Skip to main content
SpringerLink
Log in

Genetics of Hybrid Inviability and Sterility in Drosophila: Dissection of Introgression of D. simulans Genes in D. melanogaster Genome

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Interspecific crosses between Drosophila melanogaster and Drosophila simulans usually produce sterile unisexual hybrids. The barrier preventing genetic analysis of hybrid inviability and sterility has been taken away by the discovery of a D. simulans strain which produces fertile female hybrids. D. simulans genes in the cytological locations of 21A1 to 22C1-23B1 and 30F3-31C5 to 36A2-7 have been introgressed into the D. melanogaster genetic background by consecutive backcrosses. Flies heterozygous for the introgression are fertile, while homozygotes are sterile both in females and males. The genes responsible for the sterility have been mapped in the introgression. The male sterility is caused by the synergistic effect of multiple genes, while the female sterility genes have been localized to a 170 kb region (32D2 to 32E4) containing 20 open reading frames. Thus, the female sterility might be attributed to a single gene with a large effect. We have also found that the Lethal hybrid rescue mutation which prevents the inviability of male hybrids from the cross of D. melanogaster females and D. simulans males cannot rescue those carrying the introgression, suggesting that D. simulans genes maybe non-functional in this hybrid genotype. The genes responsible for the inviability have not been separated from the female sterility genes by recombination.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adams, M.D. et al., 2000. The genome sequence of Drosophila melanogaster. Science 287: 2185–2195.

    Google Scholar 

  • Agard, D.A., Y. Hiraoka, P. Shaw & J. Sedat, 1989. Fluorescence microscopy in three dimensions, pp. 353–377 in Methods in Cell Biology, Vol. 30, edited by L. Wilson. Academic Press, New York.

    Google Scholar 

  • Ashburner, M. et al., 1999. An exploration of the sequence of a 2.9-Mb region of the genome of Drosophila melanogaster. The Adh region. Genetics 153: 179–219.

    Google Scholar 

  • Barbash, D.A. & M. Ashburner, 2001. A novel system of fertility rescue in D. melanogaster/D. simulans species hybrids. Ann. Drosophila Res. Conf. 42: 889.

    Google Scholar 

  • Barbash, D.A. & M. Ashburner, 2003. A novel system of fertility rescue in Drosophila hybrids reveals a link between hybrid lethality and female sterility. Genetics 163: 217–226.

    Google Scholar 

  • Barbash, D.A., J. Roote & M. Ashburner, 2000. The Drosophila melanogaster Hybrid male rescue gene causes inviability in male and female species hybrids. Genetics 154: 1747–1771.

    Google Scholar 

  • Barrio, R., J.F. de Celis, S. Bolshakov & F.C. Kafatos, 1999. Identification of regulatory regions driving the expression of the Drosophila spalt complex at different developmental stages. Dev. Biol. 215: 33–47.

    Google Scholar 

  • Coulhart, M.B. & R.S. Singh, 1988. High level of divergence of male-reproductive-tract proteins between Drosophila melanogaster and its sibling species, Drosophila simulans. Mol. Biol. Evol. 5: 182–191.

    Google Scholar 

  • Coyne, J.A., S. Simeonidis & P. Rooney, 1998. Relative paucity of genes causing inviability in hybrids between Drosophila melanogaster and D. simulans. Genetics 150: 1091–1103.

    Google Scholar 

  • Davis, A.W., J. Roote, T. Morley, K. Sawamura, S. Herrmann & M. Ashburner, 1996. Rescue of hybrid sterility in crosses between D. melanogaster and D. simulans. Nature 380: 157–159.

    Google Scholar 

  • Dobzhansky, T., 1937. Genetics and the Origin of Species. Columbia University Press, New York.

    Google Scholar 

  • Graner, M., K. Stupka & T.L. Karr, 1994. Biochemical and cytological characterization of DROP-1: a widely distributed proteoglycan in Drosophila. Insect Biochem. Mol. Biol. 24: 557–567.

    Google Scholar 

  • Haldane, J.B.S., 1922. Sex ratio and unisexual sterility in hybrid animals. J. Genet. 12: 101–109.

    Google Scholar 

  • Hollocher, H. & C.-I. Wu, 1996. The genetics of reproductive isolation in the Drosophila simulans clade: X vs. autosomal effects and male vs. female effects. Genetics 143: 1243–1255.

    Google Scholar 

  • Hutter, P. & M. Ashburner, 1987. Genetic rescue of inviable hybrids between Drosophila melanogaster and its sibling species. Nature 327: 331–333.

    Google Scholar 

  • Hutter, P., J. Roote & M. Ashburner, 1990. A genetic basis for the inviability of hybrids between sibling species of Drosophila. Genetics 124: 909–920.

    Google Scholar 

  • Karr, T.L., 1991. Intracellular sperm/egg interactions in Drosophila: a three-dimensional structural analysis of a paternal product in the developing egg. Mech. Dev. 34: 101–112.

    Google Scholar 

  • Karr, T.L. & B.M. Alberts, 1986. Organization of the cytoskeleton in early Drosophila embryos. J. Cell Biol. 102: 1494–1509.

    Google Scholar 

  • Liu, J., J.M. Mercer, L.F. Stam, G.C. Gibson, Z.-B. Zeng & C.C. Laurie, 1996. Genetic analysis of a morphological shape difference in the male genitalia of Drosophila simulans and D. mauritiana. Genetics 142: 1129–1145.

    Google Scholar 

  • Mayr, E., 1942. Systematics and the Origin of Species. Columbia University Press, New York.

