Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-30T23:22:30.613Z Has data issue: false hasContentIssue false

Accumulation of P elements in minority inversions in natural populations of 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, N.Y. 11794
Cedric Wesley
Affiliation:
Department of Ecology and Evolution, State University of New York, Stony Brook, N.Y. 11794
Brian Charlesworth
Affiliation:
Department of Ecology and Evolution, 1101 East 57th Street, University of Chicago, Chicago, IL 60637
*
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.

The accumulation of a transposable element inside chromosomal inversions is examined theoretically by a mathematical model, and empirically by counts of P elements associated with inversion polymorphisms in natural populations of Drosophila melanogaster. The model demonstrates that, if heterozygosity for an inversion effectively reduces element associated production of detrimental chromosome rearrangements, a differential accumulation of elements is expected, with increased copy number inside the minority inversion. Several-fold differential accumulations are possible with certain parameter values. We present data on P element counts for inversion polymorphisms on all five chromosome arms of 157 haploid genomes from two African populations. Our observations show significantly increased numbers of elements within the regions associated with the least common, or minority arrangements, in natural inversion polymorphisms.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1992

References

Ajioka, J. W. & Eanes, W. F. (1989). The accumulation of P elements at the tip of the X chromosome in populations of Drosophila melanogaster. Genetical Research 53, 16.CrossRefGoogle ScholarPubMed
Ashburner, M. (1989). Drosophila. A Laboratory Handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor N.Y.Google Scholar
Ashburner, M. & Lemeunier, F. (1976). Relationships within the melanogaster species subgroup of the genus Drosophila. I. Inversion polymorphism in Drosophila melanogaster and Drosophila simulans. Proceedings of the Royal Society B 193, 137157.Google ScholarPubMed
Beech, R. N. & Leigh-Brown, A. J. (1989). Insertion-deletion variation in the yellow-achaete-scute region in two natural populations of Drosophila melanogaster. Genetical Research 53, 715.CrossRefGoogle ScholarPubMed
Berg, R. L.Engels, W. R. & Kreber, R. A. (1980). Site-specific X-chromosome rearrangements from hybrid dysgenesis in Drosophila melanogaster. Science 210, 427429.CrossRefGoogle ScholarPubMed
Charlesworth, B. & Langley, C. H. (1989). The population genetics of Drosophila transposable elements. Annual Review of Genetics 23, 251287.Google Scholar
Charlesworth, B. & Lapid, A. (1989). A study of ten transposable elements on X chromosomes from a population of Drosophila melanogaster. Genetical Research 54, 113125.Google Scholar
Davis, P. S.Sheen, M. W. & Judd, B. H. (1987). Asymmetric pairings of transposons in a proximal to the white locus of Drosophila account for four classes of regularly exchanged products. Proceedings of the National Academy of Sciences, USA 84, 174178.CrossRefGoogle Scholar
Eanes, W. F.Labate, J. & Ajioka, J. W. (1989). Restriction-map variation with the yellow-achaete-scute region in five populations of Drosophila melanogasler. Molecular Biology and Evolution 6, 492502.Google Scholar
Eanes, W. F.Wesley, C.Hey, J.Houle, D. & Ajioka, J. W. (1988). The fitness consequences of P element insertion in Drosophila melanogaster. Genetical Research 52, 1726.CrossRefGoogle Scholar
Engels, W. R. (1989). P elements in Drosophila. In Mobile DNA (ed Berg, D. and Howe, M.) pp. 437484. American Society of Microbiology Publications, Washington DC.Google Scholar
Engels, W. R.Johnson-Sclitz, D. M.Eggelston, W. R. & Sved, J. A. (1990). High-frequency P element loss in Drosophila is homolog dependent. Cell 62, 515525.CrossRefGoogle ScholarPubMed
Engels, W. R. & Preston, C. R. (1981). Identifying P factors in Drosophila by means of chromosome breakage hotspots. Cell 26, 421428.CrossRefGoogle ScholarPubMed
Finnegan, D. J. & Fawcett, D. H. (1986). Oxford Surveys on Eukaryotic Genes 3, 162.Google Scholar
Goldberg, M. L.Sheen, J.-Y.Gehring, W. J. & Green, M. M. (1983). Unequal crossing-over associated with asymmetric synapsis between nomadic elements of the Drosophila genome. Proceedings of the National Academy of Sciences, USA 80, 50175021.CrossRefGoogle Scholar
Inoue, Y. & Watanabe, T. K. (1979). Inversion polymorphisms in Japanese natural populations of Drosophila melanogaster. Japanese Journal of Genetics 54, 6982.Google Scholar
Jackson, J. A. & Fink, G. R. (1985). Meiotic recombination between duplicated genetic elements in Saccharomyces cerevisiae. Genetics 109, 303322.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
Langley, C. H.Montgomery, E.Hudson, R.Kaplan, N. & Charlesworth, B. (1988). On the role of unequal exchange in the containment of transposable element copy number. Genetical Research 52, 223235.Google Scholar
Lim, J. K.Simmons, M. J.Raymond, J. D.Cox, N. M.Doll, R. F. & Culbert, T. P. (1983). Homologue destabilization by a putative transposable element in Drosophila melanogaster. Proceedings of the National Academy of Sciences, USA 80, 66246627.CrossRefGoogle ScholarPubMed
Montgomery, E.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.Google Scholar
O'Hare, K. & Rubin, G. M. (1983). Structures of P transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome. Cell 34, 2535.CrossRefGoogle ScholarPubMed
Pardue, M. L. & Gall, J. G. (1975). Nucleic acid hybridization to the DNA of cytological preparations. Methods in Cell Biology 10, 117.CrossRefGoogle Scholar
Petes, T. D. & Hill, C. W. (1988). Recombination between repeated genes in microorganism. Annual Review of Genetics 22, 147168.Google Scholar
Roberts, P. A. (1976). The genetics of chromosomal aberration. In The Genetics and Biology of Drosophila, Vol. 1 a (ed. Ashburner, M. and Novitski, E.), pp. 68184. Academic Press.Google Scholar
Sokal, R. R. & Rohlf, F. J. (1981). Biometry, pp. 429445. Freeman & Co.Google Scholar
Steele, D. F.Morris, M. E. & Jinks-Robertson, S. (1991). Allelic and ectopic interactions in recombination-defective yeast strains. Genetics 127, 4360.CrossRefGoogle ScholarPubMed
Sturtevant, A. H. (1971). Genetic factors affecting the strength of linkage in Drosophila. Proceedings of the National Academy of Sciences, USA 3, 555558.Google Scholar
White, M. J. D. (1973). Animal Cytology and Evolution. Cambridge University Press.Google Scholar