Hostname: page-component-77c89778f8-vsgnj Total loading time: 0 Render date: 2024-07-16T21:24:00.431Z Has data issue: false hasContentIssue false
  • English
  • Français

Genetic studies of three sibling species of Drosophila with relationship to theories of speciation

Published online by Cambridge University Press:  14 April 2009

Jerry A. Coyne
Jerry A. Coyne
Affiliation:
Department of Zoology, the University of Maryland, College Park, MD 20742, USA

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.

Drosophila melanogaster, D. simulans and D. mauritiana are closely related species, the first two cosmopolitan and the last restricted to the oceanic island of Mauritius. D. simulans and D. mauritiana are the most closely related pair, with the latter species probably resulting from a founder event. The relatedness of the three species and their ability to hybridize allow tests of recent theories of speciation. Genetic analysis of two characters differing between D. simulans and D. mauritiana (sex comb tooth number and testis colour) show that the differences are due to at least five and three loci respectively. Behavioural tests further demonstrate that sex combs are probably used by males at a crucial step in mating, and that the differences between the two species may be related to differences in their mating ability. These genetic studies and previous work indicate that differences among these species are polygenic and not (as proposed by recent theories) attributable to only one or two loci of large effect. Further studies of interspecific hybrids show that genetic divergence leading to developmental anomalies is more advanced in the older species pair D. simulans/D. melanogaeter than in the younger pair D. simulans/D. mauritiana. This supports the neo-Darwinian contention that reproductive isolation is one step in a continuous process of genetic change among isolated populations, and does not support current theories that such change occurs only during the evolution of reproductive isolation. Finally, investigations of the degree of gonadal atrophy and its sensitivity to temperature in D. simulans/D. mauritiana hybrids fail to support recent speculations that phenomena similar to hybrid dysgenesis (which causes such atrophy in D. melanogaster) play a role in speciation.

Type
Research Article
Information
Genetics Research , Volume 46 , Issue 2 , October 1985 , pp. 169 - 192
Copyright
Copyright © Cambridge University Press 1985

