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Hybrid dysgenesis-induced response to selection in Drosophila melanogaster

Published online by Cambridge University Press:  14 April 2009

Patricia M. Pignatelli  and
Trudy F. C. Mackay
Patricia M. Pignatelli
Affiliation:
Institute of Animal Genetics, West Mains Road, Edinburgh EH9 3JN, Scotland
Trudy F. C. Mackay*
Affiliation:
Institute of Animal Genetics, West Mains Road, Edinburgh EH9 3JN, Scotland
*
* Corresponding author. Department of Genetics, Box 7614, North Carolina State University, Raleigh, North Carolina 27695-7614, USA.
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In Drosophila melanogaster, the P−M and I−R systems of hybrid dysgenesis are associated with high rates of transposition of P and I elements, respectively, in the germlines of dysgenic hybrids formed by crossing females of strains without active elements to males of strains containing them. Transposition rates are not markedly accelerated in the reciprocal, nondysgenic hybrids. Previous attempts to evaluate the extent to which hybrid dysgenesis-mediated P transposition contributes to mutational variance for quantitative characters by comparing the responses to selection of P−M dysgenic and nondysgenic hybrids have given variable results. This experimental design has been extended to include an additional quantitative trait and the I−R hybrid dysgenesis system. The selection responses of lines founded from both dysgenic and nondysgenic crosses showed features that would be expected from the increase in frequency of initially rare genes with major effects on the selected traits. These results differ from those of previous experiments which showed additional selection response only in lines started from dysgenic crosses, and can be explained by the occasional occurrence of large effect transposable element-induced polygenic mutations in both dysgenic and nondysgenic selection lines. High rates of transposition in populations founded from nondysgenic crosses may account for the apparently contradictory results of the earlier selection experiments, and an explanation is proposed for its occurrence.

Type
Research Article
Information
Genetics Research , Volume 54 , Issue 3 , December 1989 , pp. 183 - 195
Copyright
Copyright © Cambridge University Press 1989

References

Anxolabéhère, D., Benes, H., Nouaud, D. & Periquet, G. (1987). Evolutionary steps and transposable elements in Drosophila melanogaster: the missing RP type obtained by genetic transformation. Evolution 41, 846–853.Google ScholarPubMed
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
Black, D. M., Jackson, M. S., Kidwell, M. G. & Dover, G. A. (1987). KP elements repress P-induced hybrid dysgenesis in D. melanogaster. European Molecular Biology Organization Journal 6, 4125–4135.CrossRefGoogle Scholar
Blackman, R. K., Grimaila, R., Koehler, M. M. & Gelbart, W. M. (1987). Mobilization of hobo elements residing within the decapentaplegic gene complex: suggestion of a new hybrid dysgenesis system in Drosophila melanogaster. Cell 49, 497–505.CrossRefGoogle ScholarPubMed
Boussy, I. A., Healy, M. J., Oakeshott, J. G. & Kidwell, M. G. (1988). Molecular analysis of the P−M gonadal dysgenesis cline in eastern Australian Drosophila melanogaster. Genetics 119, 889–902.CrossRefGoogle Scholar
Bregliano, J. C. & Kidwell, M. G. (1983). Hybrid dysgenesis determinants. In Mobile Genetic Elements ed. Shapiro, J. A.), pp. 363–410. New York: Academic Press.Google Scholar
Bucheton, A., Paro, R., Sang, H. M., Pelisson, A. & Finnegan, D. J. (1984). The molecular basis I−R hybrid dysgenesis in Drosophila melanogaster: identification, cloning, and properties of the I factor. Cell 38, 153–163.CrossRefGoogle ScholarPubMed
Bucheton, A. & Picard, G. (1978). Non-Mendelian female sterility in Drosophila melanogaster: hereditary transmission of reactivity levels. Heredity 40, 207–223.CrossRefGoogle Scholar
Chia, W., Howes, G., Martin, M., Meng, Y., Moses, K. & Tsubota, S. (1986). Molecular analysis of the yellow locus in Drosophila. European Molecular Biology Organization Journal 13, 3597–3605.CrossRefGoogle Scholar
Daniels, S. B., Clark, S. H., Kidwell, M. G. & Chovnik, A. (1987). Genetic transformation of Drosophila melanogaster with an autonomous P element: phenotypic and molecular analyses of long-established transformed lines. Genetics 115, 711–723.CrossRefGoogle ScholarPubMed
Engels, W. R. (1979). Hybrid dysgenesis in Drosophila melanogaster: Rules of inheritance of female sterility. Genetical Research 33, 219–236.CrossRefGoogle Scholar
Engels, W. R. (1988). P elements in Drosophila. In Mobile DNA, (ed. Berg, D. E. and Howe, M. M.). In press.Google Scholar
Falconer, D. S. (1981). Introduction to Quantitive Genetics. London and New York: Longman.Google Scholar
Finnegan, D. J. (1985). Transposable elements in eukaryotes. International Review of Cytology 93, 281–326.CrossRefGoogle ScholarPubMed
Finnegan, D. J. & Fawcett, D. H. (1986). Transposable elements in Drosophila melanogaster. Oxford Surveys on Eukaryotic Genes 3, 1–62.Google ScholarPubMed
Fitzpatrick, B. J. & Sved, J. A. (1986). High levels of fitness modifiers induced by hybrid dysgenesis in Drosophila melanogaster. Genetical Research 48, 89–94.CrossRefGoogle Scholar
Frankham, R. & Nurthen, R. K. (1981). Forging links between population and quantitative genetics. Theoretical and Applied Genetics 59, 251–263.CrossRefGoogle ScholarPubMed
Hill, W. G. (1977). Variation in response to selection. In Proceedings of the International Conference in Quantitative Genetics, (ed. Pollack, E., Kempthorne, O. and Bailey, T. B.), pp. 343–365. Ames, Iowa: Iowa State University Press.Google Scholar
Karess, R. E. & Rubin, G. M. (1984). Analysis of P transposable element functions in Drosophila. Cell 38, 135–146.CrossRefGoogle ScholarPubMed
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
Kidwell, M. G. (1986). P−M mutagenesis. In Drosophila – A Practical Approach, (ed. Roberts, D. B.) pp. 59–81, Oxford: IRL Press.Google 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.CrossRefGoogle ScholarPubMed
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
Kidwell, M. G. & Sang, H. M. (1986). Hybrid dysgenesis in Drosophila melanogaster: synthesis of RP strains by chromosomal contamination. Genetical Research 47, 181–185.CrossRefGoogle ScholarPubMed
Kiyasu, P. K. & Kidwell, M. G. (1984). Hybrid dysgenesis in Drosophila melanogaster: the evolution of mixed P and M populations maintained at high temperature. Genetical Research 44, 251–259.CrossRefGoogle Scholar
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
Mackay, T. F. C. (1984). Jumping genes meet abdominal bristles: hybrid dysgenesis-induced quantitative variation in Drosophila melanogaster. Genetical Research 44, 231–237.CrossRefGoogle Scholar
Mackay, T. F. C. (1985). Transposable element-induced response to artificial selection in Drosophila melanogaster. Genetics 111, 351–374.CrossRefGoogle ScholarPubMed
