Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-21T16:00:32.040Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparative population structuring of molecular and allozyme variation of Drosophila melanogaster Adh between Europe, West Africa and East Africa

Published online by Cambridge University Press:  14 April 2009

Véronique Bénassi  and
Michel Veuille
Véronique Bénassi
Affiliation:
Institut d'Ecologie, Université Paris VI, 7 quai Saint Bernard, 75252 Paris Cedex 5, France
Michel Veuille*
Affiliation:
Institut d'Ecologie, Université Paris VI, 7 quai Saint Bernard, 75252 Paris Cedex 5, France
*
* Corresponding author
Rights & Permissions [Opens in a new window]

Summary

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Restriction enzyme molecular variation in Drosophila melanogaster Adh was compared between three natural populations from Europe, West Africa and East Africa. The frequency distribution of silent variation in the slow allele was compatible with the neutral model in all three samples. The number of haplotypes in East Africa was significantly higher than in the other two populations. The largest divergence, as measured by Fst, was between the East African population and a group made up from the West African, the European, and previously studied American populations. We suggest that a split first occurred within African populations at least 44000 years ago. European populations separated from West Africa more recently, between the last glacial maximum and the post-glacial optimum, 18000 to 8000 years ago. We suggest that this species was domesticated recently relative to human evolution, possibly with the advent of agriculture. Population differentiation with respect to the two allozymes, fast and slow, does not follow the geographical pattern of silent variation. It opposes European to both African populations, and probably results from selection for adaptation to alcohol in recent temperate populations.

Type
Research Article
Information
Genetics Research , Volume 65 , Issue 2 , April 1995 , pp. 95 - 103
Copyright
Copyright © Cambridge University Press 1995