    Google Scholar 

  • Muller, H.J. & G. Pontecorvo, 1940. Recombinants between Drosophila species the F1 hybrids of which are sterile. Nature 146: 199–200.

    Google Scholar 

  • Nurminsky, D.I., M.V. Nurminskaya, D. De Aguiar & D.L. Hartl, 1998. Selective sweep of a newly evolved sperm-specific gene in Drosophila. Nature 396: 572–575.

    Google Scholar 

  • Orr, H.A., 1992. Mapping and characterization of a 'speciation gene' in Drosophila. Genet. Res. 59: 73–80.

    Google Scholar 

  • Orr, H.A. & S. Irving, 2000. Genetic analysis of the Hybrid male rescue locus of Drosophila. Genetics 155: 225–231.

    Google Scholar 

  • Presgraves, D.C., 2003. A fine-scale genetic analysis of hybrid incompatibilities in Drosophila. Genetics 163: 955–972.

    Google Scholar 

  • Sawamura, K., 2000. Genetics of hybrid inviability and sterility in Drosophila: the Drosophila melanogaster-Drosophila simulans case. Plant Species Biol. 15: 237–247.

    Google Scholar 

  • Sawamura, K., A.W. Davis & C.-I. Wu, 2000. Genetic analysis of speciation by means of introgression into Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 97: 2652–2655.

    Google Scholar 

  • Sawamura, K., T. Taira & T.K. Watanabe, 1993. Hybrid lethal systems in the Drosophila melanogaster species complex. I. The maternal hybrid rescue (mhr) gene of Drosophila simulans. Genetics 133: 299–305.

    Google Scholar 

  • Sawamura, K., M.-T. Yamamoto & T.K. Watanabe, 1993. Hybrid lethal systems in the Drosophila melanogaster species complex. II. The Zygotic hybrid rescue (Zhr) gene of D. melanogaster. Genetics 133: 307–313.

    Google Scholar 

  • Sawamura, K., J. Roote, C.-I. Wu & M.-T. Yamamoto (in preparation). Reassessment of Dobzhansky-Muller model of reproductive isolation: genetic analysis of male sterility caused by interspecific introgression in Drosophila.

  • Singh, R.S. & R.J. Kulathinal, 2000. Sex gene pool evolution and speciation: a new paradigm. Genes Genet. Syst. 75: 119–130.

    Google Scholar 

  • Sturtevant, A.H., 1920. Genetic studies on Drosophila simulans. I. Introduction. Hybrids with Drosophila melanogaster. Genetics 5: 488–500.

    Google Scholar 

  • Swanson, W.J., A.G. Clark, H.M. Waldrip-Dail, M.F. Wolfner & C.F. Aquadro, 2001. Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc. Natl. Acad. Sci. USA 98: 7375–7379.

    Google Scholar 

  • Ting, C.-T., S.-C. Tsaur, M.-L. Wu & C.-I. Wu, 1998. A rapidly evolving homeobox at the site of a hybrid sterility gene. Science 282: 1501–1504.

    Google Scholar 

  • True, J.R., B.S. Weir & C.C. Laurie, 1996. A genome-wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans. Genetics 142: 819–837.

    Google Scholar 

  • Tsaur, S.-C. & C.-I. Wu, 1997. Positive selection and the molecular evolution of a gene of male reproduction, Acp26Aa of Drosophila. Mol. Biol. Evol. 14: 544–549.

    Google Scholar 

  • Watanabe, T.K., 1979. A gene that rescues the lethal hybrids between Drosophila melanogaster and Drosophila simulans. Jpn. J. Genet. 54: 325–331.

    Google Scholar 

  • Wu, C.-I. & M.F. Palopoli, 1994. Genetics of postmating reproductive isolation in animals. Ann. Rev. Genet. 28: 283–308.

    Google Scholar 

  • Wu, C.-I., N.A. Johnson & M.F. Palopoli, 1996. Haldane's rule and its legacy: why are there so many sterile males? Trends Ecol. Evol. 11: 281–284.

    Google Scholar 

  • Yagyu, M., 1997. Master's Thesis. Kyoto Institute of Technology, Kyoto (in Japanese).

    Google Scholar 

  • Yoshii, M., 1999. Master's Thesis. Kyoto Institute of Technology, Kyoto (in Japanese).

    Google Scholar 

Download references

Author information

Author notes

  1. Kyoichi Sawamura

    Present address: Institute of Biological Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki, 305-8572, Japan

  2. Timothy L. Karr

    Present address: Department of Biology and Biochemistry, University of Bath, 4 South Building, Claverton Down, Bath, BA2 7AY, UK

Authors and Affiliations

  1. Drosophila Genetic Resource Center, Kyoto Institute of Technology, Saga-Ippongi-cho, Ukyo-ku, Kyoto, 616-8354, Japan

    Kyoichi Sawamura, Timothy L. Karr & Masa-Toshi Yamamoto

  2. Department of Organismal Biology and Anatomy, University of Chicago, 1027 E. 57th Street, Chicago, IL, 60637, USA

    Timothy L. Karr

Authors
  1. Kyoichi Sawamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Timothy L. Karr
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Masa-Toshi Yamamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sawamura, K., Karr, T.L. & Yamamoto, MT. Genetics of Hybrid Inviability and Sterility in Drosophila: Dissection of Introgression of D. simulans Genes in D. melanogaster Genome. Genetica 120, 253–260 (2004). https://doi.org/10.1023/B:GENE.0000017646.11191.b0

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:GENE.0000017646.11191.b0

Search

Navigation