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. 1999 Mar;151(3):1081–1091. doi: 10.1093/genetics/151.3.1081

Potential variance affecting homeotic Ultrabithorax and Antennapedia phenotypes in Drosophila melanogaster.

G Gibson 1, M Wemple 1, S van Helden 1
PMCID: PMC1460536  PMID: 10049924

Abstract

Introgression of homeotic mutations into wild-type genetic backgrounds results in a wide variety of phenotypes and implies that major effect modifiers of extreme phenotypes are not uncommon in natural populations of Drosophila. A composite interval mapping procedure was used to demonstrate that one major effect locus accounts for three-quarters of the variance for haltere to wing margin transformation in Ultrabithorax flies, yet has no obvious effect on wild-type development. Several other genetic backgrounds result in enlargement of the haltere significantly beyond the normal range of haploinsufficient phenotypes, suggesting genetic variation in cofactors that mediate homeotic protein function. Introgression of Antennapedia produces lines with heritable phenotypes ranging from almost complete suppression to perfect antennal leg formation, as well as transformations that are restricted to either the distal or proximal portion of the appendage. It is argued that the existence of "potential" variance, which is genetic variation whose effects are not observable in wild-type individuals, is a prerequisite for the uncoupling of genetic from phenotypic divergence.

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Selected References

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  1. 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]
  2. Boube M., Benassayag C., Seroude L., Cribbs D. L. Ras1-mediated modulation of Drosophila homeotic function in cell and segment identity. Genetics. 1997 Jun;146(2):619–628. doi: 10.1093/genetics/146.2.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Clark A. G., Wang L., Hulleberg T. Spontaneous mutation rate of modifiers of metabolism in Drosophila. Genetics. 1995 Feb;139(2):767–779. doi: 10.1093/genetics/139.2.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Frischer L. E., Hagen F. S., Garber R. L. An inversion that disrupts the Antennapedia gene causes abnormal structure and localization of RNAs. Cell. 1986 Dec 26;47(6):1017–1023. doi: 10.1016/0092-8674(86)90816-0. [DOI] [PubMed] [Google Scholar]
  5. Gellon G., Harding K. W., McGinnis N., Martin M. M., McGinnis W. A genetic screen for modifiers of Deformed homeotic function identifies novel genes required for head development. Development. 1997 Sep;124(17):3321–3331. doi: 10.1242/dev.124.17.3321. [DOI] [PubMed] [Google Scholar]
  6. Gibson G., Hogness D. S. Effect of polymorphism in the Drosophila regulatory gene Ultrabithorax on homeotic stability. Science. 1996 Jan 12;271(5246):200–203. doi: 10.1126/science.271.5246.200. [DOI] [PubMed] [Google Scholar]
  7. Gibson G., van Helden S. Is function of the Drosophila homeotic gene Ultrabithorax canalized? Genetics. 1997 Nov;147(3):1155–1168. doi: 10.1093/genetics/147.3.1155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Goldstein D. B., Clark A. G. Microsatellite variation in North American populations of Drosophila melanogaster. Nucleic Acids Res. 1995 Oct 11;23(19):3882–3886. doi: 10.1093/nar/23.19.3882. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hartl D. L., Dykhuizen D. E. Potential for selection among nearly neutral allozymes of 6-phosphogluconate dehydrogenase in Escherichia coli. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6344–6348. doi: 10.1073/pnas.78.10.6344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kennison J. A., Tamkun J. W. Dosage-dependent modifiers of polycomb and antennapedia mutations in Drosophila. Proc Natl Acad Sci U S A. 1988 Nov;85(21):8136–8140. doi: 10.1073/pnas.85.21.8136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kerridge S., Morata G. Developmental effects of some newly induced Ultrabithorax alleles of Drosophila. J Embryol Exp Morphol. 1982 Apr;68:211–234. [PubMed] [Google Scholar]
  12. Lai C., Lyman R. F., Long A. D., Langley C. H., Mackay T. F. Naturally occurring variation in bristle number and DNA polymorphisms at the scabrous locus of Drosophila melanogaster. Science. 1994 Dec 9;266(5191):1697–1702. doi: 10.1126/science.7992053. [DOI] [PubMed] [Google Scholar]
  13. Lander E. S., Botstein D. Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics. 1989 Jan;121(1):185–199. doi: 10.1093/genetics/121.1.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Larsen E., Lee T., Glickman N. Antenna to leg transformation: dynamics of developmental competence. Dev Genet. 1996;19(4):333–339. doi: 10.1002/(SICI)1520-6408(1996)19:4<333::AID-DVG6>3.0.CO;2-A. [DOI] [PubMed] [Google Scholar]
  15. Lewis E. B. A gene complex controlling segmentation in Drosophila. Nature. 1978 Dec 7;276(5688):565–570. doi: 10.1038/276565a0. [DOI] [PubMed] [Google Scholar]
  16. Long A. D., Mullaney S. L., Reid L. A., Fry J. D., Langley C. H., Mackay T. F. High resolution mapping of genetic factors affecting abdominal bristle number in Drosophila melanogaster. Genetics. 1995 Mar;139(3):1273–1291. doi: 10.1093/genetics/139.3.1273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ludwig M. Z., Kreitman M. Evolutionary dynamics of the enhancer region of even-skipped in Drosophila. Mol Biol Evol. 1995 Nov;12(6):1002–1011. doi: 10.1093/oxfordjournals.molbev.a040277. [DOI] [PubMed] [Google Scholar]
  18. Marín I., Baker B. S. The evolutionary dynamics of sex determination. Science. 1998 Sep 25;281(5385):1990–1994. doi: 10.1126/science.281.5385.1990. [DOI] [PubMed] [Google Scholar]
  19. Orr H. A. The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics. 1995 Apr;139(4):1805–1813. doi: 10.1093/genetics/139.4.1805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Purugganan M. D., Suddith J. I. Molecular population genetics of the Arabidopsis CAULIFLOWER regulatory gene: nonneutral evolution and naturally occurring variation in floral homeotic function. Proc Natl Acad Sci U S A. 1998 Jul 7;95(14):8130–8134. doi: 10.1073/pnas.95.14.8130. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Saiki R. K., Bugawan T. L., Horn G. T., Mullis K. B., Erlich H. A. Analysis of enzymatically amplified beta-globin and HLA-DQ alpha DNA with allele-specific oligonucleotide probes. Nature. 1986 Nov 13;324(6093):163–166. doi: 10.1038/324163a0. [DOI] [PubMed] [Google Scholar]
  22. Schlötterer C., Vogl C., Tautz D. Polymorphism and locus-specific effects on polymorphism at microsatellite loci in natural Drosophila melanogaster populations. Genetics. 1997 May;146(1):309–320. doi: 10.1093/genetics/146.1.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Struhl G. Genes controlling segmental specification in the Drosophila thorax. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7380–7384. doi: 10.1073/pnas.79.23.7380. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Weatherbee S. D., Halder G., Kim J., Hudson A., Carroll S. Ultrabithorax regulates genes at several levels of the wing-patterning hierarchy to shape the development of the Drosophila haltere. Genes Dev. 1998 May 15;12(10):1474–1482. doi: 10.1101/gad.12.10.1474. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Zeng Z. B. Precision mapping of quantitative trait loci. Genetics. 1994 Apr;136(4):1457–1468. doi: 10.1093/genetics/136.4.1457. [DOI] [PMC free article] [PubMed] [Google Scholar]

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