Skip to main content
PMC home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 1998 Mar 7;265(1394):391–395. doi: 10.1098/rspb.1998.0307

Overcoming cytoplasmic incompatibility in Drosophila.

T L Karr 1, W Yang 1, M E Feder 1
PMCID: PMC1688895  PMID: 9523438

Abstract

The endocellular microbe Wolbachia pipientis infects a wide variety of invertebrate species, in which its presence is closely linked to a form of reproductive failure termed cytoplasmic incompatibility (CI). CI renders infected males unable to father offspring when mated to uninfected females. Because CI can dramatically affect fitness in natural populations, mechanisms that abate CI can have equally large impacts on fitness. We have discovered that repeated copulation by Wolbachia-infected male Drosophila simulans significantly diminishes CI. Repeated copulation does not prevent Wolbachia from populating developing spermatids, but may reduce the time during spermatogenesis when Wolbachia can express CI. This restoration of fertility in premated infected males could have important implications for Wolbachia transmission and persistence in nature and for its exploitation as an agent of biological pest control.

Full Text

The Full Text of this article is available as a PDF (158.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Boyle L., O'Neill S. L., Robertson H. M., Karr T. L. Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science. 1993 Jun 18;260(5115):1796–1799. doi: 10.1126/science.8511587. [DOI] [PubMed] [Google Scholar]
  2. Braig H. R., Guzman H., Tesh R. B., O'Neill S. L. Replacement of the natural Wolbachia symbiont of Drosophila simulans with a mosquito counterpart. Nature. 1994 Feb 3;367(6462):453–455. doi: 10.1038/367453a0. [DOI] [PubMed] [Google Scholar]
  3. Breeuwer J. A., Stouthamer R., Barns S. M., Pelletier D. A., Weisburg W. G., Werren J. H. Phylogeny of cytoplasmic incompatibility micro-organisms in the parasitoid wasp genus Nasonia (Hymenoptera: Pteromalidae) based on 16S ribosomal DNA sequences. Insect Mol Biol. 1992;1(1):25–36. doi: 10.1111/j.1365-2583.1993.tb00074.x. [DOI] [PubMed] [Google Scholar]
  4. Breeuwer J. A., Werren J. H. Cytoplasmic incompatibility and bacterial density in Nasonia vitripennis. Genetics. 1993 Oct;135(2):565–574. doi: 10.1093/genetics/135.2.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bressac C., Rousset F. The reproductive incompatibility system in Drosophila simulans: DAPI-staining analysis of the Wolbachia symbionts in sperm cysts. J Invertebr Pathol. 1993 May;61(3):226–230. doi: 10.1006/jipa.1993.1044. [DOI] [PubMed] [Google Scholar]
  6. Fine P. E. On the dynamics of symbiote-dependent cytoplasmic incompatibility in culicine mosquitoes. J Invertebr Pathol. 1978 Jan;31(1):10–18. doi: 10.1016/0022-2011(78)90102-7. [DOI] [PubMed] [Google Scholar]
  7. Giordano R., O'Neill S. L., Robertson H. M. Wolbachia infections and the expression of cytoplasmic incompatibility in Drosophila sechellia and D. mauritiana. Genetics. 1995 Aug;140(4):1307–1317. doi: 10.1093/genetics/140.4.1307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hoffmann A. A., Turelli M., Harshman L. G. Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics. 1990 Dec;126(4):933–948. doi: 10.1093/genetics/126.4.933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Karr T. L. Cytoplasmic incompatibility. Giant steps sideways. Curr Biol. 1994 Jun 1;4(6):537–540. doi: 10.1016/s0960-9822(00)00118-4. [DOI] [PubMed] [Google Scholar]
  10. LAVEN H. Speciation by cytoplasmic isolation in the Culex pipiens-complex. Cold Spring Harb Symp Quant Biol. 1959;24:166–173. doi: 10.1101/sqb.1959.024.01.017. [DOI] [PubMed] [Google Scholar]
  11. LEFEVRE G., Jr, JONSSON U. B. Sperm transfer, storage, displacement, and utilization in Drosophila melanogaster. Genetics. 1962 Dec;47:1719–1736. doi: 10.1093/genetics/47.12.1719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Laven H. Eradication of Culex pipiens fatigans through cytoplasmic incompatibility. Nature. 1967 Oct 28;216(5113):383–384. doi: 10.1038/216383a0. [DOI] [PubMed] [Google Scholar]
  13. O'Neill S. L., Giordano R., Colbert A. M., Karr T. L., Robertson H. M. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):2699–2702. doi: 10.1073/pnas.89.7.2699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. O'Neill S. L., Karr T. L. Bidirectional incompatibility between conspecific populations of Drosophila simulans. Nature. 1990 Nov 8;348(6297):178–180. doi: 10.1038/348178a0. [DOI] [PubMed] [Google Scholar]
  15. Rousset F., Bouchon D., Pintureau B., Juchault P., Solignac M. Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proc Biol Sci. 1992 Nov 23;250(1328):91–98. doi: 10.1098/rspb.1992.0135. [DOI] [PubMed] [Google Scholar]
  16. Rousset F., Vautrin D., Solignac M. Molecular identification of Wolbachia, the agent of cytoplasmic incompatibility in Drosophila simulans, and variability in relation with host mitochondrial types. Proc Biol Sci. 1992 Mar 23;247(1320):163–168. doi: 10.1098/rspb.1992.0023. [DOI] [PubMed] [Google Scholar]
  17. Turelli M., Hoffmann A. A. Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics. 1995 Aug;140(4):1319–1338. doi: 10.1093/genetics/140.4.1319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Turelli M., Hoffmann A. A., McKechnie S. W. Dynamics of cytoplasmic incompatibility and mtDNA variation in natural Drosophila simulans populations. Genetics. 1992 Nov;132(3):713–723. doi: 10.1093/genetics/132.3.713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Turelli M., Hoffmann A. A. Rapid spread of an inherited incompatibility factor in California Drosophila. Nature. 1991 Oct 3;353(6343):440–442. doi: 10.1038/353440a0. [DOI] [PubMed] [Google Scholar]
  20. Werren J. H., Zhang W., Guo L. R. Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc Biol Sci. 1995 Jul 22;261(1360):55–63. doi: 10.1098/rspb.1995.0117. [DOI] [PubMed] [Google Scholar]
  21. Yen J. H., Barr A. R. The etiological agent of cytoplasmic incompatibility in Culex pipiens. J Invertebr Pathol. 1973 Sep;22(2):242–250. doi: 10.1016/0022-2011(73)90141-9. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES