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Genetics of morphological differences and hybrid sterility between Drosophila sechellia and its relatives

Published online by Cambridge University Press:  14 April 2009

Jerry A. Coyne ,
John Rux  and
Jean R. David
Jerry A. Coyne*
Affiliation:
Department of Ecology and Evolution, The University of Chicago, 1103 East 57th Street, Chicago, Illinois 60637, USA
John Rux
Affiliation:
Department of Ecology and Evolution, The University of Chicago, 1103 East 57th Street, Chicago, Illinois 60637, USA
Jean R. David
Affiliation:
Laboratoire de Biologie et Génétique Évolutives, Centre National de la Recherche Scientifique, 91198 Gif-sur-Yvette Cedex, France
*
* Corresponding author.
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Summary

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We conducted classical genetic analysis of the difference in male genitalia and hybrid sterility between the island-dwelling sibling species Drosophila sechellia and D. mauritiana. At least two loci (one on each autosome) are responsible for the genital difference, with the X chromosome having no significant effect. In contrast, male hybrid sterility is caused by at least four gene loci distributed among all major chromosomes, with those on the X chromosome having the largest effect.

We also show that the large difference in ovariole number between D. sechellia and its mainland relative D. simulans is due to at least two gene substitutions, one on each major autosome. The X and the left arm of the second chromosome, however, have no significant effect on the character. This implies that the evolution of reduced ovariole number involved relatively few gene substitutions.

These results extend previous findings that morphological differences between Drosophila species are caused by genes distributed among all chromosomes, while hybrid sterility and inviability are due primarily to X-linked genes. Because strong X-effects on male sterility have been found in all three pairwise hybridizations among D. simulans, D. sechellia and D. mauritiana, these effects must have evolved at least twice independently.

Type
Research Article
Information
Genetics Research , Volume 57 , Issue 2 , April 1991 , pp. 113 - 122
Copyright
Copyright © Cambridge University Press 1991

References

Caccone, A., Amato, G. D. & Powell, J. R. (1988). Rates and patterns of scnDNA and mtDNA divergence within the Drosophila melanogaster subgroup. Genetics 118, 671–683.CrossRefGoogle ScholarPubMed
Cariou, M. L. (1987). Biochemical phylogeny of the eight species in the Drosophila melanogaster subgroup, including D. sechellia and D. orena. Genetical Research 50, 181–185.CrossRefGoogle ScholarPubMed
Charlesworth, B., Coyne, J. A., and Barton, N. H. (1987). Relative rates of evolution of sex chromosomes and autosomes. American Naturalist 130, 113–146.CrossRefGoogle Scholar
Coyne, J. A. (1983). Genetic basis of differences in genital morphology among three sibling species of Drosophila. Evolution 37, 1101–1118.CrossRefGoogle ScholarPubMed
Coyne, J. A. (1984). Genetic basis of male sterility in hybrids between two closely related species of Drosophila. Proceedings of the National Academy of Science USA 81, 4444–4447.CrossRefGoogle ScholarPubMed
Coyne, J. A. (1985 a). The genetic basis of Haldane's rule. Nature 314, 736–738.CrossRefGoogle ScholarPubMed
Coyne, J. A. (1985 b). Genetic studies of three sibling species of Drosophila with relationship to theories of speciation. Genetical Research 46, 169–192.CrossRefGoogle ScholarPubMed
Coyne, J. A. (1989). The genetics of sexual isolation in two sibling species of Drosophila, D. simulons and D. mauritiana. Proceedings of the National Academy of Science USA 86, 5464–5468.CrossRefGoogle Scholar
Coyne, J. A. & Charlesworth, B. (1986). Location of an X-linked factor causing sterility in male hybrids of Drosophila simulons and D. mauritiana. Heredity 57, 243–246.CrossRefGoogle ScholarPubMed
Coyne, J. A. & Kreitman, M. (1986). Evolutionary genetics of two sibling species, Drosophila simulons and D. sechellia. Evolution 40, 673–691.CrossRefGoogle ScholarPubMed
Coyne, J. A. & Charlesworth, B. (1989). Genetic analysis of X-linked sterility in hybrids between three sibling species of Drosophila. Heredity 62, 97–106.CrossRefGoogle ScholarPubMed
Coyne, J. A. & Orr, H. A. (1989). Two rules of speciation. In Speciation and its Consequence (ed. Otte, D. and Endler, J.), pp. 180–207. Sunderland, MA: Sinauer Associates.Google Scholar
David, J. R. & Bocquet, C. (1975). Similarities and differences in latitudinal adaptation of two Drosophila sibling species. Nature 257, 588–590.CrossRefGoogle ScholarPubMed
David, J. R. & Clavel, M. F. (1965). Interaction entre le génotype et le milieu d'élevage. Conséquences sur les caractéristiques du développement de la Drosophila. Bulletin Biologique de la France et de la Belgique 99, 369–378.Google Scholar
David, J., Lemeunier, F., Tscacas, L. & Bocquet, C. (1974). Hybridation d'une nouvelle espèce Drosophila mauritiana avec D. melanogaster et D. simulons. Annales Génétique 17, 234–241.Google Scholar
Dobzhansky, T. (1936). Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 21, 113–135.CrossRefGoogle ScholarPubMed
Fisher, R. A. (1958). The Genetical Theory of Natural Selection. New York: Dover.Google Scholar
Haldane, J. B. S. (1922). Sex-ratio and unisexual sterility in hybrid animals. Journal of Genetics 12, 101–109.CrossRefGoogle Scholar
Lachaise, D., Cariou, M.-L., David, J. R., Lemeunier, F., Tsacas, L. & Ashburner, M. (1988). Historical bio-geography of the Drosophila melanogaster species subgroup. Evolutionary Biology 22, 159–225.CrossRefGoogle Scholar
Lande, R. (1983). The response to selection on major and minor mutations affecting a metrical trait. Heredity 50, 47–65.CrossRefGoogle Scholar
Lande, R. & Arnold, S. J. (1985). Evolution of mating preference and sexual dimorphism. Journal of Theoretical Biology 117, 651–664.CrossRefGoogle ScholarPubMed
Lemeunier, F. & Ashburner, M. (1976). Relationships within the melanogaster subgroup of the genus Drosophila (Sophophora). II. Phylogenetic relationships between six species based upon polytene chromosome banding sequences. Proceedings of the Royal Society of London B93, 275–294.Google Scholar
Lemeunier, F. & Ashburner, M. (1984). Relationships within the melanogaster subgroup of the genus Drosophila (Sophophora). IV. The chromosomes of two new species. Chromosoma 89, 343–351.CrossRefGoogle Scholar
Lemeunier, F., David, J. R., Tsacas, L. & Ashburner, M. (1986). The melanogaster species group. In The Genetics and Biology of Drosophila, vol. 3e (ed. Ashburner, M., Carson, H. L. and Thompson, J. N. Jr), pp. 147–256. London: Academic Press.Google Scholar
Louis, J. & David, J. R. (1986). Ecological specialization in the Drosophila melanogaster species subgroup: a case study of D. sechellia. Acta Oecologica/Oecologia Generalis 7, 215–229.Google Scholar
Mahowald, A. P. & Kambysellis, M. P. (1980). Oogenesis. In The Genetics and Biology of Drosophila, vol. 2d (ed. Ashburner, M. and Wright, T. R. F.), pp. 141–224. London: Academic Press.Google Scholar
Mayr, E. (1963). Animal Species and Evolution. Cambridge, MA: Harvard University Press.CrossRefGoogle Scholar
Orr, H.A. (1987). Genetics of male and female sterility in hybrids of Drosophila pseudoobscura and D. persimilis. Genetics 116, 555–563.CrossRefGoogle ScholarPubMed
Orr, H. A. (1990). Genetics of postzygotic isolation between Drosophila melanogaster and D. simulons. Drosophila Information Service (in the press).Google Scholar
Shrimpton, A. E. & Robertson, A. (1988). The isolation of polygenic factors controlling bristle score in Drosophila melanogaster.I. Distribution of third chromosome bristle effects within chromosome sections. Genetics 118, 445–459.CrossRefGoogle ScholarPubMed
Solignac, M., Monnerot, M. & Mounolou, J.-C. (1986). Mitochondrial DNA evolution in the melanogaster subgroup of Drosophila. Journal of Molecular Evolution 23, 31–40.CrossRefGoogle ScholarPubMed
Sturtevant, A. H. (1929). The genetics of Drosophila simulans. In Contributions to the Genetics of Drosophila simulans and Drosophila melanogaster (ed. Sturtevant, A. H, Bridges, C. B., Morgan, T. H., Morgan, L. V. and Li, J. C.), pp. 1–62. Washington: Carnegie Institute, publication 339.Google Scholar
Tsacas, L. & Bächli, G. (1981). Drosophila sechellia n. sp., huitième espèce du sousgroupe melanogaster des Iles Séchelles (Diptera, Drosophilidae). Revue Fr. Entomol. 3, 146–150.Google Scholar
Tsacas, L. & David, J. (1974). Drosophila mauritiana, n. sp. du groupe melanogaster de l'Ile 1974. Bulletin de la Société Entomologique de France 79, 42–44.CrossRefGoogle Scholar
Turner, J. R. G. (1977). Butterfly mimicry: the genetical evolution of an adaptation. Evolutionary Biology 10, 163 206.Google Scholar
Wu, C.-I. & Beckenbach, A. T. (1983). Evidence for extensive genetic differentiation between the sex-ratio and the standard arrangement of Drosophila pseudoobscura and identification of hybrid sterility factors. Genetics 105, 71–86.CrossRefGoogle ScholarPubMed