References

REFERENCES

Ahearn, J. N. (1980). Evolution of behavioral reproductive isolation in a laboratory stock of Drosophila silvestris. Experientia 36, 63–64.Google Scholar
Avise, J. C. (1976). Genetic differentiation during speciation. In Molecular Evolution (ed. Ayala, F. J.), pp. 106–122. Sunderland, Massachussetts, Sinauer.Google Scholar
Ayala, F. J. (1975). Genetic differentiation during the speciation process. Evolutionary Biology 8, 1–73.Google Scholar
Barnes, S. R., Webb, D. A. & Dover, G. (1978). The distribution of satellite and main-band DNA components in the melanogaster species subgroup of Drosophila. Chromosomu 67, 341–363.Google Scholar
Barton, N. & Charlesworth, B. (1984). Genetic revolutions, founder effects, and speciation. Annual Review of Ecology and Systematics 15, 133–164.Google Scholar
Biddle, R. L. (1932). The bristles of hybrids between Drosophila melanogaster and Drosophila simulans. Genetics 17, 153–174.CrossRefGoogle ScholarPubMed
Bingham, P. M., Kidwell, M. G. & Rubin, G. M. (1982). The molecular basis of P-M hybrid dysgenesis: the role of the P element, a P-strain specific transposon family. Cell 29, 995–1004.CrossRefGoogle Scholar
Bock, J. R. (1984). Interspecific hybridization in the genus Drosophila. Evolutionary Biology 18, 41–70.Google Scholar
Bodmer, M. & Ashburner, M. (1984). Conservation and change in the DNA sequences coding for alcohol dehydrogenase in sibling species of Drosophila. Nature 309, 425–429.Google Scholar
Bregliano, J.-C. & Kidwell, M. G. (1983). Hybrid dysgenesis determinants. In Mobile Genetic Elements (ed. Shapiro, J. A.), pp. 363–410. London: Academic Press.Google Scholar
Carson, H. L. (1975). The genetics of speciation at the diploid level. The American Naturalist 109, 83–92.Google Scholar
Carson, H. L. & Kaneshiro, K. Y. (1976). Drosophila of Hawaii: systematics and ecological genetics. Annual Review of Ecology and Systematics 7, 311–345.CrossRefGoogle Scholar
Carson, H. L. & Templeton, A. R. (1984). Genetic revolutions in relation to speciation phenomena: the founding of new populations. Annual Review of Ecology and Systematics 15, 97–131.Google Scholar
Charlesworth, B., Lande, R. & Slatkin, M. (1982). A neo-Darwinian commentary on macroevolution. Evolution 36, 1101–1118.Google ScholarPubMed
Coen, E., Strachan, T. & Dover, G. (1982). Dynamics of concerted evolution of ribosomal DNA and histone gene families in the melanogaster species subgroup of Drosophila. Journal of Molecular Biology 158, 17–35.Google Scholar
Cohn, V. H., Thompson, M. A. & Moore, G. P. (1984). Nucleotide sequence comparison of the Adh gene in three drosophilids. Journal of Molecular Biology 20, 31–37.Google ScholarPubMed
Cook, R. M. (1977). Behavioral role of the sexcombs in Drosophila melanogasler and Drosophila simulans. Behavior Genetics 7, 349–357.CrossRefGoogle Scholar
Coyne, J. A. (1983). Genetic basis of differences in genital morphology among three sibling species of Drosophila. Evolution 37, 1101–1118.Google Scholar
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.Google Scholar
Coyne, J. A. (1985). The genetic basis of Haldane's rule. Nature 314, 736–738.CrossRefGoogle ScholarPubMed
David, J., Lemeunier, F., Tsacas, K. & Bouquet, C. (1974). Hybridation d'une nouvelle espèce Drosophila mauritiana avec D. melanogaster et D. simulans. Annales de Génétique 17, 235–241.Google Scholar
David, J., Bocquet, C., Lemeunier, F. & Tsacas, L. (1976). Persistence of male sterility in strains issued from hybrids between two sibling species: Drosophila simulans and D. mauritiana. Journal of Genetics 62, 93–100.CrossRefGoogle Scholar
Dobzhansky, T. (1951). Genetics and the Origin of Species. New York. Columbia University Press.Google Scholar
Douglas, M. E. & Avise, J. C. (1982). Speciation rates and morphological divergence in fishes: tests of gradual versus rectangular modes of evolutionary change. Evolution 36, 224–232.CrossRefGoogle ScholarPubMed
Engels, W. R. & Preston, C. R. (1979). Hybrid dysgenesis in Drosophila melanogaster: the biology of male and female sterility. Genetics 92, 161–174.Google Scholar
Falconer, D. S. (1960). Quantitative Genetics. New York: Ronald Press.Google Scholar
Ginzburg, L. R., Bingham, P. M. & Yoo, S. (1984). On the theory of speciation induced by transposable elements. Genetics 107, 331–341.CrossRefGoogle ScholarPubMed
Gonzales, A. M., Cabrera, V. M., Larrunga, J. M. & Gullon, A. (1982). Genetic distance in the sibling species Drosophila melanogaster, D. simulans, and D. mauritiana. Evolution 36, 517–522.CrossRefGoogle Scholar
Gould, S. J. (1977). Ontogeny and Phylogeny. Cambridge, MA: Harvard University Press.Google Scholar
Gould, S. J. (1980). Is a new and general theory of evolution emerging? Paleobiology 6, 119–130.Google Scholar
Hodgson, E. S. (1974). Chemoreception. In The Physiology of Insecta 2nd ed. vol. II ed. Rockstein, M., pp. 127–164. London: Academic Press.CrossRefGoogle Scholar
Horton, I. H. (1939). A comparison of the salivary gland chromosomes of Drosophila melanogaster and D. simulans. Genetics 24, 234–243.CrossRefGoogle ScholarPubMed
Kidwell, M. G. (1983). Evolution of hybrid dysgenesis determinants in Drosophila melanogaster. Proceedings of the National Academy of Science USA 80, 1655–1659.Google Scholar
Kidwell, M. G., Kidwell, J. F. & Sved, J. A. (1977). Hybrid dysgenesis in Drosophila melanogaster: a syndrome of aberrant traits including mutation, sterility, and male recombination. Genetice 86, 813–833.Google Scholar
