Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-18T05:33:28.053Z Has data issue: false hasContentIssue false

The fitness consequences of P element insertion in Drosophila melanogaster

Published online by Cambridge University Press:  14 April 2009

Walter F. Eanes*
Affiliation:
Department of Ecology and Evolution, State University of New York, Stony Brook, New York 11794, U.S.A.
Cedric Wesley
Affiliation:
Department of Ecology and Evolution, State University of New York, Stony Brook, New York 11794, U.S.A.
Jody Hey
Affiliation:
Department of Ecology and Evolution, State University of New York, Stony Brook, New York 11794, U.S.A.
David Houle
Affiliation:
Department of Ecology and Evolution, State University of New York, Stony Brook, New York 11794, U.S.A.
James W. Ajioka
Affiliation:
Department of Ecology and Evolution, State University of New York, Stony Brook, New York 11794, U.S.A.
*
* Corresponding author.
Rights & Permissions [Opens in a new window]

Summary

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

In this study we estimate the frequency at which P-element insertion events, as identified by in situ hybridization, generate lethal and mild viability mutations. The frequency of lethal mutations generated per insertion event was 0·004. Viability dropped an average of 1% per insertion event. Our results indicate that it is deletions and rearrangements resulting from the mobilization of P elements already in place and not the insertions per se that cause the drastic effects on viability and fitness observed in most studies of P–M dysgenesis-derived mutations. Elements of five other families (I, copia, 412, B104, and gypsy) were not mobilized in these crosses. Finally, we contrast the density of P elements on the X chromosome with the density on the four autosomal arms in a collection of thirty genomes from an African population. The relative number of P elements on the X chromosome is too high to be explained by either a hemizygous selection or a neutrality model. The possible reasons for the failure to detect selection are discussed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1988

References

Bender, W., Akam, M., Karch, F., Beachy, P. A., Peifer, M., Spierer, P., Lewis, E. B. & Hogness, D. S. (1983). Molecular genetics of the bithorax complex in Drosophila melanogaster. Science 221, 2329.CrossRefGoogle ScholarPubMed
Berg, R. L., Engels, W. R. & Kreber, R. A. (1980). Site-specific X chromosomal rearrangements from hybrid dysgenesis in Drosophila melanogaster. Science 210, 427–29.CrossRefGoogle ScholarPubMed
Bingham, P. M., Kidwell, M. G. & Rubin, G. M. (1982). The molecular basis of P–M hybrid dysgenesis: the role of the P element, a.P-strain-specific transposon family. Cell 29, 9951004.CrossRefGoogle Scholar
Blackman, R. K., Grimaila, R., Koehler, M. M. D. & Gelbart, W. M. (1987). Mobilization of hobo elements residing within the decapentaplegic gene complex: suggestion of a new hybrid dysgenesis system in Drosophila melanogaster. Cell 49, 497505.CrossRefGoogle ScholarPubMed
Bowman, J. T. Jr (1965). Spontaneous reversion of the white-ivory mutant of Drosophila melanogaster. Genetics 52, 10691079.CrossRefGoogle ScholarPubMed
Bucheton, A., Paro, R., Sang, H. M., Pelisson, A. & Finnigan, D. A. (1983). The molecular basis of I-R dysgenesis in Drosophila melanogaster, identification, cloning, a.d properties of the I factor. Cell 38, 153163.CrossRefGoogle Scholar
Campuzano, S., Carramolino, L., Cabrera, C. V., Ruiz-Gomez, M., Villares, R., Boronat, A. & Modolell, J. (1985). Molecular genetics of the achaete-scute gene complex of D. melanogaster. Cell 40, 327338.CrossRefGoogle ScholarPubMed
Charlesworth, B. (1985). The population genetics of transposable elements. In Population Genetics and Molecular Evolution (ed. Ohta, T. and Aoki, K.-I.). Berlin: Springer-Verlag.Google Scholar
Charlesworth, B. & Charlesworth, D. (1983). The population dynamics of transposable elements. Genetical Research 42, 127.CrossRefGoogle Scholar
Charlesworth, B. & Langley, C. H. (1986). The evolution of self-regulated transposition of transposable elements. Genetics 112, 359383.CrossRefGoogle ScholarPubMed
Choo, J. K. & Lee, T. J. (1986). Genetic changes in a Korean population of Drosophila melanogaster. Japanese Journal of Genetics 61, 337343.Google Scholar
Coté, B., Bender, W., Curtis, D. & Chovnick, A. (1986). Molecular mapping of the rosy locus in Drosophila melanogaster. Genetics 112, 769783.CrossRefGoogle ScholarPubMed
Demerec, M. (1937). Frequency of spontaneous mutation in certain stocks of Drosophila melanogaster. Genetics 22, 469–78.CrossRefGoogle ScholarPubMed
Eanes, W. F., Hey, J. & Houle, D. (1985). Homozygous and hemizygous viability variation on the X chromosome of Drosophila melanogaster. Genetics 111, 831844.CrossRefGoogle ScholarPubMed
Engels, W. R. (1979). Hybrid dysgenesis in Drosophila melanogaster: rules of inheritance of female sterility. Genetical Research 33, 219236.CrossRefGoogle Scholar
Engels, W. R. (1983). The P family of transposable elements in Drosophila. Annual Review of Genetics 17, 315344.CrossRefGoogle Scholar
Engels, W. R. & Preston, C. R. (1984). Formation of chromosomal rearrangements by P factors in Drosophila. Genetics 107, 657678.CrossRefGoogle ScholarPubMed
Falconer, D. S. (1981). Introduction to Quantitative Genetics. London: Longman Group.Google Scholar
Fitzpatrick, G. J. & Sved, J. A. (1986). High levels of fitness modifiers induced by hybrid dysgenesis in Drosophila melanogaster. Genetical Research 48, 8994.CrossRefGoogle Scholar
Gerasimova, T. I., Mizrokhi, L. J. & Georgiev, G. P. (1984). Transposition bursts in genetically unstable Drosophila melanogaster. Nature 309, 714716.CrossRefGoogle Scholar
Green, M. M. (1967). The genetics of a mutable gene at the white locus of Drosophila melanogaster. Genetics 56, 467482.CrossRefGoogle ScholarPubMed
Gromko, M. H., Gilbert, D. G. & Richmond, R. C. (1984). Sperm transfer and use in the multiple mating system of Drosophila. In Sperm Competition and the Evolution of Mating Systems (ed. Smith, R. L.). New York: Academic Press.Google Scholar
Hiraizumi, Y. (1979). A model of the negative correlation between male recombination and transmission frequency in Drosophila melanogaster. Genetics 93, 449459.CrossRefGoogle Scholar
Kidd, S., Lockett, T. J. & Young, M. W. (1983). The Notch locus of Drosophila melanogaster. Cell 34, 421433.CrossRefGoogle ScholarPubMed
Kidwell, M. G., Kidwell, J. F. & Nei, M. (1973). A case of high rate of spontaneous mutation affecting viability in Drosophila melanogaster. Genetics 75, 133153.CrossRefGoogle ScholarPubMed
Langer, P. R., Waldrop, A. A. & Ward, D. C. (1981). Enzymatic synthesis of biotin-labeled polynucleotides. Proceedings of the National Academy of Sciences, USA 78, 66336637.CrossRefGoogle ScholarPubMed
Lefevre, G. & Watkins, W. (1986). The question of total gene number in Drosophila melanogaster. Genetics 113, 869895.CrossRefGoogle ScholarPubMed
Lewin, B. (1980). Gene Expression, vol. 2. New York: John Wiley & Sons.Google Scholar
Lindsley, D. L., Sandier, L., Baker, B. S., Carpenter, A. T. C., Denell, R. E., Hall, J. C., Jacobs, P. A., Miklos, L. G., Davis, B. K., Gethmana, R. C., Hardy, R. W., Hessler, A., Miller, S. M., Nozawa, H., Parry, D. M. & Gould-Somero, M. (1972). Segmental aneuploidy and the gross genetic structure of the Drosophila genome. Genetics 71, 157184.CrossRefGoogle ScholarPubMed
