Hostname: page-component-5c6d5d7d68-tdptf Total loading time: 0 Render date: 2024-08-30T06:00:35.993Z Has data issue: false hasContentIssue false
  • English
  • Français

A study of ten families of transposable elements on X chromosomes from a population of Drosophila melanogaster

Published online by Cambridge University Press:  14 April 2009

Brian Charlesworth  and
Angela Lapid
Brian Charlesworth*
Affiliation:
Department of Ecology and Evolution, The University of Chicago, 1103 E. 57th St, Chicago, IL 60637, USA
Angela Lapid
Affiliation:
Department of Ecology and Evolution, The University of Chicago, 1103 E. 57th St, Chicago, IL 60637, USA
*
* Corresponding author.

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.

Data were collected on the distribution of ten families of transposable elements among fourteen X chromosomes isolated from a natural population of Drosophila melanogaster, by means of in situ hybridization to polytene chromosomes. It was found that, with the exception of roo, the copy number per chromosome followed a Poisson distribution. There was no evidence for linkage disequilibrium, either within or between families. Some pairs of families of elements were correlated with respect to the identity of the sites that were occupied in the sample, although there was no evidence for a correlation with respect to the sites at which elements attained relatively high frequencies. Elements appeared to be distributed randomly along the distal part of the X chromosome. There was, however, a strong tendency for elements to accumulate at the base of the chromosome. Element frequencies per chromosome band were generally low, except at the base of the chromosome where bands in subdivisions 19E and 20A sometimes had high frequencies of occupation. 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 accumulation of elements at the base of the chromosome is consistent with the idea that unequal exchange between elements at non-homologous sites is such a force, although other possibilities cannot be excluded at present. The data suggest that the rate of transposition per element per generation is of the order of 10−4, for the elements included in this study.

Type
Research Article
Information
Genetics Research , Volume 54 , Issue 2 , October 1989 , pp. 113 - 125
Copyright
Copyright © Cambridge University Press 1989

