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A test for the role of natural selection in the stabilization of transposable element copy number in a population of Drosophila melanogaster

Published online by Cambridge University Press:  14 April 2009

Elizabeth Montgomery ,
Brian Charlesworth  and
Charles H. Langley
Elizabeth Montgomery*
Affiliation:
Laboratory of Genetics, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina, 27709
Brian Charlesworth
Affiliation:
Department of Biology, The University of Chicago, Chicago, IL 60637
Charles H. Langley
Affiliation:
Laboratory of Genetics, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina, 27709
*
Elizabeth Montgomery, Laboratory of Genetics, NIEHS, Research Triangle Park, N C 27709, USA.
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The numbers of members of three families of copia-like elements were counted on twenty X, 2nd and 3rd chromosomes collected from a natural population of Drosophila melanogaster. Theoretical predictions were computed for two models of copy number stabilization: (1) element frequencies are regulated by a simple genetic process such as copy number dependent transposition or excision, independent of chromosomal location; (2) elements are eliminated by natural selection against mutational effects of their insertion into the chromosome. Since insertions into the X can be expected to suffer more selection than autosomal insertions, due to expression of mutant phenotypes in the hemizygous state, hypothesis 2, called the disproportional model, predicts that the proportion of elements on the X will be smaller than the proportion of the genome contributed by the X, while hypothesis 1, called the equiproportional model, predicts that this proportionality will be unaffected. Two of the elements, 297 and roo, showed no evidence for deficiency of X-linked elements, but the data for a third element, 412, were consistent with the prediction based on the selective model.

These results indicate that simple selection against mutational effects of insertions of transposable elements is not generally adequate to account for their distribution within populations. We argue that a mechanism such as recombination between elements at different chromosomal sites, leading to rearrangements with highly deleterious, dominant effects could play a role in stabilizing copy number. This process would lead to a higher abundance of elements in genomic regions with restricted crossing over. We present some data indicating such an effect, and discuss possible interpretations.

Type
Research Article
Information
Genetics Research , Volume 49 , Issue 1 , February 1987 , pp. 31 - 41
Copyright
Copyright © Cambridge University Press 1987

References

Aquadro, C. F., Deese, S. F., Bland, M. M., Langley, C. H. & Laurie-Ahlberg, C. C. (1986). Molecular population genetics of alcohol dehydrogenase gene region of Drosophila melanogaster. Genetics. (In the Press.)CrossRefGoogle Scholar
Brahic, M. & Haase, A. T. (1978). Detection of viral sequences of low reiteration frequency by in situ hybridization. Proceedings of the National Academy of Sciences, USA 75, 6125–6129.CrossRefGoogle ScholarPubMed
Brookfield, J. F. Y., Montgomery, E. A. & Langley, C. H. (1984). Apparent absence of transposable elements related to the P element of D. melanogaster in other species of Drosophila. Nature 310, 330–332.CrossRefGoogle Scholar
Charlesworth, B. (1985 a). Recombination, genome size and chromosome number. In The Evolution of Genome Size (ed. T., Cavalier-Smith), pp. 489–513. Chichester: John Wiley.Google Scholar
Charlesworth, B. (1985 b). The population genetics of transposable elements. In Population Genetics and Molecular Evolution (ed. Ohta, T. and K.-I., Aoki), pp. 213–232. Berlin: Springer-Verlag.Google 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 tranposable elements. Genetics 112, 359–383.CrossRefGoogle Scholar
Charlesworth, B., Langley, C. H. & Stephan, W. (1986). The evolution of restricted recombination and the accumulation of repeated DNA sequences. Genetics 112, 947–962.CrossRefGoogle ScholarPubMed
Chovnick, A. (1973). Gene conversion and transfer of genetic information within the inverted region of inversion heterozygotes. Genetics 75, 123–131.CrossRefGoogle ScholarPubMed
Davis, P. S., Shen, M. W. & Judd, B. H. (1986). Asymetrical pairings of transposons in and proximal to the white locus of Drosophila account for four classes of regularly occurring exchange products. Proceedings of the National Academy of Sciences, USA. (In the Press.)Google Scholar
Engels, W. R. (1983). The P family of transposable elements in Drosophila. Annual Review of Genetics 17, 315–344.CrossRefGoogle Scholar
Felsenstein, J. (1974). The evolutionary advantage of recombination. Genetics 78, 737–756.CrossRefGoogle ScholarPubMed
Goldberg, M. L., Sheen, J.-Y., Gehring, W. J. & Green, M. M. (1983). Unequal crossing-over associated with asymetrical synapsis between nomadic elements in the Drosophila melanogaster genome. Proceedings of the National Academy of Sciences, USA 80, 5017–5021.CrossRefGoogle Scholar
Golding, G. D., Aquadro, C. F. & Langley, C. H. (1986). Sequence evolution within populations under multiple types of mutation. Proceedings of the National Academy of Sciences, USA 83, 427–431.CrossRefGoogle ScholarPubMed
Haigh, J. (1978). The accumulation of deleterious genes in a population – Muller's ratchet. Theoretical Population Biology 14, 251–267.CrossRefGoogle Scholar
Haldane, J. B. S. (1927). A mathematical theory of natural and artificial selection. Part V. Selection and Mutation. Proceedings of the Cambridge Philosophical Society 23, 838–844.CrossRefGoogle Scholar
Hilliker, A. J., Appels, R. & Schalet, A. (1980). The genetic analysis of D. melanogaster heterochromatin. Cell 21, 607–619.CrossRefGoogle ScholarPubMed
Inouye, S., Saigo, K., Yamada, K. & Kuchino, Y. (1986). Identification and nucleotide sequence determination of a potential primer tRNA for reverse transcription of a Drosophila retrotransposon, 297. Nucleic Acid Research. (In the Press.)CrossRefGoogle Scholar
Ishii, K. & Charlesworth, B. (1977). Associations between aliozyme loci and gene arrangements due to hitch-hiking effects of new inversions. Genetical Research 30, 93–106.CrossRefGoogle Scholar
Jaenisch, R. (1980). Retroviruses and embryogenesis: micro- injection of Moloney murine leukemia virus into midgestation mouse embryos. Cell 19, 181–188.CrossRefGoogle Scholar
Jenkins, N. A. & Copeland, N. G. (1985). High frequency germline acquisition of ecotropic MuLV Proviruses in SWR/J-RF/J hybrid mice. Cell 43, 811–819.CrossRefGoogle ScholarPubMed
Judd, B. H., Shen, M. W. & Kaufman, T. C. (1972). The anatomy and function of a segment of the X chromosome of Drosophila melanogaster. Genetics 71, 139–156.CrossRefGoogle ScholarPubMed
Kaplan, N. & Brookfield, J. F. Y. (1983). Transposable elements in Mendelian populations. III. Statistical results. Genetics 104, 485–495.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, 6633–6637.CrossRefGoogle ScholarPubMed
Langley, C. H., Brookfield, J. F. Y. & Kaplan, N. (1983). Transposable elements in Mendelian populations. I. A theory. Genetics 104, 457–471.CrossRefGoogle 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, 5631–5635.CrossRefGoogle ScholarPubMed
Lefevre, G. (1976). A photographic representation and interpretation 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
Lefevre, G. (1981). The distribution of randomly recovered X-ray-induced sex-linked genetic effects in Drosophila melanogaster. Genetics 99, 461–480.CrossRefGoogle ScholarPubMed
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
