Abstract
As an initial study of the influence of transposable DNA elements on life history traits, and as a model system for estimating the impact of somatic genetic damage on longevity, the effect of P DNA element movement in somatic cells on adult lifespan was measured in Drosophila melanogaster males. Lifespan was significantly reduced in males that contained the somatically active P[ry+ Δ2–3](99B) element and 17, 4, 3, but not just a single P element. Furthermore, there appears to be a direct correlation between the number of transposing P elements and the amount of lifespan reduction. This reduction in lifespan observed in males with somatically active P elements is probably due to genetic damage in embryos, larvae and pupae from P-element excisions and insertions, leading to changes in gene structure and regulation, chromosome breakage, and subsequent cell death in adults. This hypothesis is supported in this study by a significant increase in recessive sex-linked lethal mutations in the same males that had reduced lifespans and by the previous observation of chromosome breakage in somatic cells of similar males. The evolutionary implications of these results are discussed, including the possible influence of somatic DNA transpositions on fitness and other life history traits.
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References
Abrahamson, S., H. U. Meyer, E. Himoe & G. Daniel, 1966. Further evidence demonstrating germinal selection in early permeiotic germ cells of Drosophila males. Genetics 54: 687–697.
Ajioka, J. W. & D. L. Hartl, 1989. Population dynamics of transposable elements. pp. 939–958 in Mobile DNA, edited by D. E. Berg and M. M. Howe. American Society for Microbiology, Washington, D.C.
Arking, R. & S. P. Dudas, 1989. Review of genetic investigations into the aging processes of Drosophila. J. Amer. Geriatrics Soc. 37: 757–773.
Ashburner, M., 1989. Drosophila: A Laboratory Handbook, Cold Spring Harbor Laboratory, Cold Spring Harbor.
Auerbach, C, 1976. Mutation Research. Chapman and Hall, London.
Berg, D. E. & M. M. Howe, 1989. Mobile DNA. American Society of Microbiology Publication, Washington, D.C.
Blackman, R. K. & W. M. Gelbart, 1989. The transposable element hobo of Drosophila melanogaster, pp. 523–529 in Mobile DNA, edited by D. E. Berg and M. M. Howe. American Society of Microbiology Publication, Washington, D.C.
Brosius, J., 1991. Retroposons-seeds of evolution. Science 753.
Carson, H. L., 1990. Increased genetic variance after a population bottleneck. TREE 5: 228–230.
Charlesworth, B. & C. H. Langley, 1991. Population genetics of transposable elements in Drosophila, pp. 150–176 in Evolution at the Molecular Level, edited by R. K. Selander, A. G. Clark and T. S. Whittam. Sinauer Associates Inc., Sunderland, Massachusetts.
Corces, V. G. & P. K. Geyer, 1991. Interactions of retrotransposons with the host genome — The case of the gypsy element of Drosophila. Trends Genet. 7: 86–90.
Crow, J. F., 1984. The P factor: A transposable element in Drosophila, pp.257–273 in Mutation, Cancer and Malformation, edited by E. H. Y. Chu and W. M. Generoso. Plenum, New York.
Davis, P. S., M. W. Shen & B. H. Judd. 1987. Asymmetrical pairings of transposons in and proximal to the white locus of Drosophila account for four classes of regularly occurring exchange products. Proc. Natl. Acad. Sci. USA 84: 174–
Engels, W. R., 1989. P elements in Drosophila melanogaster, pp. 437–484 in Mobile DNA, edited by D. E. Berg and M. M. Howe. American Society of Microbiology Publication, Washington, D.C.
Engels, W. R., W. K. Benz, C. R. Preston, P. L. Graham, R. W. Phillis & H. M. Robertson, 1987. Somatic effects of P element activity in Drosophila melanogaster. pupal lethality. Genetics 117: 745–757.
Finch, C. E., 1990. Longevity, Senescence, and the Genome. The University of Chicago Press, Chicago.
Finnegan, D. J. & D. H. Fawcett, 1986. Transposable elements in Drosophila melanogaster in Oxford Survey Eukaryotic. Genes 3: 1–62.
Frankham, R., A. Torkamanzehi & C. Moran, 1991. P-element transposon-induced quantitative genetic variation for inebriation time in Drosophila melanogaster. Theor. Appl. Genet. 81: 317–320.
Ganetzky, B. & J. R. Flanagan. 1978. On the relationship between senescence and age-related changes in two wild-type strains of Drosophila melanogaster. Exp. Geront. 13: 189–196.
Georgiev, P. G., S. L. Kiselev, O. B. Simonova & T. I. Gerasimova, 1990. A novel transposition system in Drosophila melanogaster depending on the Stalker mobile genetic element. EMBO J. 9: 2037–2044.
Green, M. M., 1988. Mobile DNA elements and spontaneous gene mutation, pp. 41–50 in Eukaryotic Transposable Elements as Mutagenic Agents, edited by M. E. Lambert, J. F. McDonald and I. B. Weinstein. Cold Spring Harbor Laboratory, Cold Spring Harbor.
Grigliatti, T., M. Richter & I. Whitebread, 1990. Mutations in Drosophila that act in the larval stage and influence larval or adult longevity, pp. 153–176 in Genetic Effects on Aging II, edited by D. E. Harrison. The Telford Press, Inc., Caldwell, New Jersey.
Gunn, J. S., R. C. Woodruff & R. L. Ludwiczak, 1989. The effect of temperature on the movement of P DNA elements in somatic tissues of Drosophila melanogaster. Mutation Res. 226: 267–272.
Hartl, D. L., 1989. Transposable Element mariner in Drosophila Species, pp. 531–536 in Mobile DNA, edited by D. E. Berg and M. M. Howe. American Society for Microbiology, Washington, D.C.
Henderson, S. A., R. C. Woodruff & J. N. Thompson Jr., 1978. Spontaneous chromosome breakage at male meiosis associated with male recombination in Drosophila melanogaster. Genetics 88: 93–107.
Itoh, M., M. Iwabuchi, K. Yoshida & S. H. Hori, 1989. Four tandem defective P-elements associated with positive regulation of the Drosophila melanogaster glucose-6-phosphate dehydrogenase gene. Biochemical Genetics 27: 699–718.
Johnson, T. E., 1990. Caenorhabditis elegans offers the potential for molecular dissection of the aging process, pp. 45–59 in Handbook of The Biology of Aging, edited by E. L. Schneider and J. W. Rowe. Academic Press, Inc., New York.
Jungen, H. & D. L. Hartl, 1979. Average fitness and populations of Drosophila melanogaster as estimated using compoundautosome strains. Evolution 33: 359–370.
Kidwell, M. G., 1984. Hybrid dysgenesis in Drosophila melanogaster: partial sterility associated with embryo lethality in the P-M system. Genetical Research, Cambridge 44: 11–28.
Kidwell, M. G., J. Kidwell & J. Sved, 1977. Hybrid dysgenesis in Drosophila melanogaster: A syndrome of aberrant traits Including mutation, sterility and male recombination. Genetics 86: 813–833.
Kim, A. I. & E. S. Belyaeva, 1991a. Direct demonstration of the transposition of mobile element MDG4 in the sex and somatic cells of the unstable mutator line of Drosophila melanogaster. Doklady Biological Sciences 314: 595–598.
Kim, A. I. & E. S. Belyaeva, 1991b. Transpositions of mobile elements gypsy (mdg 4) and hobo in germ-line and somatic cells of a genetically unstable mutator strain of Drosophila melanogaster. Mol. Gen. Genet. 229: 437–444.
Kirkwood, T. B. L., 1988. DNA mutations and aging. Mutations Res. 7–13.
Lamb, M. J., 1988. Radiation, pp. 71–84 in Drosophila as a Model Organism for Aging Studies, edited by F. A. Lints and M. H. Soliman. Blackie and Son, Glasgow.
Lambert, M. E., J. F. McDonald & I. B. Weinstein, 1988. Eukaryotic Transposable Elements as Mutagenic Agents. Cold Spring Harbor Press, Cold Spring Harbor, New York.
Laski, F. A., D. C. Rio & G. M. Rubin, 1986. Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing. Cell 44: 7–19.
Levis, R., T. Hazelrigg & G. M. Rubin, 1985. Effects of genomic position on the expression of transduced copies of the white gene of Drosophila. Science 229: 558–561.
Lindsley, D. L. & E. H. Grell, 1968. Genetic Variations of Drosophila melanogaster. Carnegie Institution of Washington, Washington, D.C.
