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Population dynamics of the copia, mdg1, mdg3, gypsy, and P transposable elements in a natural population of Drosophila melanogaster

Published online by Cambridge University Press:  14 April 2009

C. Biémont ,
F. Lemeunier ,
M. P. Garcia Guerreiro ,
J. F. Brookfield ,
C. Gautier ,
S. Aulard  and
E. G. Pasyukova
C. Biémont
Affiliation:
Laboratoire de Biométrie, Génétique, Biologie des populations, URA C.N.R.S. 243, Université Lyon 1, 69621 Villeurbanne Cedex, France
F. Lemeunier
Affiliation:
Laboratoire de Biologie et Génétique évolutives C.N.R.S., 91198, Gif-sur-Yvette Cedex, France
M. P. Garcia Guerreiro
Affiliation:
Laboratoire de Biométrie, Génétique, Biologie des populations, URA C.N.R.S. 243, Université Lyon 1, 69621 Villeurbanne Cedex, France
J. F. Brookfield
Affiliation:
University of Nottingham, Department of Genetics, Queen's Medical Centre, Nottingham NG7 2UH, UK
C. Gautier
Affiliation:
Laboratoire de Biométrie, Génétique, Biologie des populations, URA C.N.R.S. 243, Université Lyon 1, 69621 Villeurbanne Cedex, France
S. Aulard
Affiliation:
Laboratoire de Biologie et Génétique évolutives C.N.R.S., 91198, Gif-sur-Yvette Cedex, France
E. G. Pasyukova
Affiliation:
Institute of Molecular Genetics, Russia Academy of Science, Kurchatov Sq. 46, 123182, Moscow, Russia
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The insertion site polymorphism of the copia, mdg1, mdg3, gypsy, and P transposable elements was analysed by in situ hybridization to the polytene chromosomes in genomes of males from a natural population of Drosophila melanogaster. Parameters of various theoretical models of the population biology of transposable elements were estimated from our data, and different hypotheses explaining TE copy number containment were tested. The copia, mdg1 and gypsy elements show evidence for a deficiency of insertions on the X chromosomes, a result consistent with selection against the mutational effects of insertions. On the contrary, mdg3 and P copy numbers fit a neutral model with a balance between regulated transposition and excisions. There is no strong evidence of a systematic accumulation of elements in the distal and proximal regions of the chromosomes where crossing over and ectopic exchanges are reduced. For all chromosome arms but 3L, however, the TE site density increases from the proximal to the distal parts of the chromosomes (the centromeric regions were excluded in this analysis) with sometimes a sharp decrease in density at the extreme tip, following in part the exchange coefficient. The way the copy number of TEs is contained in genomes depends thus on the element considered, and on various forces acting simultaneously, indicating that models of TE dynamics should include details of each element.

Type
Research Article
Information
Genetics Research , Volume 63 , Issue 3 , June 1994 , pp. 197 - 212
Copyright
Copyright © Cambridge University Press 1994

References

Ajioka, J. W. & Eanes, W. F. (1989). The accumulation of P-elements on the tip of the X chromosome in populations of Drosophila melanogaster. Genetical Research 53, 1–6.CrossRefGoogle ScholarPubMed
Ajioka, J. W. & Hartl, D. L. (1989). Population dynamics of transposable elements. In Mobile DNA (ed. Berg, D. E., and Howe, M.M.), pp. 939–958. Washington D.C.: American Society for Microbiology.Google Scholar
Ananiev, E. V., Barsky, V. E., Ilyin, Y. V. & Ryzic, M. V. (1984). The arrangement of transposable elements in the polytene chromosomes of Drosophila melanogaster. Chromosoma 90, 366–377.CrossRefGoogle Scholar
Baker, R. J. & Wichman, H. A. (1990). Retrotransposon MYS is concentrated on the sex chromosomes: implications for copy number containment. Evolution 44, 2083–2088.CrossRefGoogle ScholarPubMed
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, 3707–3723.CrossRefGoogle Scholar
Begun, D. J. & Aquadro, C. F. (1991). Molecular population genetics of the distal portion of the X chromosome in Drosophila: evidence for genetic hitchhiking of the yellowachaete region. Genetics 129, 1147–1158.CrossRefGoogle ScholarPubMed
Begun, D. J. & Aquadro, C. F. (1992). Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356, 519–520.CrossRefGoogle ScholarPubMed
Belyaeva, E. S., Ananiev, E. V. & Gvozdev, V. A. (1984). Distribution of mobile dispersed genes (mdg-1 and mdg-3) in the chromosomes of Drosophila melanogaster. Chromosoma 90, 16–19.CrossRefGoogle Scholar
Biémont, C. (1986). Polymorphism of the mdg-1 and I mobile elements in Drosophila melanogaster. Chromosoma 93, 393–397.CrossRefGoogle Scholar
Biémont, C. (1992). Population genetics of transposable elements. A drosophila point of view. Genetica 86, 67–84.CrossRefGoogle ScholarPubMed
Biémont, C. & Aouar, A. (1987). Copy-number dependent transpositions and excisions of the mdg-1 mobile element in inbred lines of Drosophila melanogaster. Heredity 58, 39–47.CrossRefGoogle Scholar
Biémont, C., Aouar, A. & Arnault, C. (1987). Genome reshuffling of the copia element in a Drosophila melanogaster inbred line. Nature 329, 742–744.CrossRefGoogle Scholar
Biémont, C., Arnault, C., Heizmann, A. & Ronsseray, S. (1990 a). Massive changes in genomic locations of P elements in an inbred line of Drosophila melanogaster. Naturwissenschaften 77, 485–488.CrossRefGoogle Scholar
Biémont, 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, 335–346.CrossRefGoogle Scholar
Biémont, C., Gautier, C. & Heizmann, A. (1988). Independent regulation of mobile element copy number in Drosophila melanogaster inbred lines. Chromosoma 96, 291–294.CrossRefGoogle Scholar
Biémont, C., Ronsseray, S., Anxolabéhère, D., Izaabel, H. & Gautier, C. (1990 b). Localization of P elements, copy number regulation, and cytotype determination in Drosophila melanogaster. Genetical Research 56, 3–14.CrossRefGoogle ScholarPubMed
Biesmann, H., Champion, L. E., O'Hair, M., Ikenaga, K., Kasravi, B. & Mason, J. M. (1992). Frequent transpositions of Drosophila melanogaster Het-A transposable elements to receding chromosome ends. EMBO Journal 11, 4459–4469.CrossRefGoogle Scholar
Bolshakov, V. N., Zharkikh, A. A. & Zhimulev, I. F. (1985). Intercalary heterochromatin in Drosophila. II. Heterochromatic features in relation to local DNA content along the polytene chromosomes of Drosophila melanogaster. Chromosoma 92, 200–208.CrossRefGoogle Scholar
Brookfield, J. F. Y. (1986). The population biology of transposable elements. Philosophical Transactions of the Royal Society of London B 312, 217–226.Google ScholarPubMed
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 population. In Plant Transposable Elements (ed. Nelson, O.), pp. 189–212. New York, London: Plenum Press.CrossRefGoogle Scholar
Charlesworth, B. & Charlesworth, D. (1983). The population dynamics of transposable elements. Genetical Research 42, 1–27.CrossRefGoogle Scholar
Charlesworth, B. & Langley, C. H. (1986). The evolution of self-regulated transposition of transposable elements. Genetics 112, 359–383.CrossRefGoogle ScholarPubMed
Charlesworth, B. & Langley, C. H. (1989). The population genetics of Drosophila transposable elements. Annual Review of Genetics 23, 251–287.CrossRefGoogle ScholarPubMed
