CYTOLOGICAL CHARACTERIZATION OF PREMEIOTIC VERSUS POSTMEIOTIC DEFECTS PRODUCING HYBRID MALE STERILITY AMONG SIBLING SPECIES OF THE DROSOPHILA MELANOGASTER COMPLEX
Rob Kulathinal
Department of Biology, McMaster University, Hamilton, Ontario, L8S 4K1 Canada
Search for more papers by this authorRama S. Singh
Department of Biology, McMaster University, Hamilton, Ontario, L8S 4K1 Canada
Search for more papers by this authorRob Kulathinal
Department of Biology, McMaster University, Hamilton, Ontario, L8S 4K1 Canada
Search for more papers by this authorRama S. Singh
Department of Biology, McMaster University, Hamilton, Ontario, L8S 4K1 Canada
Search for more papers by this authorAbstract
In accordance with Haldane's rule, hybridizations between species of the Drosophila simulans clade produce fertile females but sterile males. In this study, a comprehensive characterization was undertaken on the six types of F1 males that were the result of the crosses between D. simulans, D. sechellia, and D. mauritiana. With the use of light and electron microscopy, it was shown that while each particular hybrid genotype exhibited a specific sterility phenotype, these phenotypes fell into two distinct classes. The two hybrid genotypes that possessed D. mauritiana X-chromosomes contained spermatogenic defects that caused arrests in premeiotic spermatogenic stages. The other four F1 hybrids possessed postmeiotic spermatogenic defects. Nonsynchronous cell divisions, underdeveloped mitochondrial derivative-axonemal associations, and microtubule abnormalities were common to all of these hybrids. Each particular postmeiotically defective hybrid genotype demonstrated characteristically distinct profiles in sperm bundle number in addition to characteristic spermiogenic arrests in the furthest developed spermatids. These results in species hybrids contrast with the absence of significant differences in spermatogenic characters between species of this clade. In addition, by utilizing an attached-X cross, we investigated the influence of maternal effects and cytoplasmic factors on the sterility of D. simulans F1 hybrids and found none. However, we discovered a strain of D. simulans (2119) that caused a large shift in sterility from postmeiotic to premeiotic when crossed to D. sechellia. This suggests that D. simulans is polymorphic for genes involving premeiotic and postmeiotic sterility and that the two types of sterilities between species may have a simple genetic basis.
Literature Cited
- Alphey, A., J. Jimenez, H. White-Cooper, I. Dawson, P. Nurse, and D. M. Glover. 1992. twine, a cdc25 homologue that functions in the male and female germline of Drosophila. Cell 69: 977–988.
- Ashburner, M. 1989. Drosophila: a laboratory manual. Cold Spring Harbor Laboratory Press, New York.
- Bock, I. R. 1984. Interspecific hybridization in the genus Drosophila. Evol. Biol. 18: 41–70.
10.1007/978-1-4615-6977-0_3 Google Scholar
- Castrillon, D. H., R. Gonczy, S. Alexander, R. Rawson, C. G. Eberhart, S. Viswanathan, S. Dinardo, and S. A. Wasserman. 1993. Toward a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: characterization of male-sterile mutants generated by single P element mutagenesis. Genetics 135: 489–505.
- Civetta, A., and R. S. Singh. 1998. Sex and speciation: genetic architecture and evolutionary potential of sexual versus nonsexual traits in the sibling species of the Drosophila melanogaster complex. Evolution 52: 1080–1092.
- Courtot, C., C. Frankhauser, V. Simanis, and C. Lehner. 1992. The Drosophila cdc25 homolog twine is required for meiosis. Development 116: 395–402.
- Coyne, J. A. 1984. Genetic basis of male sterility in hybrids between two closely related species of Drosophila. Proc. Nat. Acad. Sci. USA 81: 4444–4447.
- Coyne, J. A. 1985. The genetic basis of Haldane's rule. Nature 314: 736–738.
- Coyne, J. A., and B. Charlesworth. 1989. Genetic analysis of X-linked sterility in hybrids between three sibling species of Drosophila. Heredity 62: 97–106.
- Coyne, J. A., and M. Kreitman. 1986. Evolutionary genetics of two sibling species, Drosophila simulans and Drosophila sechellia. Evolution 40: 673–691.
- Coyne, J. A., and H. A. Orr. 1989. Two rules of speciation. Pp. 180–207 in D. Otte and J. A. Endler, eds. Speciation and its consequences. Sinauer, Sunderland, MA.
- Darwin, C. R. 1859. The origin of species by means of natural selection. John Murray, London.
- David, J. R., F. Lemeunier, K. Tsacas, and C. Bocquet. 1974. Hybridation d'une nouvelle espèce Drosophila mauritiana avec D. melanogaster et D. simulans. Ann. Gènèt. 17: 235–241.
- Davis, A. W., E. G. Noonburg, and C.-I. Wu. 1994. Evidence for complex genic interactions between conspecific chromosomes underlying hybrid female sterility in the Drosophila simulans clade. Genetics 137: 191–199.
- Davis, A. W., J. Roote, T. Morley, K. Sawamura, S. Herrmann, and M. Ashburner. 1996. Rescue of hybrid sterility in crosses between D. melanogaster and D. simulans. Nature 380: 157–159.
- Dobzhansky, Th. 1936. Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 21: 113–135.
- Dobzhansky, Th. 1937a. Further data on Drosophila miranda and its hybrids with Drosophila pseudoobscura. J. Genet. 34: 135–151.
10.1007/BF02982259 Google Scholar
- Dobzhansky, Th. 1937b. Genetics and the origin of species. Columbia Univ. Press, New York.
- Dobzhansky, Th. 1970. Genetics and the evolutionary process. Columbia Univ. Press, New York.
- Dobzhansky, Th. 1974. Genetic analysis of hybrid sterility within the species Drosophila pseudoobscura. Hereditas 77: 81–88.
- Dobzhansky, Th., and G. W. Beadle. 1936. Studies on hybrid sterility. IV. Transplanted testes in Drosophila pseudoobscura. Genetics 21: 832–840.
- Dobzhansky, Th., and A. H. Sturtevant. 1935. Further data on maternal effects in Drosophila pseudoobscura hybrids. Genetics 21: 566–570.
- Fuller, M. T. 1993. Spermatogenesis. Pp. 71–148 in M. Bate and A. Martinez-Arias, eds. The Development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, New York.
- Gould-Somero, M., and L. Holland. 1974. The timing of RNA synthesis for spermiogenesis in organ cultures of Drosophila melanogaster testes. Wilhelm Roux's Arch. Dev. Biol. 174: 133–148.
- Goulielmos, G., and E. Zouros. 1995. Incompatibility analysis of male hybrid sterility in two Drosophila species: lack of evidence for maternal, cytoplasmic, or transposable element effects. Am. Nat. 145: 1006–1014.
- Hackstein, J. H. P. 1991. Spermatogenesis in Drosophila. A genetic approach to cellular and subcellular differentiation. European J. Cell Biol. 56: 151–169.
- Haldane, J. B. S. 1922. Sex ratio and unisexual sterility in hybrid animals. J. Genet. 12: 101–109.
- Haldane, J. B. S. 1932. The causes of evolution. Longmans, Green and Company, London.
- Hutter, P., and M. Ashburner. 1987. Genetic rescue of inviable hybrids between Drosophila melanogaster and its sibling species. Nature 327: 331–333.
- Hutter, P., J. Roote, and M. Ashburner. 1990. A genetic basis for the inviability of hybrids between sibling species of Drosophila. Genetics 124: 909–920.
- Joly, D. 1987. Between species divergence of cyst length distributions in the Drosophila melanogaster species complex. Jpn. J. Genet. 62: 257–263.
- Khadem, M., and C. B. Krimbas. 1991. Studies of the species barrier between Drosophila subobscura and D. madeirensis. I. The genetics of male hybrid sterility. Heredity 67: 157–165.
- Lachaise, D., J. R. David, F. Lemeunier, L. Tsacas, and M. Ashburner. 1986. The reproductive relationships of Drosophila sechellia with D. mauritiana, D. simulans, and D. melanogaster from the Afrotropical region. Evolution 40: 262–271.
- Lachaise, D., M.-L. Cariou, J. R. David, F. Lemeunier, L. Tsacas, and M. Ashburner. 1988. Historical biogeography of the Drosophila melanogaster species subgroup. Evol. Biol. 22: 159–225.
- Lifschytz, E. 1987. The developmental program of spermiogenesis in Drosophila: a genetic analysis. Int. Rev. Cytol. 109: 211–257.
- Lindsley, D. L., and E. Lifschytz. 1972. The genetic control of spermatogenesis in Drosophila. Pp. 203–222 in R. A. Beatty and S. Gluecksohn-Waelsch. Proceedings of the international symposium on the genetics of the spermatozoon. Bogtrykkeriet Forum, Copenhagen, Denmark.
- Lindsley, D. L., and K. T. Tokuyasu. 1980. Spermatogenesis. Pp. 225–294 in M. Ashburner and T. R. F. Wright, eds. The genetics and biology of Drosophila. Vol 2D. Academic Press, London.
- Lindsley, D. L., and G. G. Zimm. 1992. The genome of Drosophila melanogaster. Academic Press, San Diego, CA.
- Muller, H. J. 1942. Isolating mechanisms, evolution, and temperature. Biol Symp. 6: 71–125.
- Olivieri, G., and A. Olivieri. 1965. Autoradiographic study of nucleic acid synthesis during spermatogenesis in Drosophila melanogaster. Mutat. Res. 2: 366–380.
- Orr, H. A. 1987. Genetics of male and female sterility in hybrids of Drosophila pseudoobscura and D. persimilis. Genetics 116: 555–563.
- Orr, H. A. 1989. Genetics of sterility in hybrids between two subspecies of Drosophila. Evolution 43: 180–189.
- Orr, H. A. 1995. The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139: 1805–1813.
- Perez, D. E., C.-I. Wu, N. A. Johnson, and M.-L. Wu. 1993. Genetics of reproductive isolation in the Drosophila simulans clade: DNA marker-assisted mapping and characterization of a hybrid-male sterility gene, Odysseus (Ods). Genetics 133: 261–275.
- Sawamura, K., T. Taira, and T. K. Watanabe. 1993a. Hybrid lethal systems in the Drosophila melanogaster species complex. I. The maternal hybrid rescue (mhr) gene of Drosophila simulans. Genetics 133: 299–305.
- Sawamura, K., M.-T. Yamamoto, and T. K. Watanabe. 1993b. Hybrid lethal systems in the Drosophila melanogaster species complex. II. The zygotic hybrid rescue (Zhr) gene of Drosophila melanogaster. Genetics 133: 307–313.
- Sturtevant, A. H. 1919. A new species resembling Drosophila melanogaster. Psyche 26: 153–155.
10.1155/1919/97402 Google Scholar
- Sturtevant, A. H. 1920. Genetic studies on Drosophila simulans. I. Introduction. Hybrids with Drosophila melanogaster. Genetics 5: 488–500.
- Tokuyasu, K. T., W. J. Peacock, and R. W. Hardy. 1972. Dynamics of spermiogenesis in Drosophila melanogaster. I. Individualization process. Z. Zellforsch. 84: 141–175.
- Tsacas, L., and G. Bächli. 1981. Drosophila sechellia, n. sp., huitième espèce du sous-groupe melanogaster des Iles Séchelles Revue Fr. Entomol. 3: 146–150.
- Tsacas, L., and J. David. 1974. Drosophila mauritiana n. sp. du groupe melanogaster de l'île Maurice. Bull. Soc. Entomol Fr 79: 42–46.
- Turelli, M., and H. A. Orr. 1995. The dominance theory of Haldane's rule. Genetics 140: 389–402.
- Vigneault, G., and E. Zouros. 1986. The genetics of asymmetrical male sterility in Drosophila mojavensis and D. arizonensis hybrids: interactions between the Y-chromosome and autosomes Evolution 40: 1160–1170.
- Watanabe, T. K. 1979. A gene that rescues the lethal hybrid between Drosophila melanogaster and Drosophila simulans. Jpn J. Genet. 54: 325–331.
- Wu, C.-I. 1992. A note on Haldane's rule: hybrid inviability versus hybrid sterility. Evolution 46: 1584–1587.
- Wu, C.-I., and A. T. Beckenbach. 1983. Evidence for extensive genetic differentiation between the sex-ratio and the standard arrangement of Drosophila pseudoobscura and D. persimilis and identification of hybrid sterility factors. Genetics 105: 71–86.
- Wu, C.-I., and A. W. Davis. 1993. Evolution of postmating reproductive isolation: the composite nature of Haldane's rule and its genetic bases. Am. Nat. 142: 187–212.
- Zeng, L.-W., and R. S. Singh. 1993. The genetic basis of Haldane's rule and the nature of asymmetric hybrid male sterility between Drosophila simulans, Drosophila mauritiana, and Drosophila sechellia. Genetics 134: 251–260.
- Zouros, E. 1981. An autosome-Y chromosome combination that causes sterility in D. mojavensis X D. arizonensis hybrids. Dros. Inf. Serv. 56: 167–168.
- Zouros, E. 1989. Advances in the genetics of reproductive isolation in Drosophila. Genome 31: 211–220.