Kidwell, M. G. & Novy, J. B. (1979). Hybrid dysgenesis in Drosophila melanogaeter: sterility resulting from gonadal dysgenesis in the P-M system. Genetics 92, 1127–1140.Google Scholar
Lande, R. (1981). The minimum number of genes contributing to quantitative variation between and within populations. Genetics 99, 541–553.CrossRefGoogle ScholarPubMed
Lande, R. (1983). The response to selection on major and minor mutations affecting a metrical trait. Heredity 50, 47–45.Google Scholar
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 B 193, 275–294.Google Scholar
Lemeunier, F. & Ashburner, M. (1984). Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora). IV. The chromosomes of two new species. Chromosoma 89, 343–351.Google Scholar
Lewontin, R. C. (1956). Studies on homeostasis and heteozygosity. I. General considerations. Abdominal bristle number in second chromosome homozygotes of Drosophila melanogaster. The American Naturalist 90, 237–255.Google Scholar
Mayr, E. (1954). Change of genetic environment and evolution. In Evohition as a Process (ed. Huxley, J., Hardy, A. C. and Ford, E. B.), pp. 157–180. London: Allen and Unwin.Google Scholar
Mayr, E. (1963). Animal Species and Evolution. Cambridge, MA: Harvard University Press.Google Scholar
Mayr, E. (1982). Speciation and macroevolution. Evolution 36, 1119–1132.Google Scholar
Nei, M., Maruyama, T. & Wu, C.-I. (1983). Models of evolution of reproductive isolation. Genetics 103, 557–579.Google Scholar
Ohnishi, S., Kawanishi, M. & Watanabe, T. K. (1983). Biochemical phytogenies of Drosophila: protein differences detected by two-dimensional electrophoresis. Genetica 61, 55–63.CrossRefGoogle Scholar
Pontecorvo, G. (1943 a). Hybrid sterility in artificially produced recombinants between Drosophila melanogaster and D. simulans. Proceedings of the Royal Society of Edinburgh B 41, 385–297.Google Scholar
Pontecorvo, G. (1943 b). Viability interactions between chromosomes of Drosophila melanogaster and Drosophila simulans. Journal of Genetics 45, 51–66.CrossRefGoogle Scholar
Rose, M. R. & Doolittle, W. F. (1983). Molecular biological mechanisms of speciation. Science 220, 157–162.Google Scholar
Schaefer, R. E., Kidwell, M. G. & Fausto-Sterling, A. (1979). Hybrid dysgenesis in Drosophila melanogaster: morphological and cytological studies of ovarian dysgenesis. Genetics 92, 1141–1152.Google Scholar
Snedecor, G. W. & Cochran, W. G. (1967). Statistical Methods, 6th ed.Ames, Iowa: Iowa State University Press.Google Scholar
Sokal, R. R. & Rohlf, F. J. (1981). Biometry. San Francisco: Freeman.Google Scholar
Spieth, A. A. (1952). Mating behavior within the genus Drosophila (Diptera). Bulletin of the American Museum of Natural History 99, 395–474.Google Scholar
Spirito, F., Rossi, C. & Rizzoni, M. (1983). Reduction of gene flow due to the partial sterility of heterozygotes for a chromosomal mutation. I. Studies on a ‘neutral’ gene not linked to the chromosomal mutation in a two population model. Evolution 37, 785–797.Google Scholar
Stanley, S. M. (1979). Macroevolution: Pattern and Process. San Francisco: Freeman.Google Scholar
Strachan, T., Coen, E.Webb, D. & Dover, G. (1982). Modes and rates of change of complex DNA families of Drosophila. Journal of Molecular Biology 158, 37–54.CrossRefGoogle ScholarPubMed
Sturtevant, A. H. (1919). A new species resembling Drosophila melanogaster. Psyche 26, 153–155.CrossRefGoogle Scholar
Sturtevant, A. H. (1920). Genetic studies on Drosophila simulans. I. Introduction. Hybrids with Drosophila melanogaster. Genetics 5, 488–500.Google Scholar
Sturtevant, A. H. (1929). The Genetics of Drosophila simulans. Carnegie Institute of Washington Publication no. 399, pp. 1–62.Google Scholar
Sved, J. A. (1979). The ‘hybrid dysgenesis’ syndrome in Drosophila melanogaster. Bioscience 29, 659–664.CrossRefGoogle Scholar
Templeton, A. R. (1980). The theory of speciation via the founder principle. Genetics 94, 1101–1138.Google Scholar
Templeton, A. R. (1981). Mechanisms of speciation - a population genetic approach. Annual Review of Ecology and Systematics 12, 23–48.Google Scholar
Templeton, A. R. (1982). Genetic architectures of speciation. In Mechanisms of Speciation (ed. Barigozzi, C.), pp. 105–121. New York: Alan R. Liss.Google Scholar
Thompson, J. N. Jr, Henderson, S. A. & Woodruff, R. C. (1980). Sterility and testis structure in hybrids involving male recombination lines of Drosophila melanogaster. Genetica 51, 221–226.CrossRefGoogle Scholar
Tsacas, L. & David, J. (1974). Drosophila mauritiana n.sp. du groupe melanogaster de l'ile Maurice. Bulletin de la Société entomologique de France 79, 42–46.Google Scholar
Weisbrot, D. (1963). Studies on differences in the genetic architecture of related species of Drosophila. Genetics 48, 1131–1139.CrossRefGoogle ScholarPubMed
White, M. J. D. (1978). Modes of Speciation. San Francisco: Freeman.Google Scholar
Wright, S. (1932). The roles of mutation, inbreeding, crossbreeding and selection in evolution. Proceedings of the Sixth International Congress of Genetics 1, 356–366.Google Scholar
Wright, S. (1968). Evolution and the Genetics of Populations, vol. I, Genetic and Biometrie Foundations. Chicago: University of Chicago Press.Google Scholar
Wright, S. (1982). The shifting balance theory and macroevolution. Annual Review of Genetics 16, 1–19.CrossRefGoogle ScholarPubMed