References

Aquadro, C. R., Deese, S. F., Bland, M. M., Langley, C. H. & Laurie-Ahlberg, C. C. (1986). Molecular population genetics of the alcohol dehydrogenase gene region of Drosophila melanogaster. Genetics 114, 1165–1190.CrossRefGoogle ScholarPubMed
Aquadro, C. R., Lado, K. M. & Noon, W. A. (1988). The rosy region of Drosophila melanogaster and Drosophila simulans. I. Contrasting levels of naturally occurring DNA sequence variation and divergence. Genetics 119, 875–888.CrossRefGoogle ScholarPubMed
Becker, H. J. (1976). Mitotic recombination. In The Genetics and Biology of Drosophila, vol. 1 c (ed. Ashburner, M. and Novitski, E.), pp. 1020–1087. Orlando: Academic Press.Google Scholar
Brookfield, J. F. Y (1986). Population biology of transposable elements. Philosophical Transactions of the Royal Society of London, B312, 217–226.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, 330–332.CrossRefGoogle Scholar
Charlesworth, B. (1985). The population genetics of transposable elements. In Population Genetics and Molecular Evolution (ed. Ohta, T. and Aoki, K.), pp. 213–232. Berlin: Springer Verlag.Google Scholar
Charlesworth, B. (1988). The maintenance of transposable elements in natural populations. In Proceedings of the International Symposium on Plant Transposable Elements (ed. Nelson, O. J.), pp. 189–212. New York: Plenum.CrossRefGoogle Scholar
Charlesworth, B. & Charlesworth, D. (1983). The population dynamics of transposable elements. Genetical Research 42, 1–27.Google Scholar
Charlesworth, B. & Charlesworth, D. (1985). Genetic variation in recombination in Drosophila. I. Responses to selection and preliminary genetic analysis. Heredity 54, 71–84.CrossRefGoogle Scholar
Charlesworth, B. & Langley, C. H. (1986). The evolution of self-regulated transposition of transposable elements. Genetics 112, 359–383.CrossRefGoogle ScholarPubMed
Cross, S. R. H. & Birley, A. J. (1986). Restriction endo-nuclease map variation in the Adh region in populations of Drosophila melanogaster. Biochemical Genetics 24, 415–433.CrossRefGoogle Scholar
Davis, P. S., Shen, M. W. & Judd, B. H. (1987). Asymmetrical pairing of transposons in and proximal to the white locus of Drosophila accounts for four classes of regularly occurring exchange products. Proceedings of the National Academy of Sciences USA 84, 174–178.CrossRefGoogle Scholar
Doolittle, W. F. & Sapienza, C. (1980). Selfish genes, the phenotype paradigm, and genome evolution. Nature 284, 601–607.CrossRefGoogle ScholarPubMed
Eggleston, W. B., Johnson-Schlitz, D. & Engels, W. R. (1988). P-M hybrid dysgenesis does not mobilize other transposable elements in D. melanogaster. Nature 331, 368–370.CrossRefGoogle Scholar
Engels, W. R. (1986). On the evolution and population genetics of hybrid-dysgenesis causing transposable elements in Drosophila. Philosophical Transactions of the Royal Society of London, B312, 205–215.Google Scholar
Finnegan, D. J. & Fawcett, D. H. (1986). Transposable elements in Drosophila melanogaster. Oxford Surveys on Eukaryote Genes 3, 1–62.Google ScholarPubMed
Fisher, R. A. (1958). Statistical Methods for Research Workers, 13th edn, Edinburgh: Oliver and Boyd.Google Scholar
Goldberg, M. L., Sheen, J.-Y., Gehring, W. J. & Green, M. M. (1983). Unequal crossing-over associated with asymmetrical synapsis between nomadic elements in the Drosophila melanogaster genome. Proceedings of the National Academy of Sciences USA 80, 5017–5021.CrossRefGoogle ScholarPubMed
Haigh, J. (1978). The accumulation of deleterious genes in a population. Theoretical Population Biology 14, 251–267.CrossRefGoogle ScholarPubMed
Hartl, D. L., Medhora, M., Green, L. & Dykhuizen, D. E. (1986). The evolution of DNA sequences in Escherichia coli. Philosophical Transactions of the Royal Society of London B 312, 191–204.Google ScholarPubMed
Hey, J. (1989). The transposable portion of the genome of Drosophila algonqin is very different from that of D. melanogaster. Molecular Biology and Evolution 6, 666–679.Google ScholarPubMed
Holliday, R. (1982). Gene conversion: a possible mechanism for eliminating selfish DNA. In Molecular and Cellular Mechanisms of Mutagenesis (ed. Lemont, J. F. and Generoso, W. M.), pp. 259–264. New York: Plenum.CrossRefGoogle Scholar
Kaplan, N. L. & Brookfield, J. F. Y. (1983). Transposable elements in Mendelian populations. III. Statistical results. Genetics 104, 485–495.Google ScholarPubMed
Kendall, M. G., Stuart, J. D. & Ord, J. K. (1983). The Advanced Theory of Statistics, 4th edn, vol. 3. London: Charles Griffin.Google Scholar
Kupiec, M. & Petes, T. (1988). Allelic and ectopic recombination between Ty elements in yeast. Genetics 119, 549–559.Google ScholarPubMed
Langley, C. H. & Aquadro, C. F. (1987). Restriction map variation in natural populations of Drosophila melanogaster: white-locus region. Molecular Biology and Evolution 4, 651–663.Google ScholarPubMed
Langley, C. H., Brookfield, J. F. Y. & Kaplan, N. L. (1983). Transposable elements in Mendelian populations. I. A theory. Genetics 104, 457–472.Google ScholarPubMed
Langley, C. H., Montgomery, E. A. & Quattlebaum, W. F. (1982). Restriction map variation in the Adh region of Drosophila. Proceedings of the National Academy of Sciences USA 79, 5631–5625.CrossRefGoogle ScholarPubMed
Langley, C. H., Montgomery, E. A., Hudson, R. R., Kaplan, N. H. & Charlesworth, B. (1988). On the role of unequal exchange in the containment of transposable element copy number. Genetical Research 52, 223–235.CrossRefGoogle ScholarPubMed
Langley, C. H., Shrimpton, A. E., Yamazaki, T., Miyashita, N., Matsuo, Y. & Aquadro, C. F. (1988). Naturally occurring variation in the restriction map of the Amy region of Drosophila melanogaster. Genetics 119, 619–629.CrossRefGoogle ScholarPubMed
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. 31–36. Orlando: Academic Press.Google Scholar
Leigh Brown, A. J. (1983). Variation at the 87A heat shock locus in Drosophila melanogaster. Proceedings of the National Academy of Sciences USA 80, 5350–5354.CrossRefGoogle Scholar
Leigh Brown, A. J. & Moss, J. E. (1987). Transposition of the I element and copia in natural populations of Drosophila melanogaster. Genetical Research 49, 121–128.CrossRefGoogle Scholar
Lewontin, R. C. & Prout, T. (1956). Estimation of the number of different classes in a population. Biometrics 12, 211–223.CrossRefGoogle Scholar
Lindsley, D. L. & Grell, E. H. (1968). Genetic Variations of Drosophila melanogaster. Washington: Carnegie Institute.Google Scholar
Lindsley, D. L. & Sandler, L. (1977). The genetic analysis of meiosis in female Drosophila melanogaster. Philosophical Transactions of the Royal Society of London, B277, 295–312.Google Scholar
Lindsley, D. L. & Zimm, G. (1982). Computerized stock list 3. Drosophila Information Service 57, 1–213.Google Scholar
Lindsley, D. L. & Zimm, G. (1986). The genome of Drosophila melanogaster, part 2: lethals; maps. Drosophila Information Service 64, 1–158.Google Scholar
Maynard Smith, J. (1978). The Evolution of Sex. Cambridge: Cambridge University Press.Google Scholar
Maynard Smith, J. & Haigh, J. (1974). The hitch-hiking effect of a favourable gene. Genetical Research 23; 23–35.CrossRefGoogle Scholar
Miklos, G. L. G., Healy, M. J., Pain, P., Howells, A. J. & Russell, R. J. (1984). Molecular genetic studies on the euchromatin-heterochromatin junction in the X chromosome of Drosophila melanogaster. I. A cloned entry point near to the uncoordinated (unc) locus. Chromosoma 89; 218–227.Google Scholar
Miklos, G. L. G., Yamamoto, M.-T., Davies, J. & Pirrotta, V. (1988). Microcloning reveals a high frequency of repetitive sequences characteristic of chromosome 4 and the β-heterochromatin of Drosophila melanogaster. Proceedings of the National Academy of Science USA 85, 2051–2055.CrossRefGoogle ScholarPubMed
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, 31–41.CrossRefGoogle Scholar
Montgomery, E. A. & Langley, C. H. (1983). Transposable elements in Mendelian populations. II. Distribution of three copia-like elements in a natural population. Genetics 104, 473–483.CrossRefGoogle Scholar
Mukai, T. & Yamaguchi, O. (1974). The genetic structure of natural populations of Drosophila. Genetics 82, 63–82.Google Scholar
Orgel, L. E. & Crick, F. H. C. (1980). Selfish DNA: the ultimate parasite. Nature 284, 604–607.CrossRefGoogle ScholarPubMed
Rubin, G. M., Brorein, W. J., Dunsmuir, P., Flavell, A. J., Strobel, J. J., Toole, J. J. & Young, E. (1981). ‘copia’-like transposable elements in the Drosophila genome. Cold Spring Harbor Symposium on Quantitative Biology 45, 619–628.CrossRefGoogle ScholarPubMed
Rudkin, G. T. (1965). The relative mutability of DNA in regions of the X chromosome of Drosophila melanogaster. Genetics 52, 665–681.CrossRefGoogle ScholarPubMed
Schaeffer, S. W., Aquadro, C. F. & Langley, C. H. (1988). Restriction map variation in the Notch region of Drosophila melanogaster. Molecular Biology and Evolution 5, 30–40.Google ScholarPubMed
Singh, R. S. & Rhomberg, L. R. (1987). A comprehensive study of genic variation in natural populations of Drosophila melanogaster. I. Estimates of gene flow from rare alleles. Genetics 115, 313–222.CrossRefGoogle ScholarPubMed
Snedecor, G. W. & Cochran, W. G. (1980). Statistical Methods, 7th edn.Ames, Iowa: Iowa State University Press.Google Scholar
Stephan, W. & Langley, C. H. (1989). Molecular genetic variation in the centromeric region of the X chromosome in three Drosophila ananassae populations. I. Contrasts between the vermilion and forked loci. Genetics 121, 89–99.CrossRefGoogle ScholarPubMed
Thomson, G. (1977). The effect of a selected locus on linked neutral loci. Genetics 85, 753–788.Google ScholarPubMed