Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1995 Jan;139(1):337–348. doi: 10.1093/genetics/139.1.337

P-Element-Induced Variation in Metabolic Regulation in Drosophila

A G Clark 1, L Wang 1, T Hulleberg 1
PMCID: PMC1206330  PMID: 7705634

Abstract

Movement of transposable elements has been demonstrated to be a cause of genetic variation that is relevant to quantitative characters in Drosophila. Here a particular class of P-element-induced variation known to be mediated through changes in expression of targeted enzyme-encoding genes is examined. Balancer chromosomes and the ``jumpstarter'' modified P-element were used to construct 124 second-chromosome and 139 third-chromosome lines of Drosophila melanogaster bearing unique stable P-element insertions in a common genetic background. Lines that were homozygous for second-chromosome P-element insertions were significantly more heterogeneous than control lines in 10 of 16 characters, whereas third-chromosome insertion lines were heterogeneous in 11 of the 16 traits. The average mutational variance per insertion relative to environmental variance (V(m|1)/V(e)) was 5.7 X 10(-2), and estimates varied widely across characters. The distributions of mutational effects tended to be skewed, with a longer tail toward high enzyme activities. Mutational effects deviated from a normal distribution in 15 of the 16 traits and significant outlier lines were found in both a positive and negative direction in several characters. Pleiotropic effects of single P-element insertions were quantified by correlation, and, after correcting for simultaneous tests, of the 91 correlations, 37 were significant at the 5% level. The pattern of pleiotropic effects deviated both from the equilibrium genetic correlations quantified in a previous study and from the correlations of mutational effects in a mutation-accumulation experiment, suggesting that multiple forces are at play that shape extant variation.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