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., and Whittam, T. S.). Sunderland: Sinauer Associates Inc.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, 113–125.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. Elements, frequencies and distribution. Genetical Research 60, 103–114.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, 115–130.CrossRefGoogle Scholar
Daniels, S. B. & Strausbaugh, L. D. (1986). The distribution of P element sequences in Drosophila: the willistoni and saltans species group. Journal of Molecular Evolution 23, 138–148.CrossRefGoogle Scholar
Danilevkaya, O. N. & Lapta, G. E. (1991). Long telomeres in the polytene chromosomes of Drosophila melanogaster are associated with amplification of subtelomeric repeat sequences. Génétique, Sélection, Evolution 23, 15–24.CrossRefGoogle Scholar
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, 575–579.CrossRefGoogle ScholarPubMed
Eanes, W. F., Wesley, C., Hey, J., Houle, D. & Ajioka, J. (1988). The fitness consequences of P element insertion in Drosophila melanogaster. Genetical Research 52, 17–26.CrossRefGoogle Scholar
Eanes, W. F., Wesley, C. & Charlesworth, B. (1992). Accumulation of P elements in minority inversions in natural populations of Drosophila melanogaster. Genetical Research 59, 1–9.CrossRefGoogle ScholarPubMed
Echalier, G. (1989). Drosophila retrotransposons; interactions with genome. Advances in Virus Research 36, 33–105.CrossRefGoogle ScholarPubMed
Eggleston, W. B., Johnson-Schlitz, D. M. & Engels, W. R. (1988). P-M hybrid dysgenesis does not mobilize other transposable element families in Drosophila melanogaster. Nature 331, 368–370.CrossRefGoogle ScholarPubMed
Engels, W. R., Johnson-Schlitz, D. M., Eggleston, W. B. & Sved, J. (1990). High frequency P element loss in Drosophila is homolog dependent. Cell 62, 515–525.CrossRefGoogle ScholarPubMed
Ewens, W. J. (1979). Mathematical Population Genetics. Berlin: Springer-Verlag.Google Scholar
Finnegan, D. J. (1989). Eukaryotic transposable elements and genome evolution. Trends in Genetics 5, 103–107.CrossRefGoogle ScholarPubMed
Freund, R. & Meselson, M. (1984). Long terminal repeat nucleotide sequence and specific insertion of the gypsy transposon. Proceedings of the National Academy of Sciences, USA 81, 4462–4464.CrossRefGoogle ScholarPubMed
Georgiev, P. G., Kiselev, S. L., Simonova, O. B. & Gerasimova, T. I. (1990). A novel transposition system in Drosophila melanogaster depending on the stalker mobile genetic element. EMBO Journal 9, 2037–2044.CrossRefGoogle ScholarPubMed
Gerasimova, T. I., Matyunina, L. V., Ilyin, Y. V. & Georgiev, G. P. (1984). Simultaneous transposition of different mobile elements. Relation to multiple mutagenesis in Drosophila melanogaster. Molecular and General Genetics 194, 517–522.CrossRefGoogle Scholar
Gerasimova, T. I., Mizrokhi, L. J. & Georgiev, G. P. (1984). Transposition bursts in genetically unstable Drosophila melanogaster. Nature 309, 714–716.CrossRefGoogle Scholar
Goldberg, M. L., Sheen, J.-Y., Gehring, W. & 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
Hale, D. W. (1992). Sex chromosomes, heterochromatin, and retrotransposon accumulation in deer mice. Evolution 46, 1955–1958.CrossRefGoogle ScholarPubMed
Harada, K., Yukuhiro, K. & Mukai, T. (1990). Transposition rates of movable genetic elements in Drosophila melanogaster. Proceedings of the National Academy of Sciences, USA 87, 3248–3252.CrossRefGoogle ScholarPubMed
Hey, J. (1989). The transposable portion of the genome of Drosophila algonquin is very different from that in Drosophila melanogaster. Molecular Biology and Evolution 6, 66–79.Google Scholar