Lints, F. A. & M. H. Soliman, 1988. Drosophila as a Model Organism for Aging Studies. Blackie and Sons, Ltd., Glasgow.
Louis, C. & G. Yannopoulos, 1989. The transposable elements involved in hybrid dysgenesis in Drosophila melanogaster, pp. 205–250 in Oxford Surveys of Eukaryotic Genes, edited by N. MacLean. Oxford University Press, Oxford.
Mackay, T. F. C, 1989. Mutation and origin of quantitative Variation, pp. 113–119 in Evolution and Animal Breeding, edited by W. G. Hill and T. F. C. Mackay. CAB International, Wallingford, UK.
Mackay, T. F. C. & C. H. Langley, 1990. Molecular and phenotypic Variation in the achaete-scute region of Drosophila melanogaster. Nature 348: 64–66.
Mackay, W. J., W. C. Orr & G. C. Bewley, 1989. Genetic and molecular analysis of antioxidant enzymes in Drosophila melanogaster — A correlation between catalase activity levels, life span, and spontaneous mutation rate, in Molecular Biology of Aging, UCLA Symposia on Molecular and Cellular Biology, New Series, edited by M. Clegg and S. O'Brien. 123: 157–170.
Margolin, B. H., B. J. Collings & J. M. Mason, 1983. Statistical analysis and sample-size determination for mutagenicity experiments with binomial responses. Environ. Mutagen. 5: 705–716.
Mayer, P. J. & G. T. Baker, 1985. Genetic aspects of Drosophila as a model system of eukaryotic aging, pp. 61–102 in International Review of Cytology, edited by G. H. Bourne and J. F. Danielli. Academic Press, Inc., New York.
McClintock, B., 1984. The significance of responses of the genome to challenge. Science 226: 792–801.
McDonald, J., 1990. Macroevolution and retroviral elements. BioScience 40: 183–191.
Mode, C. J., R. D. Ashleigh, A. Zawodniak & G. T. Baker, 1984. On Statistical tests of significance in studies of survivorship in laboratory animals. J. Gerontol. 39: 36–42.
Moerman, D. G. & R. H. Waterston, 1989. Mobile Elements in Caenorhabditis elegans and Other Nematodes, pp. 537–556 in Mobile DNA, edited by D. E. Berg and M. M. Howe. American Society for Microbiology, Washington, D. C.
Montgomery, E. A., S.-M. Huang, C. H. Langley & B. H. Judd, 1991. Chromosome rearrangements by ectopic recombination in Drosophila melanogaster: Genome structure and evolution. Genetics 129: 1085–1098.
Murray, V, 1990. Hypotesis: Are transposons a cause of aging? Mutation Res. 237: 59–63.
Nei, M., 1987. Molecular Evolutionary Genetics. Columbia University Press, New York.
Osiewacz, H. D., 1990. Molecular analysis of aging processes in fungi. Mutation Res. 237: 1–8.
Pasyukova, E. G., E. Sp. Belyaeva, G. L. Kogan, L. Z. Kaidanov & V. A. Gvozdev, 1986. Concerted transpositions of mobile genetic elements coupled with fitness changes in Drosophila melanogaster. Mol. Biol. Evol. 3: 299–312.
Phillips, J. P., S. D. Campbell, D. Michaud, M. Charbonneau & A. J. Hilliker, 1989. Null mutation of copper/zinc Superoxide dismutase in Drosophila confers hypersensitivity to paraquat and reduced longevity. Proc. Natl. Acad. Sci. USA 86: 2761–2765.
Polivanov, S., 1969. Genetic loads and fitness of populations: I. The effects of the gene Stubble on fitness of experimental populations of Drosophila melanogaster. Genetics 63: 933–948.
Rio, D. C, 1990. Molecular mechanisms regulating Drosophila P element transposition, in Annual Review of Genetics 24: 543–578 edited by J. G. Sandalios. Annual Review Inc., New York.
Robertson, H. M., C. R. Preston, R. W. Phillips, D. M. Johnson-Schlitz, W. K. Benz & W. R. Engels, 1988. A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118: 461–470.
Roiha, H., G. M. Rubin & K. O'Hare, 1988. P element insertions and rearrangements at the singed locus of Drosophila melanogaster. Genetics 119: 75–83.
Rose, M. R., 1990. Evolutionary genetics of aging in Drosophila, pp. 41–54 in Genetic Effects on Ageing II, edited by D. E. Harrison. The Telford Press, Inc. Caldwell, New Jersey.
Rubin, G. M., 1983. Dispersed repetitive DNA's in Drosophila, pp. 329–361 in Mobile Genetic Elements, edited by J. A. Shapiro. Academic Press, New York.
Sankaranarayanan, K., 1988. Mobile genetic elements, spontaneous mutations, and the assessment of genetic radiation hazards in man, pp. 319–336 in Eukaryotic Transposable Elements as Mutagenic Agents, edited by M. E. Lambert, J. F. McDonald and I. B. Weinstein. Cold Spring Harbor Laboratory, Cold Spring Harbor.
Seperack, P. K., M. C. Strobel, D. J. Corrow, N. A. Jenkins & N. G. Copeland, 1988. Somatic and germ-line reverse mutation rates of the retrovirus-induced dilute coat-color mutation of DBA mice. Proc. Natl. Acad. Sci. USA 85: 189–192.
Servomaa, K. & T. Rytomma. 1988. Suicidal death of rat chloroleukeamia cells by activation of the long interspersed repetitive DNA element (LIRn). Cell Tissue Kinet. 21: 33–43.
Shaw, D. D., P. Wilkinson & D. J. Coates, 1983. Increased chromosomal mutation rate after hybridization between two subspecies of grasshoppers. Science 220: 1165–1167.
Sokal, R. R. & F. J. Rohlf, 1981. Biometry. W. H. Freeman and Company, San Francisco.
Sved, J. A., L. M. Blackman, A. S. Gilchrist & W. R. Engels, 1991. High levels of recombination induced by homologous P-elements in Drosophila melanogaster. Mol. Gen. Genet. 225: 443–447.
Sved, J. A., W. B. Eggleston & W. R. Engels, 1990. Germ-line and somatic recombination induced by in vitro modified P-elements in Drosophila melanogaster. Genetics 124: 331–337.
Syvanen, M., 1984. The evolutionary implications of mobile genetic elements, in Annual Review of Genetics edited by H. L. Roman, A. Campbell and L. M. Sandier. 18: 271–293.
Thompson, J. N., Jr. & R. C. Woodruff, 1980. Increased mutation in crosses between geographically separated strains of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 77: 1059–1062.
Thompson, J. N., Jr., R. C. Woodruff & G. B. Schaefer, 1978. An assay of somatic recombination in male recombination lines of Drosophila melanogaster. Genetica 49: 77–80.
Tsubota, S. & P. Schedl. 1986. Hybrid dysgenesis-induced revertrants of insertions at the 5' end of the rudimentary gene in Drosophila melanogaster: Transposon-induced control mutations. Genetics 114: 165–182.
Venugopal, S., S. N. Guzder & W. A. Deutsch. 1990. Apurinic endonuclease activity from wild-type and repair-deficient mei-9 Drosophila ovaries. Mol. Gen. Genet. 221: 421–426.
Voelker, R. A., A. L. Greenleaf, H. Gyrukovics, G. B. Wisely, S. Huang & L. L. Searles, 1984. Frequent imprecise excision among reversions of a P element-caused lethal mutation in Drosophila. Genetics 107: 279–294.
Woodruff, R. C, J. M. Mason, R. Valencia & S. Zimmering, 1985. Chemical mutagenesis testing in Drosophila. V. Results of 53 coded compounds tested for the National Toxicology Program. Environ. Mutagen. 7: 677–702.
Woodruff, R. C, J. N. Thompson Jr. & R. F. Lyman, 1979. Intraspecific hybridization and the release of mutator activity. Nature 278: 277–279.
Wurgler, F. E., F. H. Sobéis & E. Vogel, 1984. Drosophila as an assay system for detecting genetic changes, pp. 555–601 in Handbook of Mutagenicity Test Procedures, edited by B. J. Kilbey, M. Legator, W. Nichols and C. Ramel. Elsevier Science Publishers, Amsterdam.
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Woodruff, R.C. (1993). Transposable DNA elements and life history traits. In: McDonald, J.F. (eds) Transposable Elements and Evolution. Contemporary Issues in Genetics and Evolution, vol 1. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-2028-9_16
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DOI: https://doi.org/10.1007/978-94-011-2028-9_16
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