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

  1. Aguade M., Miyashita N., Langley C. H. Reduced variation in the yellow-achaete-scute region in natural populations of Drosophila melanogaster. Genetics. 1989 Jul;122(3):607–615. doi: 10.1093/genetics/122.3.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aguadé M., Miyashita N., Langley C. H. Restriction-map variation at the zeste-tko region in natural populations of Drosophila melanogaster. Mol Biol Evol. 1989 Mar;6(2):123–130. doi: 10.1093/oxfordjournals.molbev.a040538. [DOI] [PubMed] [Google Scholar]
  3. Aquadro C. F., Desse S. F., Bland M. M., Langley C. H., Laurie-Ahlberg C. C. Molecular population genetics of the alcohol dehydrogenase gene region of Drosophila melanogaster. Genetics. 1986 Dec;114(4):1165–1190. doi: 10.1093/genetics/114.4.1165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Aquadro C. F., Lado K. M., Noon W. A. The rosy region of Drosophila melanogaster and Drosophila simulans. I. Contrasting levels of naturally occurring DNA restriction map variation and divergence. Genetics. 1988 Aug;119(4):875–888. doi: 10.1093/genetics/119.4.875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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]
  6. 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]
  7. 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]
  8. Brown A. J. Variation at the 87A heat shock locus in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1983 Sep;80(17):5350–5354. doi: 10.1073/pnas.80.17.5350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Clark A. G. Causes and consequences of variation in energy storage in Drosophila melanogaster. Genetics. 1989 Sep;123(1):131–144. doi: 10.1093/genetics/123.1.131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Clark A. G., Keith L. E. Rapid enzyme kinetic assays of individual Drosophila and comparisons of field-caught D. melanogaster and D. simulans. Biochem Genet. 1989 Jun;27(5-6):263–277. doi: 10.1007/BF00554162. [DOI] [PubMed] [Google Scholar]
  11. Clark A. G. Mutation-selection balance and metabolic control theory. Genetics. 1991 Nov;129(3):909–923. doi: 10.1093/genetics/129.3.909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Eanes W. F., Ajioka J. W., Hey J., Wesley C. Restriction-map variation associated with the G6PD polymorphism in natural populations of Drosophila melanogaster. Mol Biol Evol. 1989 Jul;6(4):384–397. doi: 10.1093/oxfordjournals.molbev.a040555. [DOI] [PubMed] [Google Scholar]
  13. Eanes W. F., Labate J., Ajioka J. W. Restriction-map variation with the yellow-achaete-scute region in five populations of Drosophila melanogaster. Mol Biol Evol. 1989 Sep;6(5):492–502. doi: 10.1093/oxfordjournals.molbev.a040565. [DOI] [PubMed] [Google Scholar]
  14. Hazelrigg T., Levis R., Rubin G. M. Transformation of white locus DNA in drosophila: dosage compensation, zeste interaction, and position effects. Cell. 1984 Feb;36(2):469–481. doi: 10.1016/0092-8674(84)90240-x. [DOI] [PubMed] [Google Scholar]
  15. Hazelrigg T., Petersen S. An unusual genomic position effect on Drosophila white gene expression: pairing dependence, interactions with zeste, and molecular analysis of revertants. Genetics. 1992 Jan;130(1):125–138. doi: 10.1093/genetics/130.1.125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Houle D., Hoffmaster D. K., Assimacopoulos S., Charlesworth B. The genomic mutation rate for fitness in Drosophila. Nature. 1992 Sep 3;359(6390):58–60. doi: 10.1038/359058a0. [DOI] [PubMed] [Google Scholar]
  17. Kacser H., Burns J. A. The molecular basis of dominance. Genetics. 1981 Mar-Apr;97(3-4):639–666. doi: 10.1093/genetics/97.3-4.639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Keightley P. D., Kacser H. Dominance, pleiotropy and metabolic structure. Genetics. 1987 Oct;117(2):319–329. doi: 10.1093/genetics/117.2.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Keightley P. D. Models of quantitative variation of flux in metabolic pathways. Genetics. 1989 Apr;121(4):869–876. doi: 10.1093/genetics/121.4.869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lai C. Q., Mackay T. F. Hybrid dysgenesis-induced quantitative variation on the X chromosome of Drosophila melanogaster. Genetics. 1990 Mar;124(3):627–636. doi: 10.1093/genetics/124.3.627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Langley C. H., Montgomery E., Hudson R., Kaplan N., Charlesworth B. On the role of unequal exchange in the containment of transposable element copy number. Genet Res. 1988 Dec;52(3):223–235. doi: 10.1017/s0016672300027695. [DOI] [PubMed] [Google Scholar]
  24. Laski F. A., Rio D. C., Rubin G. M. Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing. Cell. 1986 Jan 17;44(1):7–19. doi: 10.1016/0092-8674(86)90480-0. [DOI] [PubMed] [Google Scholar]
  25. Lynch M. The rate of polygenic mutation. Genet Res. 1988 Apr;51(2):137–148. doi: 10.1017/s0016672300024150. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Mackay T. F., Langley C. H. Molecular and phenotypic variation in the achaete-scute region of Drosophila melanogaster. Nature. 1990 Nov 1;348(6296):64–66. doi: 10.1038/348064a0. [DOI] [PubMed] [Google Scholar]
  28. Mackay T. F., Lyman R. F., Jackson M. S. Effects of P element insertions on quantitative traits in Drosophila melanogaster. Genetics. 1992 Feb;130(2):315–332. doi: 10.1093/genetics/130.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Miyashita N., Langley C. H. Molecular and phenotypic variation of the white locus region in Drosophila melanogaster. Genetics. 1988 Sep;120(1):199–212. doi: 10.1093/genetics/120.1.199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pirrotta V. Vectors for P-mediated transformation in Drosophila. Biotechnology. 1988;10:437–456. doi: 10.1016/b978-0-409-90042-2.50028-3. [DOI] [PubMed] [Google Scholar]
  32. Robertson H. M., Preston C. R., Phillis R. W., Johnson-Schlitz D. M., Benz W. K., Engels W. R. A stable genomic source of P element transposase in Drosophila melanogaster. Genetics. 1988 Mar;118(3):461–470. doi: 10.1093/genetics/118.3.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Schaeffer S. W., Aquadro C. F., Langley C. H. Restriction-map variation in the Notch region of Drosophila melanogaster. Mol Biol Evol. 1988 Jan;5(1):30–40. doi: 10.1093/oxfordjournals.molbev.a040475. [DOI] [PubMed] [Google Scholar]
  34. Wilton A. N., Laurie-Ahlberg C. C., Emigh T. H., Curtsinger J. W. Naturally occurring enzyme activity variation in Drosophila melanogaster. II. Relationships among enzymes. Genetics. 1982 Oct;102(2):207–221. doi: 10.1093/genetics/102.2.207. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES