Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-23T00:24:42.508Z Has data issue: false hasContentIssue false
  • English
  • Français

Models of the spread of non-autonomous selfish transposable elements when transposition and fitness are coupled

Published online by Cambridge University Press:  14 April 2009

J. F. Y. Brookfield
J. F. Y. Brookfield
Affiliation:
Department of Genetics, University of Nottingham, Queens Medical Centre, Nottingham NG7 2UH, UK
Rights & Permissions [Opens in a new window]

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.

I investigate models of the spread of transposable elements, such as the Drosophila melanogaster P elements, that can exist in autonomous and non-autonomous forms. Elements which have their major impact on host fitness in the process of transposition can, under certain conditions, come to a stable balance between transposition and selection. This stable balance for autonomous elements can be disrupted by the invasion of further elements, which do not produce a transposase enzyme, and may produce a repressor of transposition. I examine this secondary invasion process, and show that a stable equilibrium copy number for intact elements is neither a necessary nor a sufficient condition for non-autonomous elements to invade. Nevertheless, invasion occurs under a broad range of models and conditions. This requires neither that the non-autonomous elements produce a trans-acting repressor of transposition, nor that they titrate transposase. The elimination of autonomous elements follows the increase in non-autonomous elements unless the latter encode powerful repressors of transposition. Approximate solutions for the equilibrium copy number of autonomous elements and rate of invasion of non-autonomous elements can be found under some models for transposition and selection. The predictions of the model are compared with recent empirical studies of the D. melanogaster P system

Type
Research Article
Information
Genetics Research , Volume 67 , Issue 3 , June 1996 , pp. 199 - 209
Copyright
Copyright © Cambridge University Press 1996

