W. H., Nei M. Total number of individuals affected by a single deleterious mutation in a finite population. Am J Hum Genet. 1972 Nov;24(6 Pt 1):667–679. [PMC free article] [PubMed] [Google Scholar]
  22. Lynch M. The rate of polygenic mutation. Genet Res. 1988 Apr;51(2):137–148. doi: 10.1017/s0016672300024150. [DOI] [PubMed] [Google Scholar]
  23. López M. A., López-Fanjul C. Spontaneous mutation for a quantitative trait in Drosophila melanogaster. II. Distribution of mutant effects on the trait and fitness. Genet Res. 1993 Apr;61(2):117–126. doi: 10.1017/s0016672300031220. [DOI] [PubMed] [Google Scholar]
  24. Mackay T. F., Fry J. D., Lyman R. F., Nuzhdin S. V. Polygenic mutation in Drosophila melanogaster: estimates from response to selection of inbred strains. Genetics. 1994 Mar;136(3):937–951. doi: 10.1093/genetics/136.3.937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Meyer K., Hill W. G. Mixed model analysis of a selection experiment for food intake in mice. Genet Res. 1991 Feb;57(1):71–81. doi: 10.1017/s0016672300029062. [DOI] [PubMed] [Google Scholar]
  26. Mousseau T. A., Roff D. A. Natural selection and the heritability of fitness components. Heredity (Edinb) 1987 Oct;59(Pt 2):181–197. doi: 10.1038/hdy.1987.113. [DOI] [PubMed] [Google Scholar]
  27. Mukai T., Chigusa S. I., Kusakabe S. The Genetic Structure of Natural Populations of DROSOPHILA MELANOGASTER. Xv. Nature of Developmental Homeostasis for Viability. Genetics. 1982 Jun;101(2):279–300. doi: 10.1093/genetics/101.2.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Mukai T., Chigusa S. I., Mettler L. E., Crow J. F. Mutation rate and dominance of genes affecting viability in Drosophila melanogaster. Genetics. 1972 Oct;72(2):335–355. doi: 10.1093/genetics/72.2.335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Mukai T., Harada K., Yoshimaru H. Spontaneous mutations modifying the activity of alcohol dehydrogenase (ADH) in Drosophila melanogaster. Genetics. 1984 Jan;106(1):73–84. doi: 10.1093/genetics/106.1.73. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Nuzhdin S. V., Fry J. D., Mackay T. F. Polygenic mutation in Drosophila melanogaster: the causal relationship of bristle number to fitness. Genetics. 1995 Feb;139(2):861–872. doi: 10.1093/genetics/139.2.861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ohnishi O. Spontaneous and ethyl methanesulfonate-induced mutations controlling viability in Drosophila melanogaster. III. Heterozygous effect of polygenic mutations. Genetics. 1977 Nov;87(3):547–556. doi: 10.1093/genetics/87.3.547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Roff D. A., Mousseau T. A. Quantitative genetics and fitness: lessons from Drosophila. Heredity (Edinb) 1987 Feb;58(Pt 1):103–118. doi: 10.1038/hdy.1987.15. [DOI] [PubMed] [Google Scholar]
  33. Rose M. R., Charlesworth B. Genetics of life history in Drosophila melanogaster. I. Sib analysis of adult females. Genetics. 1981 Jan;97(1):173–186. doi: 10.1093/genetics/97.1.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. SEN B. K., ROBERTSON A. AN EXPERIMENTAL EXAMINATION OF METHODS FOR THE SIMULTANEOUS SELECTION OF TWO CHARACTERS, USING DROSOPHILA MELANOGASTER. Genetics. 1964 Jul;50:199–209. doi: 10.1093/genetics/50.1.199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Scheinberg E., Bell A. E., Anderson V. L. Genetic Gain in Populations of TRIBOLIUM CASTANEUM under Uni-Stage Tandem Selection and under Restricted Selection Indices. Genetics. 1967 Jan;55(1):69–90. doi: 10.1093/genetics/55.1.69. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. Sprague G. F., Russell W. A., Penny L. H. Mutations Affecting Quantitative Traits in the Selfed Progeny of Doubled Monoploid Maize Stocks. Genetics. 1960 Jul;45(7):855–866. doi: 10.1093/genetics/45.7.855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. TANTAWY A. O., RAKHA F. A. STUDIES ON NATURAL POPULATIONS OF DROSOPHILA. IV. GENETIC VARIANCES OF AND CORRELATIONS BETWEEN FOUR CHARACTERS IN D. MELANOGASTER AND D. SIMULANS. Genetics. 1964 Dec;50:1349–1355. doi: 10.1093/genetics/50.6.1349. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES