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The population dynamics of transposable elements

Published online by Cambridge University Press:  14 April 2009

Brian Charlesworth  and
Deborah Charlesworth
Brian Charlesworth
Affiliation:
School of Biological Sciences, University of Sussex, Brighton BN1 9QG
Deborah Charlesworth
Affiliation:
School of Biological Sciences, University of Sussex, Brighton BN1 9QG
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Summary

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This paper describes analytical and simulation models of the population dynamics of transposable elements in randomly mating populations. The models assume a finite number of chromosomal sites that are occupable by members of a given family of elements. Element frequencies can change as a result of replicative transposition, loss of elements from occupied sites, selection on copy number per individual, and genetic drift. It is shown that, in an infinite population, an equilibrium can be set up such that not all sites in all individuals are occupied, allowing variation between individuals in both copy number and identity of occupied sites, as has been observed for several element families in Drosophila melanogaster. Such an equilibrium requires either regulation of transposition rate in response to copy number per genome, a sufficiently strongly downwardly curved dependence of individual fitness on copy number, or both. The probability distributions of element frequencies, generated by the effects of finite population size, are derived on the assumption of independence between different loci, and compared with simulation results. Despite some discrepancies due to violation of the independence assumption, the general pattern seen in the simulations agrees quite well with theory.

Data from Drosophila population studies are compared with the theoretical models, and methods of estimating the relevant parameters are discussed.

Type
Research Article
Information
Genetics Research , Volume 42 , Issue 1 , August 1983 , pp. 1 - 27
Copyright
Copyright © Cambridge University Press 1983

References

REFERENCES

Ananiev, E. V., Gvozdev, V. A., Ilyin, Y. V., Tchurikov, N. A. & Georgiev, G. P. (1978). Reiterated genes with varying location in intercalary heterochromatin regions of Drosophila mdanogaster. Chromosoma 70, 1–17.CrossRefGoogle Scholar
Barrett, J. A. (1982). Junk DNA and the ‘parasite paradigm’: neo-Darwinism revisited. (Unpublished MS.)Google Scholar
Bingham, P. M., Kidwell, M. G. & Rubin, G. M. (1982). The molecular basis of P-M hybrid dysgenesis: the role of the P element, a P-strain-specific transposon family. Cell 29, 995–1004.CrossRefGoogle Scholar
Brookfield, J. F. Y. (1982). Interspersed repetitive DNA sequences are unlikely to be parasitic. Journal of Theoretical Biology 94, 281–299.CrossRefGoogle ScholarPubMed
Brookfield, J. F. Y. (1983). A simple analytical model for the spread of independent transposable elements of equal effect. Journal of Theoretical Biology (submitted).Google Scholar
Bulmer, M. G. (1980). The Mathematical Theory of Quantitative Genetics. Oxford: Oxford University Press.Google Scholar
Charlesworth, B. (1983). Recombination, genome size and chromosome number. In DNA and Evolution: Natural Selection and Genome Size (ed. Cavalier-Smith, T.). Chichester: Wiley. (In press.)Google Scholar
Crow, J. F. & Kimura, M. (1970). An Introduction to Population Genetics Theory. New York: Harper & Row.Google Scholar
Doolittle, W. F. (1982). Selfish DNA after fourteen months. In Genome Evolution (ed. Dover, G. A. and Flavell, R. B.), pp. 3–28. London: Systematics Association and Academic Press.Google Scholar
Doolittle, W. F. & Sapienza, C. (1980). Selfish genes, the phenotype paradigm and genome evolution. Nature. 272, 123–124.Google Scholar
Dover, G. A. (1982). Molecular drive: a cohesive mode of species evolution. Nature 299, 111–117.Google Scholar
Engels, W. R. (1981). Hybrid dysgenesis in Drosophila and the stochastic loss hypothesis. Cold Spring Harbor Symposium on Quantitative Biology 45, 561–566.CrossRefGoogle ScholarPubMed
Ewens, W. J. (1979). Mathematical Population Genetics. Berlin: Springer-Verlag.Google Scholar
Felsenstein, J. (1976). The theoretical population genetics of variable selection and migration. Annual Review of Genetics 10, 253–280.CrossRefGoogle ScholarPubMed
Finnegan, D. J., Will, B. H., Bayev, A. A., Bowcock, A. M. & Brown, L. (1982). Transposable DNA sequences in eukaryotes. In Genome Evolution (ed. Dover, G. A. and Flavell, R. B.), pp. 29–40. London: Systematics Association and Academic Press.Google Scholar
Franklin, I. & Lewontin, R. C. (1970). Is the gene the unit of selection? Genetics 65, 701–734.CrossRefGoogle ScholarPubMed
Green, M. M. (1980). Transposable genetic elements in Drosophila and other Diptera. Annual Review of Genetics 14, 109–120.Google Scholar
Haldane, J. B. S. (1937). The effect of variation on fitness. American Naturalist 71, 337–349.Google Scholar
Hickey, D. A. (1982). Selfish DNA: a sexually-transmitted nuclear parasite. Genetics 101, 519–531.CrossRefGoogle ScholarPubMed
Hill, W. G. (1976). Non-random associations of neutral linked genes in finite populations. In Population Genetics and Ecology (eds Karlin, S. and Nevo, E.), pp. 339–376. New York: Academic Press.Google Scholar
Ilyin, Y., Chmeliauskaite, V., Ananiev, E. V. & Georgiev, G. P. (1980). Isolation and characterisation of a new family of mobile dispersed genetic elements, mdg3, in Drosophila melanogaster. Chromosoma 81, 27–53.CrossRefGoogle ScholarPubMed
Ising, G. & Block, K. (1981). Derivation-dependent distribution of insertion sites for a Drosophila transposon. Cold Spring Harbor Symposium on Quantitative Biology 45, 527–544.CrossRefGoogle ScholarPubMed
Kaplan, N. L. & Brookfield, J. F. Y. (1983 a). Transposable elements in Mendelian populations. III. Statistical results. Genetics. (In the Press.)CrossRefGoogle Scholar
Kaplan, N. L. & Brookfield, J. F. Y. (1983 b). The effect on homozygosity of selective differences between sites of transposable elements. Theoretical Population Biology. (In the Press.)CrossRefGoogle Scholar
Kidwell, M. G., Kidwell, J. F. & Sved, J. A. (1977). Hybrid dysgenesis in Drosophila melanogaster: a syndrome of aberrant traits including mutation, sterility and male recombination. Genetics 86, 813–833.Google Scholar
Kidwell, M. G., Novy, J. B. & Feeley, S. M. (1981). Rapid unidirectional change of hybrid dysgenesis potential in Drosophila. Journal of Heredity 72, 32–38.CrossRefGoogle ScholarPubMed
Kimura, M. & Ohta, T. (1971). Theoretical Aspects of Population Genetics. Princeton: Princeton University Press.Google Scholar
Kitts, P. A., Lamond, A. & Sherratt, D. J. (1982). Inter-replicon transposition of Tn1/3 occurs in two sequential genetically separable steps. Nature 295, 626–628.CrossRefGoogle ScholarPubMed
Kleckner, N. (1981). Transposable elements in prokaryotes. Annual Review of Genetics 15, 341–404.CrossRefGoogle ScholarPubMed
Langley, C. H. & Montgomery, E. A. (1983). Transposable elements in Mendelian populations. II. Distribution of three copia-like elements in a natural population of Drosophila melanogaster. Genetics. (In the Press.)Google Scholar
Langley, C. H., Brookfield, J. F. Y. & Kaplan, N. L. (1983). Transposable elements in Mendelian populations. I. A theory. Genetics. (In the Press).Google Scholar
Lewontin, R. C. (1974). The Genetic Basis of Evolutionary Change. New York: Columbia University Press.Google Scholar
Lewontin, R. C. & Prout, T. (1956). Estimation of the number of different classes in a population. Biometrics 12, 211–223.CrossRefGoogle Scholar
McClintock, B. (1956). Controlling elements and the gene. Cold Spring Harbor Symposium on Quantitative Biology 21, 197–216.CrossRefGoogle ScholarPubMed
Ohta, T. (1981). Population genetics of selfish DNA. Nature 292, 648–649.Google Scholar
Ohta, T. (1983). Theoretical study on the accumulation of selfish DNA. Genetical Research. 41, 1–16.Google Scholar
Ohta, T. & Kimura, M. (1981). Some calculations on the amount of selfish DNA. Proceedings of the National Academy of Sciences, USA 78, 1129–1132.CrossRefGoogle ScholarPubMed
Orgel, L. E. & Crick, F. H. C. (1980). Selfish DNA: the ultimate parasite. Nature 284, 606–607.CrossRefGoogle ScholarPubMed
Pierce, D. A. & Lucchesi, J. C. (1981). Analysis of a dispersed repetitive DNA sequence in isogenic lines of Drosophila. Chromosoma 82, 471–492.CrossRefGoogle ScholarPubMed
Potter, S., Brorein, W. J., Dunsmuir, P. & Rubin, G. M. (1979). Transposition of elements of the 412, copia, and 297 dispersed repeated gene families in Drosophila. Cell 17, 415–427.Google Scholar
Rasmuson, R., Westerberg, B. M., Rasmuson, A., Gvozdev, V. A., Belyaeva, E. S. & Ilyin, Y. V. (1981). Transposition, mutable genes, and the dispersed gene family Dm225 in Drosophila melanogaster. Cold Spring Habor Symposium on Quantitative Biology 45, 545–551.CrossRefGoogle ScholarPubMed
Reed, R. R., Shibuya, G. I. & Steitz, J. A. (1982). Nucleotide sequence of γδ resolvase gene and demonstration that its gene product acts as a represser of transcription. Nature 300, 381–383.CrossRefGoogle Scholar
Rubin, G. M., Kidwell, M. G. & Bingham, P. M. (1982). The molecular nature of P-M hybrid dysgenesis: the nature of induced mutations. Cell 29, 987–994.Google Scholar
Simmons, M. J. & Crow, J. F. (1977). Mutations affecting fitness in Drosophila populations. Annual Review of Genetics 11, 49–78.Google Scholar
Strobel, E., Dunsmuir, P. & Rubin, G. M. (1979). Polymorphisms 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., Lyobomirskaya, N. V. & Georgiev, S. P. (1981). General properties of mobile dispersed genetic elements in Drosophila melanogaster. Cold Spring Harbor Symposium on Quantitative Biology 45, 655–671.CrossRefGoogle ScholarPubMed
Young, M. W. (1979). Middle repetitive DNA: a fluid component of the Drosophila genome. Proceedings of the National Academy of Sciences, U.S.A. 76, 6274–6278.Google Scholar