Summary
To measure the possible correlation between genetic damage and repair ability in natural populations of a eukaryote, we compared the spontaneous frequency of sex-linked recessive lethal mutations and male recombination, which is associated with DNA transposable element induced chromosome breakage, with DNA repair efficiency in isofemale lines of a winery population of Drosophila melanogaster from Australia. Repair efficiency was measured by maternal effects on ring-X chromosome loss. Significant amounts of genetic variability for spontaneous rates of genetic change and for repair ability were observed in the isofemale lines collected during periods of low and high population density. However, there were no correlations between repair ability and rates of genetic damage. Possible reasons for the absence of correlation are discussed, along with the observations that: (a) the frequency of lethal mutations and ring-X chromosome losses were significantly higher in the small, resident population; (b) the rates of ring chromosome losses and especially lethal mutations are uniform over periods of time; (c) and inbreeding of isofemale lines leads to a reduction of the high spontaneous mutation rates.
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Avise, J C, and Smith, M H. 1974. Biochemical genetics of sunfish. I. Geographic variation and subspecific intergradation in the bluegill, Lepomis macrochirus. Evolution, 28, 42–56.
Barton, N H, Halliday, R B, and Hewitt, G M. 1983. Rare electrophoretic variants in a hybrid zone. Heredity, 50, 139–146.
Boyd, J B, and Harris, P V. 1981. Mutants partially defective in excision repair at five autosomal loci in Drosophila melanogaster. Chromosoma, 82, 249–257.
Boyd, J B, Harris, P V, Osgood, C J, and Smith, K E. 1980. Biochemical characterization of repair-deficient mutants of Drosophila. In Generoso, W. M. Shelby, M. D. and de Serres, F. J. (eds.) DNA Repair and Mutagenesis in Eukaryotes, Plenum Press, New York, pp. 209–222.
Boyd, J B, and Setlow, R B. 1976. Characterization of post-replication repair in mutagen-sensitive strains of Drosophila melanogaster. Genetics, 84, 507–526.
Bregliano, J, and Kidwell, M G. 1983. Hybrid dysgenesis determinants. In Shapiro, J. A. (ed.) Mobile Genetic Elements, Academic Press, New York, 363–410.
Brodberg, R K, Lyman, R F, and Woodruff, R C. 1983. The induction of chromosome aberrations by cis-platinum(II)diaminodichloride in Drosophila melanogaster. Environmental Mutagenesis, 5, 285–297.
Carson, H L. 1975. The genetics of speciation at the diploid level. Amer Nat, 109, 83–92.
Cooper, S F, and Zimmering, S. 1981. Genetic study on the effects of the repair-deficient mutant females mei-9a, mei-41D5, mus101D1, mus104D1, and mus302D1 of Drosophila on spontaneous and X-ray-induced chromosome loss in the paternal genome. Mutation Res, 81, 345–356.
Dobzhansky, Th. 1951. Genetics and the Origin of Species. Columbia University Press, New York.
Dubinin, N P. 1964. Problems of Radiation Genetics. Oliver and Boyd, London.
Eeken, J C J, and Sobels, F H. 1981. Modification of MR mutator activity in repair-deficient strains of Drosophila melanogaster. Mutation Res, 83, 191–200.
Eeken, J C J, and Sobels, F H. 1983. The influence of deficiencies in DNA-repair on MR-mediated reversion of an insertion-sequence mutation in Drosophila melanogaster. Mutation Res, 110, 287–295.
Generoso, W M, Cain, K T, Krishna, M, and Huff, S W. 1979. Genetic lesions induced by chemicals in spermatozoa and spermatids of mice are repaired in the egg. Proc Natl Acad Sci USA, 76, 435–437.
Gillespie, J H. 1981a. Mutation modification in a random environment. Evolution, 35, 468–476.
Gillespie, J H. 1981b. Evolution of the mutation rate at a heterotic locus. Proc natl Acad Sci USA, 78, 2452–2454.
Golding, G B, and Strobeck, C. 1983. Increased number of alleles found in hybrid populations due to intragenic recombination. Evolution, 37, 17–29.
Gould, S J, and Woodruff, D S. 1978. Natural history of Cerion VIII: Little Bahama Bank-A revision based on genetics, morphometrics and geographic distribution. Bull Mus Comp Zool, 148, 371–415.
Graf, U, Kagi, A, and Würgler, F E. 1982. Mutagenesis in spermatozoa of Drosophila melanogaster by cross-linking agents depends on the mus(1)101+ gene product in the oocyte. Mutation Res, 95, 237–249.
Green, M M. 1976. Mutable and mutator loci. In Ashburner, M. and Novitski, E. (eds) The Genetics and Biology of Drosophila Vol. 1b, Academic Press, London, pp. 929–946.
Greenbaum, I F. 1981. Genetic interactions between hybridizing cytotypes of the tent-making bat (Uroderma bilobatum). Evolution, 35, 306–321.
Hafner, J C. 1982. Genetic interactions at a contact zone of Uroderma bilobatum (Chiroptera: Phyllostomidae). Evolution, 36, 852–862.
Hunt, W G, and Selander, R K. 1973. Biochemical genetics of hybridization in European house mice. Heredity, 31, 11–33.
Ives, P T. 1950. The importance of mutation rate genes in evolution. Evolution, 4, 236–252.
Karlin, S, and McGregor, J. 1974. Towards a theory of the evolution of modifier genes. Theor Pop Biol 5, 59–103.
Kilpatrick, C W, and Zimmerman, E G. 1976. Biochemical variation and systematics of Peromyscus pectoralis. J Mamm, 57, 506–522.
Kimura, M. 1967. On the evolutionary adjustment of spontaneous mutation rates. Genet Res, Camb 9, 23–34.
Leigh, B. 1976. Ring chromosomes and radiation induced chromosome loss. In Ashburner, M. and Novitski, E. (eds.) The Genetics and Biology of Drosophila, Vol. 1b, Academic Press, London, pp. 505–528.
Leigh, E G, Jr. 1970. Natural selection and mutability. Amer Nat, 104, 301–305.
Leigh, E G, Jr. 1973. The evolution of mutation rates. Genetics, 73, 1–18.
Levins, R. 1967. Theory of fitness in a heterogeneous environment. VI. The adaptive significance of mutation. Genetics, 56, 163–178.
Lindsley, D L, and Grell, E H. 1968. Genetic Variations of Drosophila melanogaster. Carnegie Institution of Washington, publ. 627.
Mason, J M. 1980. Spontaneous mutation frequencies in mutagen-sensitive mutants of Drosophila melanogaster. Mutation Res, 72, 323–326.
Maynard Smith, J. 1976. What determines the rate of evolution? Amer Nat, 110, 331–338.
Moran, C, Wilkinson, P, and Shaw, D D. 1980. Allozyme variation across a narrow hybrid zone in the grasshopper, Caledia captiva. Heredity, 44, 69–81.
Muller, H J. 1941. Induced mutations in Drosophila. Cold Spring Harbor Symp Quant Biol, 9, 290–308.
Neel, J V. 1983. Frequency of spontaneous and induced “point” mutations in higher eukaryotes. The Journal of Heredity, 74, 2–15.
Owen, D B. 1962. Handbook of Statistical Tables. Addison-Wesley Publ. Co., Inc., London.
Peters, G B. 1982. The recurrence of chromosome fusion in inter-population hybrids of the grasshopper Astractomorphia similis. Chromosoma, 85, 323–347.
Plough, H H. 1941. Spontaneous mutability in Drosophila. Cold Spring Harbor Symp Quant Biol, 9, 127–137.
Quah, S, Von Borstel, R C, and Hastings, P J. 1980. The origin of spontaneous mutation in Saccharomyces cerevisiae. Genetics, 96, 819–839.
Racine, R, Beck, A, and Würgler, F E. 1979. The genetic control of maternal effects on mutations recovered from X-rayed mature Drosophila sperm. Mutation Res, 63, 87–100.
Rubin, G M. 1983. Dispersed repetitive DNAs in Drosophila. In Shapiro, J. A. (ed.) Mobile Genetic Elements, Academic Press, New York, pp. 329–361.
Sage, R D, and Selander, R K. 1979. Hybridization between species of the Ranapipiens complex in central Texas. Evolution, 33, 1069–1088.