References

Adams, J. M., Faure, H., Faure-Denard, L., McGlade, J. M., & Woodward, F. I., (1990). Increase in terrestrial carbon storage from the last glacial maximum to the present. Nature 348, 711–714.CrossRefGoogle Scholar
Aguadé, M. (1988). Restriction map variation at the Adh locus of D. melanogaster in inverted and non-inverted chromosomes. Genetics 119, 135–140.CrossRefGoogle Scholar
Ashburner, M., (1989). Drosophila, a Laboratory Handbook. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.Google Scholar
Ashburner, M., Bodmer, M., & Lemeunier, F., (1984). On the evolutionary relationships of Drosophila melanogaster. Developmental Genetics 4, 295–312.CrossRefGoogle Scholar
Begun, D. J., & Aquadro, C. F., (1991). Molecular population genetics of the distal portion of the X chromosome in Drosophila: evidence for genetic hitchhiking for the yellow-achaete region. Genetics 129, 1147–1158.CrossRefGoogle ScholarPubMed
Begun, D. J., & Aquadro, C. F., (1993). African and North American populations of Drosophila melanogaster are very different at the DNA level. Nature 365, 548–550.CrossRefGoogle ScholarPubMed
Begun, D. J., & Aquadro, C. F., (1994 a). Evolutionary inferences from DNA variation at the 6-phosphogluconate dehydrogenase locus in natural populations of Drosophila: selection and geographic differentiation. Genetics 136, 155–171.CrossRefGoogle ScholarPubMed
Begun, D. J., & Aquadro, C. F., (1994 b). Regional variation in fruitflies. Nature 369, 449.CrossRefGoogle Scholar
Bénassi, V., Aulard, S., Mazeau, S., & Veuille, M., (1993). Molecular variation of Adh and P6 genes in African populations of Drosophila melanogaster and its relation to chromosomal inversions. Genetics 134, 789–799.CrossRefGoogle ScholarPubMed
Benyajati, C., Spoerel, N., Haymerle, H., & Ashburner, M., (1983). The messenger RNA for alcohol dehydrogenase in Drosophila melanogaster differs in its 5′ end in different developmental stages. Cell 33, 125–133.CrossRefGoogle ScholarPubMed
Berry, A., & Kreitman, M., (1993). Molecular analysis of an allozyme cline: alcohol dehydrogenase in Drosophila melanogaster on the East coast of North America. Genetics 134, 869–893.CrossRefGoogle ScholarPubMed
Branchu, P., Haure, H., Ambrosi, J.-P., van Zinderen Bakker, E. M., & Faure-Denard, L., (1993). Africa as source and sink for atmospheric carbon dioxide. Global and Planetary Change 7, 41–49.CrossRefGoogle Scholar
Can, R. L., Stoneking, M., & Wilson, A. C., (1987). Mitochondrial DNA and human evolution. Nature 325, 31–36.CrossRefGoogle Scholar
Cavalli-Sforza, L. L., Pizza, A., Menozzi, P., & Mountain, J., (1988). Reconstruction of human evolution: bringing together genetic, archeological, and linguistic data. Proceedings of the National Academy of Sciences, USA 85, 6002–6006.CrossRefGoogle Scholar
Chambers, G. K., (1988). The Drosophila alcohol dehydrogenase gene-enzyme system. Advances in Genetics 25, 39–107.CrossRefGoogle Scholar
Charlesworth, B., Morgan, M. T., & Charlesworth, D., (1993). The effect of deleterious mutations on neutral molecular variation. Genetics 134, 1289–1303.CrossRefGoogle ScholarPubMed
Collet, C., (1988). Recent origin of a thermostable alcohol dehydrogenase allele of Drosophila melanogaster. Journal of Molecular Evolution 27, 142–146.CrossRefGoogle ScholarPubMed
David, J., (1988). Ethanol adaptation and alcohol dehydrogenase polymorphism in Drosophila: from phenotypic functions to genetic structures. In Population Genetics and Evolution (ed. de Jong, G.), pp. 163–172. Berlin, Heidelberg: Springer-Verlag.CrossRefGoogle Scholar
Dobzhansky, Th., (1965). ‘Wild’ and ‘domestic’ species of Drosophila. In The Genetics of Colonizing Species (ed. Baker, H. G., and Stebbins, G. Ledyard), pp. 533–546. New York and London: Academic PressGoogle Scholar
Eanes, W. F., Ajioka, J. W., Hey, J., & Wesley, C., (1989). Restriction map variation associated with the G6PD polymorphism in natural populations of Drosophila melanogaster. Molecular Biology and Evolution 6, 384–397.Google ScholarPubMed
Eanes, W. F., Kirchner, M., & Yoon, J., (1993). Evidence for adaptive evolution of the G6pd gene in Drosophila melanogaster and Drosophila simulans lineages. Proceedings of the National Academy of Sciences, USA 90, 7475–7479.CrossRefGoogle ScholarPubMed
Eisses, K. T., Andriesse, A. J., de Beer, A. Douwe, Thorig, G. E. W., & Weisbeek, P. J., (1990). Analysis of the gene encoding the multifunctional alcohol dehydrogenase alozyme ADH-71K of Drosophila melanogaster. Molecular Biology and Evolution 7, 459–469.Google Scholar
Gibson, J. G., Reed, D., Wilks, A. V., & Jiang, C., (1990). Molecular similarity of Drosophila melanogaster thermostable alleles from populations on different continents. Heredity 65, 1–6.CrossRefGoogle ScholarPubMed
Hale, L. R., & Singh, R. S., (1991). A comprehensive study of genie variations in natural populations of Drosophila melanogaster. IV. Mitochondrial DNA variation and the role of history vs. selection in the genetic structure of geographic populations. Genetics 129, 103–117.CrossRefGoogle Scholar
Hey, J., & Kliman, R. M., (1993). Population genetics and phylogenetics of DNA sequence variation at multiple loci within the Drosophila melanogaster species complex. Molecular Biology and Evolution 10, 804–822.Google ScholarPubMed
Hudson, R. R., (1982). Estimating genetic variability with restriction endonucleases. Genetics 100, 711–719.CrossRefGoogle ScholarPubMed
Hudson, R. R., (1987). Estimating the recombination parameter of a finite population model without selection. Genetical Research 50, 245–250.CrossRefGoogle ScholarPubMed
Hudson, R. R., Kreitman, M., & Aguadé, M., (1987). A test of neutral molecular evolution based on nucleotide data. Genetics 116, 153–159.CrossRefGoogle ScholarPubMed
Hudson, R. R., Slatkin, M., & Maddison, W. P., (1992). Estimation of levels of gene flow from DNA sequence data. Genetics 132, 583–589.CrossRefGoogle ScholarPubMed
Jiang, J. C., & Gibson, J. B., (1992 a). The alcohol dehydrogenase polymorphism in natural populations of Drosophila melanogaster: restriction map variation in the region of the Adh locus in populations from two hemispheres. Heredity 68, 1–14.CrossRefGoogle ScholarPubMed
Jiang, J. C., & Gibson, J. B., (1992 b). The alcohol dehydrogenase polymorphism in natural populations of Drosophila melanogaster: ADH activity variation, restriction site polymorphism and the Adh cline. Heredity 68, 337–344.CrossRefGoogle ScholarPubMed
Kreitman, M., (1983). Nucleotide polymorphism at the alcohol dehydrogenase gene region of Drosophila melanogaster. Nature 304, 412–417.CrossRefGoogle Scholar
Kreitman, M., & Aguadé, M., (1986 a). Genetic uniformity of two populations of Drosophila melanogaster as revealed by filter hybridization of four-nucleotide restriction enzyme digests. Proceedings of the National Academy of Sciences, USA 83, 3562–3566.CrossRefGoogle ScholarPubMed
Kreitman, M., & Aguadé, M., (1986 b). Excess polymorphism at the Adh locus in Drosophila melanogaster. Genetics 114, 93–110.CrossRefGoogle ScholarPubMed
Kreitman, M., & Hudson, R., (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.CrossRefGoogle ScholarPubMed
Lachaise, D., Cariou, M.-L., David, J. R., Lemeunier, F., & Tsacas, L., (1988). Historical biogeography of the Drosophila melanogaster species subgroup. Evolutionary Biology 22, 159–225.CrossRefGoogle Scholar
Laurie, C. C., Bridgham, J. T., & Choudary, M., (1991). Association between DNA sequence variation and variation in expression of the Adh gene in natural populations of Drosophila melanogaster. Genetics 129, 489–499.CrossRefGoogle ScholarPubMed
Lemeunier, F., & Aulard, S., (1992). Inversion polymorphism in Drosophila melanogaster. In Drosophila Inversion Polymorphism, (ed. Krimbas, C. B., and Powell, J. R.), Cleveland: CRC Press.Google Scholar
Lemeunier, F., Aulard, S., Bénassi, V., & Veuille, M., (1994). Fruitfly origins. Nature 371, 25.CrossRefGoogle ScholarPubMed
Matthews, P., Agrostis, A., Taylor, A. C., & McKechnie, W., (1992). An association between ADH protein levels and polymorphic nucleotide variation in the Adh gene of Drosophila melanogaster. Molecular Biology and Evolution 9, 526–536.Google Scholar
Miller, J. C., (1991). Restsite: a phylogenetic program that sorts raw restriction data. Journal of Heredity 82, 262–263.CrossRefGoogle ScholarPubMed
Nei, M., (1987). Molecular Evolutionary Genetics. New York: Columbia University Press.CrossRefGoogle Scholar
Nei, M., & Miller, J. C., (1990). A simple method for estimating the average number of nucleotide substitutions within and between populations from restriction data. Genetics 125, 873–879.CrossRefGoogle ScholarPubMed
Oakeshott, J. G., Gibson, J. B., Anderson, P. R., Knibb, W. R., Anderson, D. G., & Chambers, G. K., (1982). Alcohol dehydrogenase and Glycerol-3-phosphate dehydrogenase clines in Drosophila melanogaster on different continents. Evolution 36, 86–96.CrossRefGoogle ScholarPubMed
Parsons, P. A., (1975). The comparative evolutionary biology of the sibling species, Drosophila melanogaster and D. simulans. Quarterly Review of Biology 50, 151–169.CrossRefGoogle ScholarPubMed
Ruvolo, M., Zehr, S., Dornum, M. von, Pan, D., Chang, B., & Lin, J., (1993). Mitochondrial COII sequences and modern human origins. Molecular Biology and Evolution 10, 1115–1135.Google ScholarPubMed
Simmons, G. M., Kreitman, M., Quattelbaum, W. F., & Miyashita, N., (1989). Molecular analysis of the alleles of Alcohol dehydrogenase along a cline in D. melanogaster. Evolution 43, 393–409.Google Scholar
Singh, R. S., & Hale, L. R., (1994). Regional variation in fruitflies. Nature 369, 449.CrossRefGoogle ScholarPubMed
Singh, R. S., Hickey, D. A., & David, J., (1982). Genetic differentiation between geographically distant populations of Drosophila melanogaster. Genetics 101, 235–256.CrossRefGoogle ScholarPubMed
Tajima, F., (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.CrossRefGoogle ScholarPubMed
Tamura, K., & Nei, M., (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512–526.Google ScholarPubMed
Teissier, G., (1957). Discriminative biometrical characters in French and Japanese Drosophila melanogaster. Cytologia suppl. Proceedings of the International Genetics Symposia, 1956: 502–505.Google Scholar
Tsacas, L., & Lachaise, D., (1974). Quatre nouvelles espèces de la Côte dTvoire du genre Drosophila, groupe melanogaster et discussion de l'origine du sous-groupe melanogaster (Diptera: Drosophiliidae). annales de I'Universite d'Abidjan E7, 193–211.Google Scholar
Delden, W. van, & Kamping, A., (1989). The association between the polymorphisms at the Adh and alpha-Gpdh loci and the In(2L)t inversion in Drosophila melanogaster in relation to temperature. Evolution 43, 775–793.CrossRefGoogle Scholar
Vigilant, L., Stoneking, M., Harpending, H., Hawkes, K., & Wilson, A. C., (1991). African populations and the evolution of human mitochondrial DNA. Science 253, 1503–1507.CrossRefGoogle ScholarPubMed
Vigue, C. L., & Johnson, F. M., (1973). isozyme variability in species of the genus Drosophila. VI. Frequency—property—environment relationships of allelic alcohol dehydrogenases in D. melanogaster. Biochemical Genetics 9, 213–227.CrossRefGoogle ScholarPubMed
Vouidibio, J., Capy, P., Defaye, D., Pla, E., Sandrin, J., Csink, A., & David, J., (1989). Short-range genetic structure of Drosophila melanogaster populations in an Afrotropical urban area and its significance. Proceedings of the National Academy of Sciences, USA 86, 8442–8446.CrossRefGoogle Scholar
Watterson, G. A., (1975). On the number of segregating sites in genetical models without recombination. Theoretical Population Biology 7, 256–276.CrossRefGoogle ScholarPubMed
Weir, B. S., & Cockerham, C. C., (1984). Estimating Fstatistics for the analysis of population structure. Evolution 38, 1358–1370.Google ScholarPubMed
Wright, S., (1951). The genetical structure of populations. Annals of Eugenics 15, 323–354.CrossRefGoogle ScholarPubMed
Zohary, D., & Hopf, M., (1988). Domestication of Plants in the Old World. Oxford: Clarendon Press.Google Scholar