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, 3439–3457.CrossRefGoogle ScholarPubMed
Ising, B. & Block, K. (1981). Derivation-dependent distribution of insertion sites for a Drosophila transposon. Cold Spring Harbor Symposia on Quantitative Biology 45, 527–544.CrossRefGoogle ScholarPubMed
Jenkins, N. A. & Copeland, N. G. (1985). High frequency germ-line acquisition of ecotropic MuLV proviruses in SWR/J-RF/J hybrid mice. Cell 43, 811–819.CrossRefGoogle Scholar
Kaplan, N. L. & Brookfield, J. F. Y. (1983). Transposable elements in Mendelian populations. III. Statistical results. Genetics 104, 485–495.CrossRefGoogle ScholarPubMed
Kaplan, N. L., Darden, T. & Langley, C. H. (1985). Evolution and extinction of transposable elements in Mendelian populations. Genetics 109, 459–480.CrossRefGoogle ScholarPubMed
Karpen, G. H. & Spradling, A. C. (1992). Analysis of subtelomeric heterochromatin in the Drosophila minichromosome Dp 1187 by single P element insertional mutagenesis. Genetics 132, 737–753.CrossRefGoogle Scholar
Kidwell, M. G. (1983). Evolution of hybrid dysgenesis determinants in Drosophila melanogaster. Proceedings of the National Academy of Sciences, USA 80, 1655–1659.CrossRefGoogle ScholarPubMed
Kim, A. I. & Belyaeva, E. S. (1991). Transposition of mobile elements gypsy (mdg4) and hobo in germ-lime and somatic cells of a genetically unstable mutator strain of Drosophila melanogaster. Molecular and General Genetics 229, 437–444.CrossRefGoogle ScholarPubMed
Kimura, M. & Crow, J. F. (1964). The number of alleles that can be maintained in a finite population. Genetics 49, 725–738.CrossRefGoogle Scholar
Langley, C. H., Brookfield, J. F. Y. & Kaplan, N. (1983). Transposable elements in Mendelian populations. I. A theory. Genetics 104, 457–472.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, 223–236.CrossRefGoogle ScholarPubMed
Lansman, R. A., Shade, R. O., Grigliatti, T. A. & Brock, H. W. (1987). Evolution of P transposable elements: sequences of Drosophila nebulosa P elements. Proceedings of the National Academy of Sciences, USA 84, 6491–6495.CrossRefGoogle ScholarPubMed
Leigh-Brown, A. J. & Moss, J. E. (1987). Transposition of the I element and copia in a natural population of Drosophila melanogaster. Genetical Research 49, 121–128.CrossRefGoogle Scholar
Levis, R., Dunsmuir, P. & Rubin, G. M. (1980). Terminal repeats of the Drosophila transposable element copia: nucleotide sequence and genomic organisation. Cell 21, 579–581.CrossRefGoogle Scholar
Lindsley, D. L. & Sandier, L. (1977). The genetic analysis of meiosis in female Drosophila melanogaster. Philosophical Transactions of the Royal Society of London B 277, 295–312.Google ScholarPubMed
Lyubomirskaya, N. V., Arkhipova, I. R., Ilyin, Y. V. & Kim, A. I. (1990). Molecular analysis of the gypsy (mdg4) retrotransposon in two strains differing by genetic instability. Molecular and General Genetics 223, 305–309.CrossRefGoogle ScholarPubMed
Mackay, T. F. C. (1989). Transposable elements and fitness in Drosophila melanogaster. Genome 31, 284–295.CrossRefGoogle ScholarPubMed
Mevel-Ninio, M., Mariol, M. C. & Gans, M. (1989). Mobilization of the gypsy and copia retrotransposons in Drosophila melanogaster induces reversion of the ovoD dominant female-sterile mutations: molecular analysis of revertant alleles. EMBO Journal 8, 1549–1558.CrossRefGoogle 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 Sciences, USA 85, 2051–2055.CrossRefGoogle ScholarPubMed
