The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. II. Inferences on the nature of selection against elements | Genetics Research | Cambridge Core (original) (raw)
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 nine families of transposable elements among a sample of autosomes isolated from a natural population of Drosophila melanogaster, by means of in situ hybridization of biotinylated probes to polytene chromosomes. There is no general tendency for elements to accumulate at the tips of chromosomes. Elements tend to be present in excess of random expectation in the euchromatin proximal to the centromeres of the major autosomes, and on chromosome four. There is considerable heterogeneity between different families in the extent of this excess. The overall abundance of element families is inversely related to the extent to which they accumulate proximally. The level of proximal accumulation for the major autosomes is similar to that on the fourth chromosome, but less than that for the X chromosome. There is an overall deficiency of elements in the mid-section of the X compared with the mid-sections of the major autosomes, with considerable heterogeneity between families. The magnitude of this deficiency is positively related to the extent to which elements accumulate proximally. No such deficiency is seen if the proximal regions of the X and autosomes are compared. There is a small and non-significant excess of elements in third chromosomes carrying inversions. There is some between-year heterogeneity in element abundance. The implications of these findings are discussed, and it is concluded that they generally support the hypothesis that transposable element abundance is regulated primarily by the deleterious fitness consequences of meiotic ectopic exchange between elements. If this is the case, such exchange must be very infrequent in the proximal euchromatin, and the elements detected in population surveys of this kind must be inserted into sites where they have negligible mutational effects on fitness.
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, 519–520.CrossRefGoogle ScholarPubMed
Bingham, P. M. & Zachar, Z. (1989). Retroposons and the FB transposon from Drosophila melanogaster. In Mobile DNA (ed. Berg, D. E. and Howe, M. M.), pp. 485–502. Washington D.C.: American Society of Microbiology.Google 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
Charlesworth, B. (1991). Transposable elements in natural populations with a mixture of insertion sites. Genetical Research 57, 127–134.CrossRefGoogle ScholarPubMed
Charlesworth, B. & Charlesworth, D. (1983). The population dynamics of transposable elements. Genetical Research 42, 1–27.CrossRefGoogle 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
Charlesworth, B. & Langley, C. H. (1989). The population genetics of Drosophila transposable elements. Annual Review of Genetics 23, 251–287.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, 113–125.CrossRefGoogle ScholarPubMed
Charlesworth, B.Lapid, A. & Canada, D. (1992). The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. I. Element frequencies and distribution. Genetical Research 60, 103–114.CrossRefGoogle Scholar
Charlesworth, B.Coyne, J. A. & Barton, N. H. (1987). The relative rates of evolution of sex chromosomes and autosomes. American Naturalist 130, 113–146.CrossRefGoogle Scholar
Coyne, J. A. & Milstead, B. (1987). Long-distance migration of Drosophila melanogaster. 3. Dispersal of alleles from a Maryland orchard. American Naturalist 130, 70–82.CrossRefGoogle Scholar
Crow, J. F. & Simmons, M. J. (1983). The mutation load in Drosophila. In The Genetics and Biology of Drosophila, vol. 3c (ed. Carson, H. L.Ashburner, M. and Thomson, J. N.), pp. 1–35. London: Academic Press.Google 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
Gowen, J. W. & Gay, E. H. (1983). Gene number, size and kind in Drosophila. Genetics 18, 1–31.CrossRefGoogle Scholar
Hartl, D. L.Ajioka, J. W.Cai, H.Lohe, A. R.Lozovskaya, E. R.Smoller, D. A. & Duncan, I. W. (1992). Towards a Drosophila genome map. Trends in Genetics 8, 70–75.CrossRefGoogle ScholarPubMed
Hochman, B. (1976). The fourth chromosome of Drosophila melanogaster. In The Genetics and Biology of Drosophila, vol. 1b (ed. Ashburner, M. and Novitski, E.), pp. 903–928. London: Academic Press.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, 31–41.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. 31–36. London: Academic Press.Google Scholar
Lindsley, D. L. & Grell, E. H. (1968). Genetic Variations of Drosophila melanogaster. Washington: Carnegie Institution.Google Scholar
Lindsley, D. L. & Zimm, G. (1992). The Genome of Drosophila melanogaster. San Diego: Academic Press.Google Scholar
Maynard, Smith J. & Haigh, J. (1974). The hitch-hiking effect of a favourable gene. Genetical Research 23, 23–35.Google Scholar
Miklos, G. L. G. & Cotsell, J. N. (1990). Chromosome structure at interfaces between major chromosomal types: β-heterochromatin and β-heterochromatin. Bioessays 12, 1–7.CrossRefGoogle ScholarPubMed
Montgomery, E. A. & Langley, C. H. (1983). Transposable elements in IMendelian populations. II. Distribution of three copy a-like elements in a natural population. Genetics 104, 473–483.CrossRefGoogle ScholarPubMed
Montgomery, E. A.Charlesworth, B. & Langley, C. H. (1987). A test for the role of natural selection in the stabilization 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
Mosteller, F. & Tukey, J. W. (1977). Data Analysis and Regression. Reading, Mass.: Addison-Wesley.Google Scholar
Simmons, M. J. & Crow, J. F. (1977). Mutations affecting fitness in Drosophila. Annual Review of Genetics 11, 49–78.CrossRefGoogle ScholarPubMed
Shrimpton, A. E.Montgomery, E. A. & Langley, C. H. (1986). Om mutations in Drosophila ananassae are linked to insertions of a transposable element. Genetics 114, 125–135.CrossRefGoogle ScholarPubMed
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, 237–254.CrossRefGoogle Scholar
Tanda, S.Shrimpton, A. E.Ling-Ling, C.Itayama, H.Matsubayashi, H.Saigo, K.Tobari, Y. N. & Langley, C. H. (1988). Retrovirus-like features and site specific insertions of a transposable element, torn, in Drosophila ananassae. Molecular and General Genetics 214, 405–411.CrossRefGoogle Scholar
Yamamoto, M.-T.Mitchelson, A.Tudor, M.O'Hare, K.Davies, J. A. & Miklos, G. L. G. (1990). Molecular and cytogenetic analysis of the heterochromatin-euchromatin junction region of the Drosophila melanogaster X chromosome. Genetics 125, 821–832.CrossRefGoogle ScholarPubMed