Shaw, D D, Wilkinson, P, and Coates, D J. 1983. Increased chromosomal mutation rate after hybridization between two subspecies of grasshopper. Science, 220, 1165–1167.
Slatko, B E, Mason, J M, and Woodruff, R C. 1984. The DNA transposition system of hybrid dysgenesis in Drosophila melanogaster can function despite defects in host DNA repair. Genet Res, Camb: in press.
Smith, M F. 1979. Geographic variation in genie and morphological characters in Peromyscus-califomicus. J Mamm, 60, 705–722.
Smith, P D, Snyder, R D, and Dusenbery, R L. 1980. Isolation and characterization of repair-deficient mutants of Drosophila melanogaster. In Generoso, W. M. Shelby, M. D. and de Serres, F. J. (eds.) DNA Repair and Mutagenesis in Eukaryotes, Plenum Press, New York, pp. 175–188.
Sokal, R R, and Rohlf, F J. 1981. Biometry W. H. Freeman and Co., San Francisco.
Sturtevant, A H. 1937. Essays on evolution I. On the effects of selection on mutation rate. Quart. Rev Biol, 12, 464–467.
Szostak, J W, Orr-Weaver, T L, Rothstein, R J, and Stahl, F W. 1983. The double-strand-break repair model for recombination. Cell, 33, 25–35.
Thompson, J N, Jr, and Woodruff, R C. 1978. Mutator genes: Pacemakers of evolution. Nature, 274, 317–321.
Thompson, J N, Jr, and Woodruff, R C. 1980. Increased mutation in crosses between geographically separated strains of Drosophila melanogaster. Proc Natl Acad Sci USA, 77, 1059–1062.
Williams, G C. 1966. Adaptation and Natural Selection. Princeton University Press. Princeton, N.J.
Woodruff, R C, Slatko, B E, and Thompson, J N, Jr. 1983. Factors affecting mutation rates in natural populations. In Ashburner, M. Carson, H. L. and Thompson, J. N., Jr. (eds.) The Genetics of Biology of Drosophila, Vol. 3c, Academic Press, London, pp. 37–124.
Woodruff, R C, and Thompson, J N, Jr. 1982a. Genetic factors that affect rates of spontaneous mutation and chromosome aberrations in Drosophila melanogaster. Cytogenetics and Cell Genetics, 33, 152–159.
Woodruff, R C, and Thompson, J N, Jr. 1982b. Hybrid release of mutator activity in crosses between natural population lines of Drosophila melanogaster. Genetics, 100, s75.
Woodruff, R C, Thompson, J N, Jr, and Lyman, R F. 1979. Intraspecific hybridization and the release of mutator activity. Nature, 278, 277–279.
Würgler, F E, and Graf, U. 1980. Mutation induction in repair-deficient strains of Drosophila. In Generoso, W. M. Shelby, M. D. and de Serres, F. J. (eds.) DNA Repair and Mutagenesis in Eukaryotes, Plenum Press, New York, pp. 223–240.
Würgler, F E, and Graf, U. 1982. Stability of Drosophila melanogaster chromosomes replicating for the first time in a repair-deficient cell. Mutation Res, 92, 99–106.
Würgler, F E, and Maier, P. 1972. Genetic control of mutation induction in Drosophila melanogaster. I. Sex-chromosome loss in X-rayed mature sperm. Mutation Res, 15, 41–53.
Vijayalaxmi, Evans, H J, Ray, J H, and German, J. 1983. Bloom's syndrome: Evidence for an increased mutation frequency in vivo. Science, 221, 851–853.
Zimmering, S. 1981. Review of the current status of the mei-9 test for chromosome loss in Drosophila melanogaster: An assay with radically improved detection capacity for chromosome lesions induced by methyl methanesulfonate (MMS), dimethylnitrosamine (DMN), and especially diethylnitrosamine (DEN) and procarbazine. Mutation Res, 83, 69–80.
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Woodruff, R., Thompson, J., Seeger, M. et al. Variation in spontaneous mutation and repair in natural population lines of Drosophila melanogaster. Heredity 53, 223–234 (1984). https://doi.org/10.1038/hdy.1984.78
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DOI: https://doi.org/10.1038/hdy.1984.78
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