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Selection against transposable elements in D. simulans and D. melanogaster

Published online by Cambridge University Press:  14 April 2009

C. Vieira
Affiliation:
Laboratoire de Biométrie, Génétique, Biologie des populations, UMR CNRS 5558, Université Lyon 1, 69622 Villeurbanne Cedex, France
C. Biémont*
Affiliation:
Laboratoire de Biométrie, Génétique, Biologie des populations, UMR CNRS 5558, Université Lyon 1, 69622 Villeurbanne Cedex, France
*
* Corresponding author.

Summary

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The insertion site numbers of the transposable elements (TEs) copia, mdgl, 412 and gypsy were determined in various natural populations of Drosophila melanogaster and D. simulans by in situ hybridization. We showed that, while all elements except gypsy had many insertion sites scattered over the chromosomes in D. melanogaster, only the 412 element in D. simulans presented a high number of insertions, and this number was lower than in D. melanogaster. This low 412 site number per genome in D. simulans was associated with a lower proportion of insertions on the X chromosome in comparison with D. melanogaster, as determined in diploid genomes (0·090 for D. simulans against 0·137 for D. melanogaster) and in haploid genomes (0·102 against 0·146), each value being, moreover, lower than the value of 0·20 expected on the hypothesis of no selection against insertional mutations. These results suggest that selection is a major mechanism explaining 412 copy number regulation in Drosophila, and is stronger in D. simulans than in D. melanogaster.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1996

