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Variation in spontaneous mutation and repair in natural population lines of Drosophila melanogaster
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  • Original Article
  • Published: 01 August 1984

Variation in spontaneous mutation and repair in natural population lines of Drosophila melanogaster

  • R C Woodruff1,
  • James N Thompson Jr2,
  • Mark A Seeger1 &
  • …
  • William E Spivey2 

Heredity volume 53, pages 223–234 (1984)Cite this article

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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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References

  • 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.

    Article  PubMed  Google Scholar 

  • Barton, N H, Halliday, R B, and Hewitt, G M. 1983. Rare electrophoretic variants in a hybrid zone. Heredity, 50, 139–146.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • Boyd, J B, and Setlow, R B. 1976. Characterization of post-replication repair in mutagen-sensitive strains of Drosophila melanogaster. Genetics, 84, 507–526.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bregliano, J, and Kidwell, M G. 1983. Hybrid dysgenesis determinants. In Shapiro, J. A. (ed.) Mobile Genetic Elements, Academic Press, New York, 363–410.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Carson, H L. 1975. The genetics of speciation at the diploid level. Amer Nat, 109, 83–92.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Dobzhansky, Th. 1951. Genetics and the Origin of Species. Columbia University Press, New York.

    Google Scholar 

  • Dubinin, N P. 1964. Problems of Radiation Genetics. Oliver and Boyd, London.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gillespie, J H. 1981a. Mutation modification in a random environment. Evolution, 35, 468–476.

    Article  PubMed  Google Scholar 

  • Gillespie, J H. 1981b. Evolution of the mutation rate at a heterotic locus. Proc natl Acad Sci USA, 78, 2452–2454.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Golding, G B, and Strobeck, C. 1983. Increased number of alleles found in hybrid populations due to intragenic recombination. Evolution, 37, 17–29.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • Greenbaum, I F. 1981. Genetic interactions between hybridizing cytotypes of the tent-making bat (Uroderma bilobatum). Evolution, 35, 306–321.

    PubMed  Google Scholar 

  • Hafner, J C. 1982. Genetic interactions at a contact zone of Uroderma bilobatum (Chiroptera: Phyllostomidae). Evolution, 36, 852–862.

    Article  PubMed  Google Scholar 

  • Hunt, W G, and Selander, R K. 1973. Biochemical genetics of hybridization in European house mice. Heredity, 31, 11–33.

    Article  CAS  PubMed  Google Scholar 

  • Ives, P T. 1950. The importance of mutation rate genes in evolution. Evolution, 4, 236–252.

    Article  Google Scholar 

  • Karlin, S, and McGregor, J. 1974. Towards a theory of the evolution of modifier genes. Theor Pop Biol 5, 59–103.

    Article  CAS  Google Scholar 

  • Kilpatrick, C W, and Zimmerman, E G. 1976. Biochemical variation and systematics of Peromyscus pectoralis. J Mamm, 57, 506–522.

    Article  CAS  Google Scholar 

  • Kimura, M. 1967. On the evolutionary adjustment of spontaneous mutation rates. Genet Res, Camb 9, 23–34.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • Leigh, E G, Jr. 1970. Natural selection and mutability. Amer Nat, 104, 301–305.

    Article  Google Scholar 

  • Leigh, E G, Jr. 1973. The evolution of mutation rates. Genetics, 73, 1–18.

    Google Scholar 

  • Levins, R. 1967. Theory of fitness in a heterogeneous environment. VI. The adaptive significance of mutation. Genetics, 56, 163–178.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Maynard Smith, J. 1976. What determines the rate of evolution? Amer Nat, 110, 331–338.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Muller, H J. 1941. Induced mutations in Drosophila. Cold Spring Harbor Symp Quant Biol, 9, 290–308.

    Article  Google Scholar 

  • Neel, J V. 1983. Frequency of spontaneous and induced “point” mutations in higher eukaryotes. The Journal of Heredity, 74, 2–15.

    Article  CAS  PubMed  Google Scholar 

  • Owen, D B. 1962. Handbook of Statistical Tables. Addison-Wesley Publ. Co., Inc., London.

    Google Scholar 

  • Peters, G B. 1982. The recurrence of chromosome fusion in inter-population hybrids of the grasshopper Astractomorphia similis. Chromosoma, 85, 323–347.

    Article  Google Scholar 

  • Plough, H H. 1941. Spontaneous mutability in Drosophila. Cold Spring Harbor Symp Quant Biol, 9, 127–137.

    Article  Google Scholar 

  • Quah, S, Von Borstel, R C, and Hastings, P J. 1980. The origin of spontaneous mutation in Saccharomyces cerevisiae. Genetics, 96, 819–839.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Rubin, G M. 1983. Dispersed repetitive DNAs in Drosophila. In Shapiro, J. A. (ed.) Mobile Genetic Elements, Academic Press, New York, pp. 329–361.

    Google Scholar 

  • Sage, R D, and Selander, R K. 1979. Hybridization between species of the Ranapipiens complex in central Texas. Evolution, 33, 1069–1088.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • Sokal, R R, and Rohlf, F J. 1981. Biometry W. H. Freeman and Co., San Francisco.

    Google Scholar 

  • Sturtevant, A H. 1937. Essays on evolution I. On the effects of selection on mutation rate. Quart. Rev Biol, 12, 464–467.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Thompson, J N, Jr, and Woodruff, R C. 1978. Mutator genes: Pacemakers of evolution. Nature, 274, 317–321.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Williams, G C. 1966. Adaptation and Natural Selection. Princeton University Press. Princeton, N.J.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • Woodruff, R C, Thompson, J N, Jr, and Lyman, R F. 1979. Intraspecific hybridization and the release of mutator activity. Nature, 278, 277–279.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Biological Sciences, Bowling Green State University, Bowling Green, 43403, Ohio

    R C Woodruff & Mark A Seeger

  2. Department of Zoology, University of Oklahoma, Norman, 73019, Oklahoma

    James N Thompson Jr & William E Spivey

Authors
  1. R C Woodruff
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  2. James N Thompson Jr
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  3. Mark A Seeger
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  4. William E Spivey
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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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  • Received: 20 October 1983

  • Issue date: 01 August 1984

  • DOI: https://doi.org/10.1038/hdy.1984.78

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