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. 1995 Feb;139(2):767–779. doi: 10.1093/genetics/139.2.767

Spontaneous Mutation Rate of Modifiers of Metabolism in Drosophila

A G Clark 1, L Wang 1, T Hulleberg 1
PMCID: PMC1206380  PMID: 7713431

Abstract

A rigorous test of our understanding of evolutionary quantitative genetics would be to predict accurately the equilibrium distribution of a character from empirical estimates of the relevant parameters in a mutation-selection-drift balance model. an aspect of this problem that is amenable to experimental analysis is the distribution of the effects of new mutations. This study quantifies the divergence among 200 lines of Drosophila melanogaster as they accumulated mutations on the second chromosome and estimates the rate of increase of variation and covariation in metabolic characters. Amounts of stored triacylglycerol and glycogen and the activities of a series of 12 metabolic enzymes were assayed in a subset of lines at generations 0, 11, 22, 33 and 44. Analyses of the rate of increase in the among-line variance in each trait allowed estimation of V(m)/V(e), the ratio of among-line variance added per generation to the environmental variance. Values of V(m)/V(e) for the second chromosome ranged from 0.0004 to 0.0289 per generation. Six of the 16 characters showed significant departure from a normal distribution, and several lines exhibited large changes in more than one character. The covariance of pairs of traits also was partitioned into a within-line component (environmental covariance, Cov(e)) and an among-line component (mutational covariance, Cov(m)). Both variances and covariance among lines increased over time, as assessed by linear regression, whereas environmental covariance showed no such trend. Results indicate that the quantitative genetic parameters describing the variation in metabolic traits are similar to those of other continuous characters.

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Selected References

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  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. The maintenance of polygenic variation through a balance between mutation and stabilizing selection. Genet Res. 1986 Jun;47(3):209–216. doi: 10.1017/s0016672300023156. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. Beaumont M. A. Stabilizing selection and metabolism. Heredity (Edinb) 1988 Dec;61(Pt 3):433–438. doi: 10.1038/hdy.1988.135. [DOI] [PubMed] [Google Scholar]
  6. Bulmer M. G. The genetic variability of polygenic characters under optimizing selection, mutation and drift. Genet Res. 1972 Feb;19(1):17–25. doi: 10.1017/s0016672300014221. [DOI] [PubMed] [Google Scholar]
  7. Bürger R. Linkage and the maintenance of heritable variation by mutation-selection balance. Genetics. 1989 Jan;121(1):175–184. doi: 10.1093/genetics/121.1.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Clark A. G., Keith L. E. Variation among extracted lines of Drosophila melanogaster in triacylglycerol and carbohydrate storage. Genetics. 1988 Jul;119(3):595–607. doi: 10.1093/genetics/119.3.595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Crawford D. L., Powers D. A. Evolutionary adaptation to different thermal environments via transcriptional regulation. Mol Biol Evol. 1992 Sep;9(5):806–813. doi: 10.1093/oxfordjournals.molbev.a040762. [DOI] [PubMed] [Google Scholar]
  10. Eggleston W. B., Johnson-Schlitz D. M., Engels W. R. P-M hybrid dysgenesis does not mobilize other transposable element families in D. melanogaster. Nature. 1988 Jan 28;331(6154):368–370. doi: 10.1038/331368a0. [DOI] [PubMed] [Google Scholar]
  11. Hartl D. L., Dykhuizen D. E., Dean A. M. Limits of adaptation: the evolution of selective neutrality. Genetics. 1985 Nov;111(3):655–674. doi: 10.1093/genetics/111.3.655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Labate J., Eanes W. F. Direct measurement of in vivo flux differences between electrophoretic variants of G6PD from Drosophila melanogaster. Genetics. 1992 Nov;132(3):783–787. doi: 10.1093/genetics/132.3.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lande R. The maintenance of genetic variability by mutation in a polygenic character with linked loci. Genet Res. 1975 Dec;26(3):221–235. doi: 10.1017/s0016672300016037. [DOI] [PubMed] [Google Scholar]
  15. Laurie-Ahlberg C. C., Barnes P. T., Curtsinger J. W., Emigh T. H., Karlin B., Morris R., Norman R. A., Wilton A. N. Genetic variability of flight metabolism in Drosophila melanogaster. II. Relationship between power output and enzyme activity levels. Genetics. 1985 Dec;111(4):845–868. doi: 10.1093/genetics/111.4.845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Laurie-Ahlberg C. C., Maroni G., Bewley G. C., Lucchesi J. C., Weir B. S. Quantitative genetic variation of enzyme activities in natural populations of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1980 Feb;77(2):1073–1077. doi: 10.1073/pnas.77.2.1073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Laurie-Ahlberg C. C., Wilton A. N., Curtsinger J. W., Emigh T. H. Naturally occurring enzyme activity variation in Drosophila melanogaster. I. Sources of variation for 23 enzymes. Genetics. 1982 Oct;102(2):191–206. doi: 10.1093/genetics/102.2.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. López M. A., López-Fanjul C. Spontaneous mutation for a quantitative trait in Drosophila melanogaster. I. Response to artificial selection. Genet Res. 1993 Apr;61(2):107–116. doi: 10.1017/s0016672300031219. [DOI] [PubMed] [Google Scholar]
  19. Mackay T. F. Transposable element-induced response to artificial selection in Drosophila melanogaster. Genetics. 1985 Oct;111(2):351–374. doi: 10.1093/genetics/111.2.351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Miyashita N., Laurie-Ahlberg C. C. Genetical analysis of chromosomal interaction effects on the activities of the glucose 6-phosphate and 6-phosphogluconate dehydrogenases in Drosophila melanogaster. Genetics. 1984 Apr;106(4):655–668. doi: 10.1093/genetics/106.4.655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. Nagylaki T. The maintenance of genetic variability in two-locus models of stabilizing selection. Genetics. 1989 May;122(1):235–248. doi: 10.1093/genetics/122.1.235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Santiago E., Albornoz J., Domínguez A., Toro M. A., López-Fanjul C. The distribution of spontaneous mutations on quantitative traits and fitness in Drosophila melanogaster. Genetics. 1992 Nov;132(3):771–781. doi: 10.1093/genetics/132.3.771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Slatkin M., Frank S. A. The quantitative genetic consequences of pleiotropy under stabilizing and directional selection. Genetics. 1990 May;125(1):207–213. doi: 10.1093/genetics/125.1.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Szathmáry E. Do deleterious mutations act synergistically? Metabolic control theory provides a partial answer. Genetics. 1993 Jan;133(1):127–132. doi: 10.1093/genetics/133.1.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Thomson M. S., Jacobson J. W., Laurie C. C. Comparison of alcohol dehydrogenase expression in Drosophila melanogaster and D. simulans. Mol Biol Evol. 1991 Jan;8(1):31–48. doi: 10.1093/oxfordjournals.molbev.a040630. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Watt W. B. Allozymes in evolutionary genetics: self-imposed burden or extraordinary tool? Genetics. 1994 Jan;136(1):11–16. doi: 10.1093/genetics/136.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]

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