Levis, R. & Rubin, G. M. (1982). The unstable w DZL mutation of Drosophila is caused by a 13 kilobase insertion that is imprecisely excised in phenotypic revertants. Cell 30, 543–550.CrossRefGoogle ScholarPubMed
Lindsley, D. L. & Grell, E. H. (1968). Genetic Variations of Drosophila melanogaster. Washington: Carnegie Institute.Google Scholar
Maeda, N. & Smithies, O. (1986). The evolution of multi-gene families with special reference to human haptoglobin genes. Annual Review of Genetics. (In the Press.)CrossRefGoogle Scholar
Maniatis, T., Fritsch, E. F. & Sambrook, J. (1982). Molecular Cloning. A Laboratory Manual. Coldy Spring Harbor: Cold Spring Harbor Laboratory.Google Scholar
Meyerowitz, E. M. & Hogness, D. S. (1982). Molecular organization of a Drosophila puff site that responds to ecdysone. Cell 28, 165–176.CrossRefGoogle ScholarPubMed
Mikus, M. D. & Petes, T. D. (1982). Recombination between genes located on nonhomologous chromosomes in Saccharomyces cerevisiae. Genetics 101, 369–404.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
Pardue, M. L. & Gall, J. G. (1975). Nucleic acid hybridization to the DNA of cytological preparations. Methods in Cell Biology 10, 1–17.CrossRefGoogle Scholar
Pimpineili, S., Bonaccorsi, S., Gatti, M. & Sandler, L. (1986). The peculiar genetic organization of Drosophila heterochromatin. Trends in Genetics 2, 17–20.CrossRefGoogle Scholar
Potter, S. S., Brorein, W. J., Dunsmuir, P. & Rubin, G. M. (1979). Transposition of elements of the 412, copia and 297 dispersed repeated gene families of Drosophila. Cell 17, 415–427.CrossRefGoogle ScholarPubMed
Rigby, P. W. J., Dieckmann, J. M., Rhodes, C. & Berg, P. (1977). Labelling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase. I. Journal of Molecular Biology 113, 237–251.CrossRefGoogle ScholarPubMed
Roeder, G. S. (1983). Unequal crossing over between yeast transposable elements. Molecular and General Genetics 190, 117–121.CrossRefGoogle Scholar
Rowe, W. P. & Kozak, C. A. (1980). Germline reinsertions of AKR murine leukemia virus genomes in Akv-1 congenic mice. Proceedings of the National Academy of Sciences, USA 77, 4871–4874.CrossRefGoogle ScholarPubMed
Rubin, G. M., Brorein, W. J., Dunsmuir, P., Flavell, A. J., Levis, R., Strobel, E., Toole, J. J. & Young, E. (1981). Copia-like transposable elements in the Drosophila genome. Cold Spring Harbor Symposium on Quantitative Biology 45, 617–628.CrossRefGoogle ScholarPubMed
Rudkin, G. T. (1965). The relative mutabilities of DNA in regions of the X chromcsome of Drosophila melanogaster. Genetics 52, 665–681.CrossRefGoogle ScholarPubMed
Scherer, G., Tschudi, C., Perera, J., Delias, H. & Pirrotta, J. (1982). B104, a new dispersed repeated gene family in Drosophila melanogaster and its analogies with retroviruses. Journal of Molecular Biology 157, 435–451.CrossRefGoogle ScholarPubMed
Shapiro, J. A. (1983). Mobile Genetic Elements. Orlando: Academic Press.Google Scholar
Simmons, M. J. & Crow, J. F. (1977). Mutations affecting fitness in Drosophila populations. Annual Review of Genetics 11, 49–78.CrossRefGoogle ScholarPubMed
Sims, S. H., MacGregor, H. C., Pellatt, P. S. & Homer, V. (1984). Chromosome 1 in crested and marbled newts (Triturus). An extraordinary case of heteromorphism and independent evolution. Chromosoma 89, 169–185.CrossRefGoogle Scholar
Spierer, P., Spierer, A., Bender, W. & Hogness, D. S. (1983). Molecular mapping of genetic and chromomeric units in Drosophila melanogaster. Journal of Molecular Biology 168, 35–50.CrossRefGoogle ScholarPubMed
Steinemann, M. (1982). Multiple sex chromosomes in Drosophila miranda: a system to study the degeneration of a chromosome. Chromosoma 89, 59–76.CrossRefGoogle Scholar
Strobel, E. (1982). Mobile dispersed repeated DNA elements in the Drosophila genome. Federation Proceedings 41, 42–44.Google ScholarPubMed
Wallace, B. (1968). Mutation rates for autosomal lethals in Drosophila melanogaster. Genetics 60, 389–393.CrossRefGoogle ScholarPubMed
Wright, T. R. F., Beerman, W., Marsh, J. L., Bishop, C. P., Steward, R., Black, B., Tomsett, C. A. D. & Wright, E. Y. (1981). The genetics of dopa decarboxylase in Drosophila melanogaster. IV. The genetics and cytology of the 37B10–37D1 region. Chromosoma 83, 45–58.CrossRefGoogle ScholarPubMed
Young, M. W. & Schwartz, H. E. (1981). Nomadic gene families in Drosophila. Cold Spring Harbor Symposium on Quantitative Biology 45, 629–640.CrossRefGoogle ScholarPubMed
Young, M. W. (1979). Middle repetitive DNA: a fluid component of the Drosophila genome. Proceedings of the National Academy of Sciences, USA 76, 6274–6278.CrossRefGoogle ScholarPubMed
Yuki, S., Ishimaru, S., Inouye, S. & Saigo, K. (1986). Identification of genes for reverse transcriptase-like enzymes in two Drosophila retrotransposons, 412 and gypsy; a rapid detection method of reverse transcriptase genes using YXDD box probes. Nucleic Acids Research. (In the Press.)CrossRefGoogle Scholar