Mackay, T. F. C. (1986). Transposable element-induced fitness mutations in Drosphila melanogaster. Genetical Research 48, 77–87.CrossRefGoogle Scholar
Mackay, T. F. C. (1987). Transposable element-induced polygenic mutations in Drosophila melanogaster. Genetical Research 49, 225–233.CrossRefGoogle Scholar
Mackay, T. F. C. (1988). Transposable element-induced quantitative genetic variation in Drosophila. In Proceedings of the Second International Congress in Quantitative Genetics (ed. Weir, B. S., Eisen, E. J., Goodman, M. M. and Namkoong, G.), pp. 219–235. Sunderland, Massachusetts: Sinauer.Google Scholar
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 Acadamy of Sciences USA 80, 1678–1682.CrossRefGoogle ScholarPubMed
Montgomery, E., 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. & 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
Morton, R. A. & Hall, S. C. (1985). Response of dysgenic and nondysgenic populations to malathion exposure. Drosophila Information Service 61, 126–128.Google Scholar
Mount, S. M., Green, M. M. & Rubin, G. M. (1988). Partial revertants of the transposable element-associated suppressible allele white-apricot in Drosophila melanogaster: structures and responsiveness to genetic modifiers. Genetics 118, 221–234.CrossRefGoogle ScholarPubMed
Nitasaka, E., Mukai, T. & Yamazaki, T. (1987). Repressor of P elements in Drosophila melanogaster: cytotype determination by a defective P element carrying only open reading frames 0 through 2. Proceedings of the National Academy of Sciences USA 84, 7605–7608.CrossRefGoogle Scholar
O'Hare, K. & Rubin, G. M. (1983). Structure of P transposable elements of Drosophila melanogaster and their sites of insertion and excision. Cell 34, 25–35.CrossRefGoogle ScholarPubMed
Picard, G. (1976). Non-Mendelian female sterility in Drosophila melanogaster: hereditary transmission of I factor. Genetics 83, 107–123.CrossRefGoogle ScholarPubMed
Rio, D. C., Laski, F. A. & Rubin, G. M. (1986). Identification and immunochemical analysis of biologically active Drosophila P-element transposase. Cell 44, 21–32.CrossRefGoogle ScholarPubMed
Robertson, H. M., Preston, C. R., Phillis, R. W., Johnson-Schlitz, D. M., Benz, W. K. & Engels, W. R. (1988). A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118, 461–470.CrossRefGoogle ScholarPubMed
Ronsseray, S. & Anxolabéhère, D. (1986). Chromosomal distribution of P and I transposable elements in a natural population of Drosophila melanogaster. Chromosoma 94, 433–40.CrossRefGoogle Scholar
Rubin, G. M. (1983). Dispersed repetitive DNA's in Drosophila. In Mobile Genetic Elements (ed. Shapiro, J. A.), pp. 329–361. New York: Academic Press.Google Scholar
Sakoyama, Y., Todo, T., Chigusa, S. I., Honjo, T. & Kondo, S. (1985). Structures of defective P transposable elements prevalent in natural Q and Q-derived M strains of Drosophila melanogaster. Proceedings of the National Academy of Sciences USA 82, 6236–6239.CrossRefGoogle ScholarPubMed
Shapiro, J. A. & Cordell, B. (1982). Eukaryotic mobile and repeated genetic elements. Biology of the Cell 43, 31–54.Google Scholar
Simmons, M. J. & Bucholz, L. M. (1985). Transposase titration in Drosophila Melanogaster: a model for cytotype in the P−M system of hybrid dysgenesis. Proceedings of the National Academy of Sciences USA 82, 8119–8123.CrossRefGoogle Scholar
Sved, J. A. (1987). Hybrid dysgenesis in Drosophila melanogaster: evidence from sterility and Southern hybridization that P cytotype is not maintained in the absence of chromosomal P factors. Genetics 115, 121–127.CrossRefGoogle Scholar
Todo, T., Sakoyama, Y., Chigusa, S. I., Fukunaga, A., Honjo, T. & Kondo, S. (1984). Polymorphism in distribution and structure of P elements in natural populations of Drosophila melanogaster in and around Japan. Japanese Journal of Genetics 59, 441–451.Google Scholar
Torkamanzehi, A., Moran, C. & Nicholas, F. W. (1988). P-element-induced mutation and quantitative variation in Drosophila melanogaster: lack of enhanced response to selection in lines derived from dysgenic crosses. Genetical Research 51, 231–238.CrossRefGoogle Scholar
Tsubota, S. & Schedl, P. (1986). Hybrid dysgenesis-induced revertants of insertions at the 5′ end of the rudimentary gene in Drosophila melanogaster: Transposon-induced control mutations. Genetics 114, 165–182.CrossRefGoogle ScholarPubMed
Yannopoulos, G., Stamatis, N., Monastirioti, M., Hatzopoulos, P. & Louis, C. (1987). hobo is responsible for the induction of hybrid dysgenesis by strains of Drosophila melanogaster bearing the male recombination factor 23.5 MRF. Cell 49, 487–495.CrossRefGoogle Scholar
Yukuhiro, K., Harada, K. & Mukai, T. (1985). Viability mutations induced by the P elements in Drosophila melanogaster. Japanese Journal of Genetics 60, 531–537.Google Scholar