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The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. I. Element frequencies and distribution

Published online by Cambridge University Press:  14 April 2009

Brian Charlesworth*
Affiliation:
Department of Ecology and Evolution, The University of Chicago, 1101 E. 57th St, Chicago IL 60637-1573, USA
Angela Lapid
Affiliation:
Department of Ecology and Evolution, The University of Chicago, 1101 E. 57th St, Chicago IL 60637-1573, USA
Darlene Canada
Affiliation:
Department of Ecology and Evolution, The University of Chicago, 1101 E. 57th St, Chicago IL 60637-1573, USA
*
*Corresponding author.
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Data were collected on the distribution of nine families of transposable elements among second and third chromosomes isolated from a natural population of Drosophila melanogaster, by means of in situ hybridization of element probes to polytene chromosomes. It was found that the copy numbers per chromosome in the distal sections of the chromosome arms followed a Poisson distribution. Elements appeared to be distributed randomly along the distal sections of the chromosome arms. There was no evidence for linkage disequilibrium in the distal sections of the chromosomes, but some significant disequilibrium was detected in proximal regions. There were many significant correlations between different element families with respect to the identity of the sites that were occupied in the sample. There were also significant correlations between families with respect to sites at which elements achieved relatively high frequencies. Element frequencies per chromosome band were generally low in the distal sections, but were higher proximally. These results are discussed in the light of models of the population dynamics of transposable elements. It is concluded that they provide strong evidence for the operation of a force or forces opposing transpositional increase in copy number. The data suggest that the rate of transposition perelement per generation is of the order of 10−4, for the elements included in this study.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1992

References

Ashburner, M. (1989). Drosophila. A Laboratory Handbook. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory.Google Scholar
Begun, D. J. & Aquadro, C. F. (1992). Levels of naturally occurring DNA polymorphism correlate with recombination rate in D. melanogaster. Nature 356, 519520.Google Scholar
Brookfield, J. F. Y.Montgomery, E. A. & Langley, C. H. (1984). Apparent absence of transposable elements related to the P element of Drosophila melanogaster in other species of Drosophila. Nature 310, 330332.CrossRefGoogle Scholar
Bulmer, M. G. (1980). The Mathematical Theory of Quantitative Genetics. Oxford: Oxford University Press.Google Scholar
Charlesworth, B. (1990). Mutation-selection balance and the evolutionary advantage of sex and recombination. Genetical Research 55, 199221.CrossRefGoogle ScholarPubMed
Chariesworth, B. (1991). Transposable elements in natural populations with a mixture of insertion sites. Genetical Research 57, 127134.CrossRefGoogle Scholar
Charlesworth, B. & Charlesworth, D. (1983). The population dynamics of transposable elements. Genetical Research 42, 127.Google Scholar
Charlesworth, B. & Charlesworth, D. (1985). Genetic variation in recombination in Drosophila. I. Responses to selection and preliminary genetic analysis. Heredity 54, 7184.Google Scholar
Charlesworth, B. & Langley, C. H. (1989). The population genetics of Drosophila transposable elements. Annual Review of Genetics 23, 251287.CrossRefGoogle ScholarPubMed
Charlesworth, B. & Lapid, A. (1989). A study often families of transposable elements on X chromosomes from a population of Drosophila melanogaster. Genetical Research 54, 113125.CrossRefGoogle ScholarPubMed
Charlesworth, B.Lapid, A. & Canada, D. (1992). The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. II. Inferences on the nature of selection against elements. Genetical Research 60, 115130.Google Scholar
Finnegan, D. J. (1989). F and related elements in Drosophila melanogaster. In Mobile DNA (ed. Berg, D. E. and Howe, M. M.), pp. 519521. Washington D.C.: American Society of Microbiology.Google Scholar
Fisher, R. A. (1958). Statistical Methods for Research Workers, 13th edn.Edinburgh: Oliver and Boyd.Google Scholar
Hey, J. (1989). The transposable portion of the genome of Drosophila algonquin is very different from that of D. melanogaster. Molecular Biology and Evolution 6, 666679.Google Scholar
Kaplan, N. L. & Brookfield, J. F. Y. (1983). Transposable elements in Mendelian populations. III. Statistical results. Genetics 104, 485495.Google Scholar
Kaplan, N. L.Hudson, R. R. & Langley, C. H. (1989). The ‘hitchhiking effect’ revisited. Genetics 123, 887889.CrossRefGoogle ScholarPubMed
Kendall, M. G.Stuart, J. D. & Ord, J. K. (1983). The Advanced Theory of Statistics, vol. 3, 4th edn.London: Charles Griffin.Google Scholar
Langley, C. H.Montgomery, E. A.Hudson, R. R.Kaplan, N. L. & Charlesworth, B. (1988). On the role of unequal exchange in the containment of transposable element copy number. Genetical Research 49, 3141.Google Scholar
Lefevre, G. (1976). A photographic representation of the polytene chromosomes of Drosophila melanogaster salivary glands. In The Genetics and Biology of Drosophila, vol. 1a (ed. Ashburner, M. and Novitski, E.), pp. 3136. London: Academic Press.Google Scholar
Lewontin, R. C. & Prout, T. (1956). Estimation of the number of different classes in a population. Biometrics 12, 211223.Google Scholar
Lindsley, D. L. & Zimm, G. (1992). The Genome of Drosophila melanogaster. San Diego: Academic Press.Google Scholar
McDonald, J. F. (1990). Macroevolution, gene regulation and retro-viral like elements. Bioscience 40, 183191.Google Scholar
Maynard, Smith J. & Haigh, J. (1974). The hitch-hiking effect of a favourable gene. Genetical Research 23, 2335.Google 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.Google Scholar
Mukai, T. & Yamaguchi, O. (1974). The genetic structure of natural populations of Drosophila. XI. Genetic variability in a natural population. Genetics 82, 6382.Google Scholar
Robertson, A. & Hill, W. G. (1983). Population and quantitative genetics of many linked loci in finite populations. Proceedings of the Royal Society of London B 219, 253264.Google Scholar
Rubin, G. M.Brorein, W. J.Dunsmuir, P.Flavell, A. J.Strobel, E.Toole, J. J. & Young, E. (1981). ‘Copia-like’ transposable elements in the Drosophila genome. Cold Spring Harbor Symposium on Quantitative Biology 45, 619628.Google Scholar
Singh, R. S. & Rhomberg, L. R. (1987). A comprehensive study of genie variation in natural populations of Drosophila melanogaster. I. Estimates of gene flow from rare alleles. Genetics 115, 313322.Google Scholar
Snedecor, G. W. & Cochran, W. G. (1980). Statistical Methods, 7th edn.Ames, Iowa: Iowa State University Press.Google Scholar
Stephan, W.Wiehe, T. H. E. & Lenz, M. W. (1992). The effect of strongly selected substitutions on neutral polymorphism: analytical results based on diffusion theory. Theoretical Population Biology 41, 237254.Google Scholar
Strobel, E. (1982). Mobile dispersed repeated DNA elements in the Drosophila genome. Federation Proceedings 41, 26562658.Google Scholar
Thomson, G. (1977). The effect of a selected locus on linked neutral loci. Genetics 85, 789814.Google Scholar