Modolell, J., Bender, W. & Meselson, M. (1983). Drosophila melanogaster mutations suppressible by the suppressor of Hairy-wing are insertions of a 7·3-kilobase mobile element. Proceedings of the National Academy of Sciences, USA 80, 1678–1682.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., Huang, S. M., Langley, C. H. & Judd, B. H. (1991). Chromosome rearrangement by ectopic recombination in Drosophila melanogaster: genome structure and evolution. Genetics 129, 1085–1098.CrossRefGoogle ScholarPubMed
Montgomery, E. A. & Langley, C. H. (1983). Transposable elements in Mendelian populations. II. Distribution of three copia-like elements in a natural population of Drosophila melanogaster. Genetics 104, 473–483.CrossRefGoogle Scholar
O'Hare, K., Driver, A., McGrath, S. & Johnson-Schlitz, D. M. (1992). Distribution and structure of cloned P elements from the Drosophila melanogaster P strain n2. Genetical Research 60, 33–41.CrossRefGoogle 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, 25–35.CrossRefGoogle ScholarPubMed
Pasyukova, E. G., Belyaeva, E. S., Ilyinskaya, L. E. & Gvozdev, V. A. (1988). Outcross-dependent transpositions of copia-like mobile genetic elements in chromosomes of an inbred Drosophila melanogaster stock. Molecular and General Genetics 212, 281–286.CrossRefGoogle Scholar
Pasyukova, E. G. & Nuzhdin, S. V. (1992). Mobilization of retrotransposon copia in genome. Genetika 28, 5–18.Google Scholar
Peifer, M. & Bender, W. (1988). Sequences of the gypsy transposon of Drosophila necessary for its effects on adjacent genes. Proceedings of the National Academy of Sciences, USA 85, 9650–9654.CrossRefGoogle ScholarPubMed
Ronsseray, S. & Anxolabéhére, D. (1986). Chromosomal distribution of P and I transposable elements in a natural population of Drosophila melanogaster. Chromosoma 94, 433–440.CrossRefGoogle Scholar
Ronsseray, S., Lehmann, M. & Anxolabéhére, D. (1989). Distribution of P and I mobile elements copy number in Drosophila melanogaster populations. Chromosoma 98, 207–214.CrossRefGoogle Scholar
Ronsseray, S., Lehmann, M. & Anxolabéhére, D. (1991). The maternally inherited regulation of P elements in Drosophila melanogaster can be elicited by two P copies at cytological site 1A on the X chromosome. Genetics 129, 501–512.CrossRefGoogle ScholarPubMed
Scheinker, V. S., Lozovskaya, E. R., Bishop, J. G., Corces, V. G. & Evgen'ev, M. B. (1990). A long terminal repeat containing retrotransposon is mobilized during hybrid dysgenesis in Drosophila virilis. Proceedings of the National Academy of Sciences, USA 87, 9615–9619.CrossRefGoogle ScholarPubMed
Steinemann, M. (1982). Multiple sex chromosomes in Drosophila miranda: a system to study the degeneration of a chromosome. Chromosoma 86, 59–76.CrossRefGoogle Scholar
Stephan, W. & Langley, C. H. (1992). Evolutionary consequences of DNA mismatch inhibited repair opportunity. Genetics 132, 567–574.CrossRefGoogle ScholarPubMed
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, 429–439.CrossRefGoogle ScholarPubMed
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, 655–665.CrossRefGoogle ScholarPubMed
Vaury, C., Bucheton, A. & Pélisson, A. (1989). The β heterochromatic sequences flanking the I elements are themselves defective transposable elements. Chromosoma 98, 215–224.CrossRefGoogle ScholarPubMed
Wilke, C. M. & Adams, J. (1992). Fitness effects of Ty transposition in Saccharomyces cerevisiae. Genetics 131, 31–42.CrossRefGoogle ScholarPubMed
Yamaguchi, O., Yamazaki, T., Saigo, K., Mukai, T. & Robertson, A. (1987). Distribution of three transposable elements, P, 297, and copia in natural populations of Drosophila melanogaster. Japanese Journal of Genetics 62, 205–216.Google Scholar