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Perturbation of gene frequencies in a natural population of Drosophila melanogaster: evidence for selection at the Adh locus

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Abstract

The cellar population of Drosophila melanogaster at the Chateau Tahbilk Winery (Victoria, Australia) was perturbed for alcohol dehydrogenase (Adh) gene frequencies. Phenol oxidase (Phox) frequencies were also perturbed and monitored as a control. Subsequent gene frequency changes, together with information on population structure, indicated that selection acted on the chromosome regions of both loci. Adh gene frequencies returned to preperturbation levels in a predictable manner. A model in which the relative fitness of Adh phenotypes was determined by temperature-dependent specific activities of enzymes of Adh genotypes adequately accounts for the rate of gene frequency change at this locus. Thus temperature behaves as a selective agent in modulating Adh gene frequencies in this cellar environment.

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References

  • Alahiotis, S. N., 1982. Adaptation of Drosophila enzymes to temperature IV. Natural selection at the alcohol dehydrogenase locus. Genetica 59: 81–87.

    Google Scholar 

  • Asada, N., K., Fujimoto, M., Tanaka & E., Ohnishi, 1993. Genetic polymorphism of prophenoloxidase A1 in Drosophila melanogaster. Jap. J. Genetics 68: 219–227.

    Google Scholar 

  • Barker, J. S. F. & P. D., East, 1980. Evidence for selection following perturbation of allozyme frequencies in a natural population of Drosophila. Nature 284: 166–168.

    Google Scholar 

  • Batterham, P., 1980. The biology of a phenol oxidase polymorphism in Drosophila melanogaster. Ph.D. Thesis, Monash University.

  • Batterham, P., 1981. A phenol oxidase polymorphism in Drosophila melanogaster: population studies, pp. 185–200 in Genetic Studies of Drosophila Populations, edited by J. B., Gibson & J. G., Oakeshott, Australian National University Press, Canberra.

    Google Scholar 

  • Batterham, P. & S. W., McKechnie, 1980. A phenol oxidase polymorphism in Drosophila melanogaster. Genetica 54: 121–125.

    Google Scholar 

  • Berry, A. & M., Kreitman, 1993. Molecular analysis of an allozyme cline: alcohol dehydrogenase in Drosophila melanogaster on the east coast of North America. Genetics 134: 869–893.

    Google Scholar 

  • Briscoe, D. A., A., Robertson & J., Malpica, 1975. Dominance at Adh locus in response of adult Drosophila melanogaster to environmental alcohol. Nature 255: 148–149.

    Google Scholar 

  • Cavener, D. R. & M. T., Clegg, 1981. Multigenic response to ethanol in Drosophila melanogaster. Evolution 35: 1–10.

    Google Scholar 

  • Clarke, B., 1975. The combination of ecological genetics to evolutionary theory: Detecting the direct effects of natural selection on particular polymorphic loci. Genetics 79: 101–113.

    Google Scholar 

  • Daly, K. & B., Clarke, 1981. Selection associated with the alcohol dehydrogenase locus in Drosophila melanogaster: Differential survival of adults maintained on low concentrations of ethanol. Heredity 46: 219–226.

    Google Scholar 

  • David, J. R., 1977. Signification d'un polymorphisme enzymatique: la deshydrogenase alcoolique chez Drosophila melanogaster. Annce Biol. 16: 451–472.

    Google Scholar 

  • Day, T. H., P. C., Hillier & B., Clarke, 1974. Properties of genetically polymorphic isozymes of alcohol dehydrogenase in Drosophila melanogaster. Biochem. Genet. 11: 141–153.

    Google Scholar 

  • Franklin, I. R., 1981. An analysis of temporal variation at isozyme loci in Drosophila melanogaster, pp. 217–236 in Genetic Studies of Drosophila Populations, edited by J. B., Gibson and J. G., Oakeshott, Australian National University Press, Canberra.

    Google Scholar 

  • Geer, B. W., P. W., Heinstra & S. W., McKechnie, 1993. The biological basis of ethanol tolerance in Drosophila. Comp. Biochem. Physiol. 105B: 203–229.

    Google Scholar 

  • Gibson, J. B., 1970. Ehzyme flexibility in Drosophila melanogaster. Nature 227: 959–960.

    Google Scholar 

  • Gibson, J. B., T. W., May & A. V., Wilks, 1981. Genetic variation at the alcohol dehydrogenase locus in Drosophila melanogaster in relation to environmental variation: Ethanol levels in breeding sites and allozyme frequencies. Oecologia (Berl) 51: 191–198.

    Google Scholar 

  • Gibson, J. B., A. V., Wilks & G. K., Chambers, 1982. Genetic variation and the aleohol dehydrogenase locus in Drosophila melanogaster: A third ubiquitous allele. Experientia 38: 653–654.

    Google Scholar 

  • Gilbert, D. G. & R. C., Richmond, 1982. Studies of esterase 6 in Drosophila melanogaster XII. Evidence for temperature selection of Est 6 and Adh alleles. Genetica 68: 109–119.

    Google Scholar 

  • Gionfriddo, M. A., C. L., Vigue & P. A., Weisgram, 1979. Seasonal variation in the frequencies of alcohol dehydrogenase isoalleles of Drosophila: correlation with environmental factors. Genet. Res. 34: 317–319.

    Google Scholar 

  • Hartl, D. L. & A. G., Clark, 1989. Principles of population genetics, Second Edition, Sinauer Associates Inc., Sunderland, Massachusetts.

    Google Scholar 

  • Hickey, D. A. & M. D., McLean, 1980. Selection for ethanol tolerance and alcohol dehydrogenase allozymes in natural populations of Drosophila melanogaster. Genet. Res. 36: 11–15.

    Google Scholar 

  • Hoffman, A. A. & S. W., McKechnie, 1991. Heritable variation in resource utilization and resource response in a winery population of Drosophila melanogaster. Evolution 45: 1000–1015.

    Google Scholar 

  • Johnson, F. M. & A., Powell, 1974. The alcohol dehydrogenase of Drosophila melanogaster: frequency changes associated with heat and cold shock. Proc. Natl. Acad. Sci. USA 71: 1783–1784.

    Google Scholar 

  • Jones, J. S., S. H., Bryant, R. C., Lewontin, J. A., Moore & T., Prout, 1981. Gene flow and the geographical distribution of a molecular polymorphism in Drosophila pseudoobscura. Genetics 98: 157–178.

    Google Scholar 

  • Jones, J. S. & D. T., Parkin, 1977. Attempts to measure natural selection by altering gene frequencies in natural populations, pp. 83–96 in Measuring Selection in Natural Populations. Lecture Notes in Biomathematics 19, edited by F. B., Christiansen & T., Fenchel, Springer, Berlin.

    Google Scholar 

  • Kreitman, M. & M., Aguade, 1986. Excess polymorphism at the Adh locus of Drosophila melanogaster. Genetics 114: 93–110.

    Google Scholar 

  • Kreitman, M. & R. H., Hudson, 1991. Inferring the evolutionary histories of the Adh and Adh-dup loci in Drosophila melanogaster from patterns of polymorphism and divergence. Genetics 127: 565–582.

    Google Scholar 

  • Laurie-Ahlberg, C. C. & L. F., Stam, 1987. Use of P-elementmediated transformation to identify the basis of naturally occurring variants affecting ADH expression in Drosophila melanogaster. Genetics 115: 129–140.

    Google Scholar 

  • Laurie, C. C., J. T., Bridgham & M., Choudhary, 1991. Associations between DNA sequence variation and variation in expression of the Adh gene in natural populations of Drosophila melanogaster. Genetics 129: 489–499.

    Google Scholar 

  • Lewis, N. & J. B., Gibson, 1978. Variation in the amount of enzyme protein in natural populations. Biochem. Genet. 16: 159–170.

    Google Scholar 

  • Lewontin, R. C., 1991. Twenty five years ago in GENETICS: electrophoresis in the development of evolutionary genetics: milestone or millstone? Genetics 128: 657–662.

    Google Scholar 

  • Malpica, J. M. & J. N., Vassallo, 1980. A test for the selective origin of environmentally correlated allozyme patterns. Nature 286: 497–498.

    Google Scholar 

  • Marks, R. W., J. G., Brittnacher, J. F., McDonald, T., Prout & F. J., Ayala, 1980. Wineries, Drosophila, alcohol and Adh. Oecologia (Berl) 47: 141–144.

    Google Scholar 

  • Matthew, P., A., Agrotis, A. C., Taylor & S. W., McKechnie, 1992. An association between ADH protein levels and polymorphic nucleotide variation in the Adh gene of Drosophila melanogaster. Mol. Biol. Evol. 9: 124–127.

    Google Scholar 

  • McKechnie, S. W. & B. W., Geer, 1993. Micro-evolution in a wine cellar population: an historical perspective. Genetica 90: 201–215.

    Google Scholar 

  • McKechnie, S. W. & J. A., McKenzie, 1983. Polymorphism of alcohol dehydrogenase (Adh) in a winery cellar population of Drosophila melanogaster: Gene frequency association with temperature and genotypic differences in progeny production. Evolution 37: 850–853.

    Google Scholar 

  • McKechnie, S. W. & P., Morgan, 1982. Alcohol dehydrogenase polymorphism of Drosophila melanogaster: Aspects of alcohol and temperature variation in the larval environment. Aust. J. Biol. Sci. 35: 85–93.

    Google Scholar 

  • McKenzie, J. A., 1974. The distribution of vineyard populations of Drosophila melanogaster and Drosophila simulans during vintage and non-vintage periods. Oecologia (Berl) 15: 1–16.

    Google Scholar 

  • McKenzie, J. A., 1975a. Gene flow and selection in a natural population of Drosophila melanogaster. Genetics 80: 349–361.

    Google Scholar 

  • McKenzie, J. A., 1975b. The influence of low temperature on survival and reproduction in populations of Drosophila melanogaster. Aust. J. Zool. 23: 237–247.

    Google Scholar 

  • McKenzie, J. A., 1980. An ecological study of the alcohol dehydrogenase (Adh) polymorphism of Drosophila melanogaster. Aust. J. Zool. 28: 709–716.

    Google Scholar 

  • McKenzie, J. A. & S. W., McKechnie, 1978. Ethanol tolerance and the Adh polymorphism in a natural population of Drosophila melanogaster. Nature 272: 75–76.

    Google Scholar 

  • McKenzie, J. A. & S. W., McKechnie, 1981. The alcohol dehydrogenase polymorphism in a vineyard cellar population of Drosophila melanogaster, pp. 201–215 in Genetic Studies of Drosophila Populations, edited by J. B., Gibson and J. G., Oakeshott. Australian National University, Canberra.

    Google Scholar 

  • McKenzie, J. A. & P. A., Parsons, 1972. Atcohol tolerance: An ecological parameter in the relafive success of Drosophila melanogaster and Drosophila simulans. Oecologia (Berl) 10: 373–388.

    Google Scholar 

  • McKenzie, J. A. & P. A., Parsons, 1974. Microdifferentiation in a natural population of Drosophila melanogaster to alcohol in the environment. Genetics 77: 385–394.

    Google Scholar 

  • Morgan, P. D., 1975. Selection acting directly on an enzyme polymorphism. Heredity 35: 124–127.

    Google Scholar 

  • Oakeshott, J. G., 1976. Selection at the alcohol dehydrogenase locus in Drosophila melanogaster imposed by environmental ethanol. Genet. Res. 26: 265–274.

    Google Scholar 

  • Oakeshott, J. G., J. B., Gibson, P. R., Anderson, W. R., Knibb, D. G., Anderson & G. K., Chambers, 1982. Alcohol dehydrogenase and glycerol-3-phosphate dehydrogenase clines in Drosophila melanogaster in different continents. Evolution 36: 86–96.

    Google Scholar 

  • Pipkin, S. B., C., Rhodes & N., Williams, 1973. Influence of temperature on Drosophila alcohol dehydrogenase polymorphism. J. Hered. 64: 181–185.

    Google Scholar 

  • Sampsell, B. & S., Sims, 1982. Effect of Adh genotype and heat stress on alcohol tolerance in Drosophila melanogaster. Nature 296: 853–855.

    Google Scholar 

  • Van, Delden, W., 1982. The alcohol dehydrogenase polymorphism in Drosophila melanogaster. Selection at an enzyme locus. Evol. Biol. 15: 187–222.

    Google Scholar 

  • Van, Delden, W., A. C., Boerema & A., Kamping, 1978. The alcohol dehydrogenase polymorphism in populations of Drosophila melanogaster. 1. Selection in different environments. Genetics 90: 161–191.

    Google Scholar 

  • Van, Delden, W. & A., Kamping, 1980. The alcohol dehydrogenase polymorphism in populations of Drosophila melanogaster. IV. Survival at high temperature. Genetica 51: 179–185.

    Google Scholar 

  • Vigue, C. L. & F. M., Johnson, 1973. Isozyme variability in species of the genes Drosophila. VI. Frequency-property-environment relationship of allelic alcohol dehydrogenase in Drosophila melanogaster. Biochem. Genet. 9: 213–227.

    Google Scholar 

  • Vigue, C. L., P. A., Weisgram & E., Rosenthal, 1982. Selection at the alcohol dehydrogenase locus of Drosophila melanogaster: effects of ethanol and temperature. Biochem. Genet. 20: 681–688.

    Google Scholar 

  • Vouidibio, J., P., Capy, D., Defaye, E., Pla, J., Sandrin, A., Cesink & J. R., David, 1989. Short-range genetic structure of Drosophila melanogaster populations in Afrotropical urban area and its significance. Proc. Nat. Acad. Sci. U.S.A. 86: 8442–8446.

    Google Scholar 

  • Ziolo, L. K. & P. A., Parsons, 1982. Ethanol tolerance, alcoholdehydrogenase activity and Adh allozymes in Drosophila melanogaster. Genetica 57: 231–237.

    Google Scholar 

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Authors and Affiliations

  1. Department of Genetics, The University of Methourne, 3052, Parkville, Victoria, Australia

    John A. McKenzie & Philip Batterham

  2. Department of Genetics, Monash University, 3168, Clayton, Victoria, Australia

    Stephen W. McKechnie

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  1. John A. McKenzie
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McKenzie, J.A., McKechnie, S.W. & Batterham, P. Perturbation of gene frequencies in a natural population of Drosophila melanogaster: evidence for selection at the Adh locus. Genetica 92, 187–196 (1994). https://doi.org/10.1007/BF00132537

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  • DOI: https://doi.org/10.1007/BF00132537

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