References

Aquadro, C. F. (1992). Why is the genome variable? Insights from Drosophila. Trends in Genetics 8, 355362.CrossRefGoogle ScholarPubMed
Aquadro, C. F., Lado, K. M. & Noon, W. A. (1988). The rosy region of Drosophila melanogaster and Drosophila simulans. I. Contrasting levels of naturally occurring DNA restriction map variation and divergence. Genetics 119, 875888.CrossRefGoogle ScholarPubMed
Aquadro, C. F., Jennings, R. N. Jr, Bland, M. M., Laurie, C. C. & Langley, C. H. (1992). Patterns of naturally occurring restriction map variation, dopa descarboxylase activity variation and linkage disequilibrium in the DdC gene region of Drosophila melanogaster. Genetics 132, 443452.CrossRefGoogle Scholar
Aulard, S., Lemeunier, F., Hoogland, C., Chaminade, N., Brookfield, J. F. & Biémont, C. (1995). Chromosomal distribution and population dynamic of the 412 retrotransposon element in a natural population of Drosophila melanogaster. Chromosoma 103, 693699.CrossRefGoogle Scholar
Bayev, A. A. Jr, Lyubomirskaya, N. V., Dzhumagalies, E. B., Ananiev, E. V., Amiantova, I. G. & Ilyin, Y. V. (1984). Structural organisation of transposable element gypsy from Drosophila melanogaster and a nucleotide sequence of its long terminal repeats. Nucleic Acids Research 12, 37073723.CrossRefGoogle Scholar
Biémont, C. (1993). Population genetics of transposable DNA elements: a Drosophila point of view. In Transposable Elements and Evolution (ed. McDonald, J. F.), pp. 74–1. Dordrecht: Kluwer.CrossRefGoogle Scholar
Biémont, C. (1994).Dynamic equilibrium between insertion and excision of P elements in highly inbred lines from an M′ strain of Drosophila melanogaster. Journal of Molecular Evolution 39, 466472.CrossRefGoogle Scholar
Biémont, C. (1995). Estimating heterozygosity in Drosophila.from transposable element copy number. Trends in Genetics 11, 299.CrossRefGoogle Scholar
Bimont, C. & Gautier, C. (1988). Localisation polymorphism of mdg-1, copia, I and P mobile elements in genomes of Drosophila melanogaster, from data of inbred lines. Heredity 60, 335346.CrossRefGoogle Scholar
Biémont, C., Lemeunier, F., Garcia, M. P. Guerreiro, Brookfield, J. F., Gautier, C., Aulard, S. & Pasyukova, E. G. (1994). Population dynamic of the copia, mdgl, mdg3, gypsy, and P transposable elements in a natural population of Drosophila melanogaster. Genetical Research 63, 197212.CrossRefGoogle Scholar
Brookfield, J. F. Y., Montgomery, E. & Langley, C. H. (1984). Apparent absence of transposable elements related to the P elements of D. melanogaster in other species of Drosophila. Nature 310, 330332.CrossRefGoogle Scholar
Carmena, M. & Gonzalez, C. (1995). Transposable elements map in a conserved pattern of distribution extending from beta-heterochromatin to centromeres in Drosophila melanogaster. Chromosoma 103, 676684.CrossRefGoogle Scholar
Charlesworth, B. (1991). Transposable elements in natural populations with a mixture of selected and neutral insertion sites. Genetical Research 57, 127134.CrossRefGoogle ScholarPubMed
Charlesworth, B. & Charlesworth, D. (1983). The population dynamics of transposable elements. Genetical Research 42, 127.CrossRefGoogle Scholar
Charlesworth, B. & Langley, C. H. (1991). Population genetics of transposable elements in Drosophila. In Evolution at the Molecular Level (ed. Selander, R. K., Clark, A. G. & Whittam, T. S.), pp. 150–76. Sunderland, MA: Sinauer.Google Scholar
Charlesworth, B. & Lapid, A. (1989). A study of 10 transposable elements on X chromosomes from a population of Drosophila melanogaster. Genetical Research 54, 113125.CrossRefGoogle ScholarPubMed
Charlesworth, B., Lapid, A. & Canada, D., (1992 a). The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. I. Element frequencies and distribution. Genetical Research 60, 103114.CrossRefGoogle Scholar
Charlesworth, B., Lapid, A. & Canada, D., (1992 b). 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.CrossRefGoogle Scholar
Charlesworth, B., Jarne, P. & Assimacopoulos, S. (1994). The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. III. Element abundances in heterochromatin. Genetical Research 64, 183197.CrossRefGoogle Scholar
Csink, A. K. & McDonald, J. F. (1990). Copia expression is variable among natural populations of Drosophila. Genetics 126, 375385.CrossRefGoogle ScholarPubMed
Dowsett, A. P. & Young, M. W. (1982). Differing levels of dispersed repetitive DNA among closely related species of Drosophila. Proceedings of the National Academy of Sciences of the USA 79, 45704574.CrossRefGoogle ScholarPubMed
Dunsmuir, P., Brorein, W. J., Simon, M. A. & Rubin, G. M. (1980). Insertion of the Drosophila transposable element copia generates a 5 base pair duplication. Cell 21, 575579.CrossRefGoogle ScholarPubMed
Eeken, J. C. J. De Jong, A. W. M. & Green, M. M. (1987). The spontaneous mutation rate in Drosophila simulans. Mutation Research 192, 259262.Google ScholarPubMed
Finnegan, D. J., Rubin, G. M., Young, H. W. & Hogness, D. C. (1978). Repeated gene families in Drosophila. Cold Spring Harbor Symposia on Quantitative Biology 42, 10531064.CrossRefGoogle ScholarPubMed
Ilyin, Y. V., Chmeliauskaite, V. G. & Georgiev, G. P. (1980). Double-stranded sequences in RNA of Drosophila melanogaster: relation to mobile dispersed genes. Nucleic Acids Research 8, 34393457.CrossRefGoogle ScholarPubMed
Inoue, Y. H. & Yamamoto, M. T. (1987). Insertional DNA and spontaneous mutation at the white locus in Drosophila simulans. Molecular and General Genetics 209, 94100.CrossRefGoogle ScholarPubMed
Langley, C. H., Montgomery, E. A., Hudson, R., Kaplan, N. & Charlesworth, B. (1988). On the role of unequal exchange in the containment of transposable element copy number. Genetical Research 52, 223236.CrossRefGoogle ScholarPubMed
Lefevre, G. (1976). A photographic representation and interpretation of polytene chromosomes of Drosophila melanogaster salivary glands. In The Genetics and Biology of Drosophila, Vol. 1A (ed. Ashburne, M. & Novitski, E.), pp. 31–6. London: Academic Press.Google Scholar
Leibovitch, B. A., Glushkova, I. V., Pasyukova, E. G., Belyaeva, E. S. & Gvozdev, V. A. (1992). Comparative analysis of retrotransposon localization and mobility in sibling species Drosophila simulans and Drosophila melanogaster. Genelika 28, 8597.Google Scholar
Levis, R., Dunsmuir, P. & Rubin, G. M. (1980). Terminal repeats of the Drosophila transposable element copia: nucleotide sequence and genomic organisation. Cell 21, 581588.CrossRefGoogle Scholar
Martin, G., Wiemasz, D. & Schedl, P. (1983). Evolution of Drosophila repetitive-dispersed DNA. Journal of Molecular Biology 19, 203213.Google ScholarPubMed
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 Sciences of the USA 85, 20512055.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, 3141.CrossRefGoogle Scholar
Nuzhdin, S. V. (1995). The distribution of transposable elements on X chromosomes from a natural population of Drosophila simulans. Genetical Research 66, 159166.CrossRefGoogle ScholarPubMed
Pimpinelli, S., Berloco, M., Fanti, L., Dimitri, P., Bonaccorsi, S., Marchetti, E., Caizzi, R., Caggnese, C. & Gatti, M. (1995). Transposable elements are stable structural components of Drosophila melanogaster heterochromatin. Proceedings of the National Academy of Sciences of the USA 92, 38043808.CrossRefGoogle ScholarPubMed
Shevelyov, Y. Y., Balakireva, M. D. & Gvozdev, V. A. (1989). Heterochromatic regions in different Drosophila melanogaster stocks contain similar arrangements of moderate repeats with inserted copia-like elements (MDG1). Chromosomal, 117122.CrossRefGoogle Scholar
Sorsa, V. (1988). Chromosome maps of Drosophila, vol. II. Boca Raton, FL: CRC Press.Google Scholar
Suh, D. S., Choi, E. H., Yamazaki, T. & Harada, K. (1995). Studies on the transposition rates of mobile genetic elements in a natural population of Drosophila melanogaster. Molecular Biology and Evolution 12, 748758.Google Scholar
Tchurikov, N. A., Ilyin, Y. V., Skryabin, K. G., Ananiev, E. V., Bayev, A. A., Krayev, A. S., Zelentsova, E. S., Kulguskin, V. V., Lyubomirskaya, N. V. & Georgiev, G. P. (1981). General properties of mobile dispersed genetic elements in Drosophila. Cold Spring Harbor Symposia on Quantitative Biology 45, 655665.CrossRefGoogle ScholarPubMed
Vaury, C., Bucheton, A. & Pélisson, A. (1989). The β-heterochromatic sequences flanking the I elements are themselves defective transposable elements. Chromosoma 98,215–24.CrossRefGoogle ScholarPubMed
Vieira, C. & Biémont, C. (1996). Geographical variation in insertion site number of retrotransposon 412 in Drosophila simulans. Journal of Molecular Evolution (in the Press).CrossRefGoogle ScholarPubMed