McClintock, B. (1956 a). Intranuclear systems controlling gene action and mutation. Brookhaven Symposia in Biology 8, 5874.Google Scholar
McClintock, B. (1956 b). Controlling elements and the gene. Cold Spring Harbor Symposia on Quantitative Biology 21, 197216.CrossRefGoogle ScholarPubMed
Mackay, T. F. (1986). Transposable element-induced fitness mutations in Drosophila melanogaster. Genetical Research 48, 7787.CrossRefGoogle Scholar
Montgomery, E. A., Charlesworth, B. & Langley, C. H. (1987). A test for the role of natural selection in the stabilization of transposable element copy number in a population of Drosophila melanogaster. Genetical Research 49, 3141.CrossRefGoogle Scholar
Mukai, T. (1964). The genetic structure of natural populations of Drosophila melanogaster. I. Spontaneous mutation rate of polygenes controlling viability. Genetics 50, 119.CrossRefGoogle ScholarPubMed
Mukai, T. (1969). The genetic structure of natural populations of Drosophila melanogaster. VII. Synergistic interaction of spontaneous mutant polygenes controlling viability. Genetics 61, 749761.CrossRefGoogle ScholarPubMed
Mukai, T., Baba, M., Akiyama, M., Uowaki, N., Kusakaba, S. & Tajima, F. (1985). Rapid change in mutation rate in a local population of Drosophila melanogaster. Proceedings of the National Academy of Sciences, U.S.A. 82, 76717675.CrossRefGoogle Scholar
Mukai, T., Chigusa, S. I., Mettler, L. E. & Crow, J. F. (1972). Mutation rate and dominance of genes affecting viability in Drosophila melanogaster. Genetics 72, 335355.CrossRefGoogle ScholarPubMed
Mukai, T. & Yukuhiro, K. (1983). An extremely high rate of deleterious viability mutations in Drosophila possibly caused by transposons in non-coding regions. Japanese Journal of Genetics 59, 316319.Google Scholar
Neel, J. V. (1942). A study of a case of high mutation rate in Drosophila melanogaster. Genetics 27, 519536.CrossRefGoogle ScholarPubMed
O'Hare, K. & Rubin, M. (1983). Structures of P transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome. Cell 24, 2535.CrossRefGoogle Scholar
Pardue, M. L. & Gall, J. G. (1975). Nucleic acid hybridization to the DNA of cytological preparations. Methods in Cell Biology 10, 117.CrossRefGoogle Scholar
Provine, W. B. (1971). The Origins of Theoretical Population Genetics. Chicago: University of Chicago Press.Google Scholar
Scott, M. P., Weiner, A. J., Hazelrigg, T. I., Polisky, B. A., Pirrotta, V., Scalenghe, F. & Kaufman, T. C. (1983). The molecular organization of the Antennapedia locus in Drosophila. Cell 35, 763776.CrossRefGoogle Scholar
Shapiro, J. A. (1983). Mobile Genetic Elements. Orlando: Academic Press.Google Scholar
Simmons, M. J. & Crow, J. F. (1977). Mutations affecting fitness in Drosophila populations. Annual Review of Genetics 11, 4978.CrossRefGoogle ScholarPubMed
Simmons, M. J. & Lim, J. K. (1980). Site specificity of mutations arising in dysgenic hybrids of Drosophila melanogaster. Proceedings of the National Academy of Sciences, U.S.A. 77, 60426046.CrossRefGoogle ScholarPubMed
Simmons, M. J., Raymond, J. D., Culbert, P. & Laverty, T. R. (1984 a). Analysis of dysgenesis induced lethal mutations on the X chromosome of a Q strain of Drosophila melanogaster. Genetics 107, 4963.CrossRefGoogle Scholar
Simmons, M. J., Raymond, J. D., Johnson, N. A. & Fahey, T. M. (1984 b). A comparison of mutation rates for specific loci and chromosome regions in dysgenic hybrid males of Drosophila melanogaster. Genetics 106, 8594.CrossRefGoogle ScholarPubMed
Simmons, M. J., Raymond, J. D., Laverty, T. R., Doll, R. F., Raymond, N. C., Kocur, G. J. & Drier, E. A. (1985). Chromosomal effects of mutability in the P-M system of hybrid dysgenesis in Drosophila melanogaster. Genetics 111, 869884.CrossRefGoogle Scholar
Strobel, E., Dunsmuir, P. & Rubin, G. M. (1979). Polymorphism in the chromosomal locations of elements of the 412, copia, and 297 dispersed repeated gene families in Drosophila. Cell 17, 429439.CrossRefGoogle ScholarPubMed
Sved, J. A. (1971). An estimate of heterosis in Drosophila melanogaster. Genetical Research. 18, 97105.CrossRefGoogle ScholarPubMed
Yannopoulos, G., Stamatis, N., Monastirioti, M., Hatzo-poulos, P., & Louis, C. (1987). Hobo is responsible for the induction of hybrid dysgenesis by strains of Drosophila melanogaster bearing the male recombination factor 23.5MRF. Cell 49, 487495.CrossRefGoogle ScholarPubMed
Yukuhiro, K., Harada, K. & Mukai, T. (1985). Viability mutations induced by P elements in Drosophila melanogaster. Japanese Journal of Genetics 60, 531537.Google Scholar
Yukuhiro, K. & Mukai, T. (1986). Increased detrimental load possibly caused by a transposon in a local population of Drosophila melanogaster. Japanese Journal of Genetics 61, 2543.Google Scholar
Young, M. W. (1979). Middle repetitive DNA: a fluid component of the Drosophila genome. Proceedings of the Natioinal Academy of Sciences, USA 76, 62746278.CrossRefGoogle ScholarPubMed
Zachar, Z. & Bingham, P. M. (1982). Regulation of white locus expression: the structure of mutant alleles at the white locus of Drosophila melanogaster. Cell 30, 529541.CrossRefGoogle ScholarPubMed