References

Anxolabéhère, D., Nouaud, D., Periquet, G., & Tchen, P., (1985). P element distribution of Eurasian populations of Drosophila melanogaster: a genetic and molecular analysis. Proceedings of the National Academy of Sciences of the USA 82, 5418–5422.CrossRefGoogle ScholarPubMed
Anxolabéhère, D., Charles-Palabost, L., Flueriet, A., & Periquet, G., (1987). Temporal surveys of French populations of Drosophila melanogaster: P—M system, enzymatic polymorphism and infection by the sigma virus. Heredity 61, 121–131.CrossRefGoogle Scholar
Anxolabéhère, D., Kidwell, M. G., & Periquet, G., (1988). Molecular characteristics of diverse populations are consistent with the hypothesis of recent invasion of Drosophila melanogaster by mobile P elements. Molecular Biology and Evolution 5, 252–269.Google ScholarPubMed
Bangham, C. R. M., & Kirkwood, T. B. L., (1990). Defective interfering particles: effects in modulating viral growth and persistence. Virology 179, 821–826.CrossRefGoogle ScholarPubMed
Biémont, C., Lemeunier, F., Guerriero, M. P. Garcia, Brookfield, J. F., Gautier, C., Aulard, S., & Pasyukova, E. G., (1994). Population dynamics of the copia, mdg1, mdg3, gypsy and P transposable elements in a natural population of Drosophila melanogaster. Genetical Research 63, 197–212.CrossRefGoogle Scholar
Black, D. M., Jackson, M. S., Kidwell, M. G., & Dover, G. A., (1987). KP elements repress P induced hybrid dysgenesis in D. melanogaster. EMBO Journal 6, 4125–4135.CrossRefGoogle Scholar
Brookfield, J. F. Y., (1991). Models of repression of transposition in P-M hybrid dysgenesis by P cytotype and by zygotically encoded repressor proteins. Genetics 128, 471–486.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 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
Engels, W. R., (1989). P elements in Drosophila. In Mobile DNA (ed. Berg, D., & Howe, M.). Washington, DC: ASM Publications.Google Scholar
Engels, W. R., Benz, W. K., Preston, C. R., Graham, P. L., Phillis, R. W., & Robertson, H. M., (1987). Somatic effects of P element activity in Drosophila melanogaster: pupal lethality. Genetics 117, 745–757.CrossRefGoogle ScholarPubMed
Federoff, N. V., (1989). Maize transposable elements. In Mobile DNA (ed. Berg, D., & Howe, M.). Washington, DC: ASM Publications.Google Scholar
Gierl, A., Saedler, H., & Peterson, P. A., (1989). Maize transposable elements. Annual Review of Genetics 23, 71–85.CrossRefGoogle ScholarPubMed
Gloor, G. B., Nassif, N. A., Johnson-Schlitz, D. M., Preston, C. R., & Engels, W. R., (1991). Targeted gene replacement in Drosophila via P element-induced gap repair. Science 253, 1110–1117.CrossRefGoogle ScholarPubMed
Gloor, G. B., Preston, C. R., Johnson-Schlitz, D. M., Nassif, N. A., Phillis, R. W., Benz, W. K., Robertson, H. M., & Engels, W. R., (1993). Type I repressors of P element mobility. Genetics 135, 81–95.CrossRefGoogle ScholarPubMed
Heath, E., & Simmons, M., (1991). Genetic and molecular analysis of repression in the P-M system of hybrid dysgenesis in Drosophila melanogaster. Genetical Research 57, 213–226.CrossRefGoogle Scholar
Hickey, D. A., (1982). Selfish DNA: a sexually transmitted nuclear parasite. Genetics 101, 519–531.CrossRefGoogle ScholarPubMed
Jackson, M. S., Black, D. M., & Dover, G. A., (1988). Amplification of KP elements associated with the repression of hybrid dysgenesis in Drosophila melanogaster. Genetics 120, 1003–1013.CrossRefGoogle ScholarPubMed
Kaplan, N., Darden, T., & Langley, C. H., (1985). Evolution and extinction of transposable elements in Mendelian populations. Genetics 109, 459–480.CrossRefGoogle ScholarPubMed
Kaufman, P. D., & Rio, D. C., (1991). Drosophila P-element transposase is a transcriptional repressor in vitro. Proceedings of the National Academy of Sciences of the USA 88, 2613–2617.CrossRefGoogle ScholarPubMed
Kidwell, M. G., (1985). Hybrid dysgenesis in Drosophila melanogaster: nature and inheritance of P element regulation. Genetics 111, 337–350.CrossRefGoogle ScholarPubMed
Laski, F. A., Rio, D. C., & Rubin, G. M., (1986). Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing. Cell 44, 7–19.CrossRefGoogle ScholarPubMed
Lemaitre, B., & Coen, D., (1991). P regulatory products repress in vivo the P promoter activity in P-lacZ fusion genes. Proceedings of the National Academy of Sciences of the USA 88, 4419–4423.CrossRefGoogle Scholar
Misra, S., & Rio, D. C., (1990). Cytotype control of Drosophila P element transposition: the 66 kD protein is a repressor of transposase activity. Cell 62, 269–284.CrossRefGoogle ScholarPubMed
Nassif, N., Penney, J., Pal, S.E., igels, W. R., & Gloor, G. B., (1994). Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair. Molecular and Cellular Biology 14, 1613–1625.Google ScholarPubMed
Nitasaka, E., Mukai, T., & Yamazaki, T., (1987). Repressor of P elements in Drosophila melanogaster: cytotype determination by a defective P element with only open reading frames 0 through 2. Proceedings of the National Academy of Sciences of the USA 84, 7605–7608.CrossRefGoogle Scholar
Preston, C., & Engels, W. R., (1989). Spread of P transposable elements in inbred lines of Drosophila melanogaster. Progress in Nucleic Acids Research and Molecular Biology 36, 71–85.CrossRefGoogle ScholarPubMed
Raymond, J. D., Ojala, T. A., White, J., & Simmons, M., (1991). Inheritance of P-element regulation in Drosophila melanogaster. Genetical Research 57, 227–234.CrossRefGoogle ScholarPubMed
Rio, D. C., (1990). Molecular mechanisms regulating Drosophila P element transposition. Annual Review of Genetics 24, 543–578.CrossRefGoogle ScholarPubMed
Robertson, H. M., & Engels, W. R., (1989). Modified P elements that mimic the P cytotype in Drosophila melanogaster. Genetics 123, 815–824.CrossRefGoogle Scholar
Ronsseray, S., Lehmann, M., & Periquet, G., (1989). Comparison of the regulation of P elements in M and M′ strains of Drosophila melanogaster. Genetical Research 54, 13–21.CrossRefGoogle Scholar
Ronsseray, S., Lehmann, M., & Anxolabéhère, 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
Szathmary, E., (1992). Natural selection and coexistence of defective and complementing virus segments. Journal of Theoretical Biology 157, 383–406.CrossRefGoogle ScholarPubMed