Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Wolbachia variability and host effects on crossing type in Culex mosquitoes


Wolbachia is a common maternally inherited bacterial symbiont able to induce crossing sterilities known as cytoplasmic incompatibility (CI) in insects1,2. Wolbachia-modified sperm are unable to complete fertilization of uninfected ova, but a rescue function allows infected eggs to develop normally. By providing a reproductive advantage to infected females, Wolbachia can rapidly invade uninfected populations3, and this could provide a mechanism for driving transgenes through pest populations4,5. CI can also occur between Wolbachia-infected populations and is usually associated with the presence of different Wolbachia strains1. In the Culex pipiens mosquito group (including the filariasis vector C. quinquefasciatus) a very unusual degree of complexity of Wolbachia-induced crossing-types has been reported, with partial or complete CI that can be unidirectional or bidirectional6,7,8,9,10,11, yet no Wolbachia strain variation was found11. Here we show variation between incompatible Culex strains in two Wolbachia ankyrin repeat-encoding genes associated with a prophage region, one of which is sex-specifically expressed in some strains, and also a direct effect of the host nuclear genome on CI rescue.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Wolbachia -mediated CI in C. quinquefasciatus.
Figure 2: Wolbachia ANK gene variability.
Figure 3: Effects of host genome introgression on CI.
Figure 4: Results of a model investigating host effects on CI.


  1. O'Neill, S. L., Hoffmann, A. A. & Werren, J. H. (eds) Influential Passengers: Inherited Microorganisms and Arthropod Reproduction (Oxford Univ. Press, Oxford, 1997)

  2. Werren, J. H. Biology of Wolbachia. Annu. Rev. Entomol. 42, 587–609 (1997)

    CAS  Article  Google Scholar 

  3. Turelli, M. & Hoffmann, A. A. Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353, 440–442 (1991)

    ADS  CAS  Article  Google Scholar 

  4. Sinkins, S. P. & O'Neill, S. L. in Insect Transgenesis: Methods and Applications (eds Handler, A. M. & James, A. A.) 271–288 (CRC, Florida, 2000)

    Book  Google Scholar 

  5. Dobson, S. L. Reversing Wolbachia-based population replacement. Trends Parasitol. 19, 128–133 (2003)

    Article  Google Scholar 

  6. Laven, H. in Genetics of Insect Vectors of Disease (eds Wright, R. & Pal, R.) 251–275 (Elsevier, Amsterdam, 1967)

    Google Scholar 

  7. Barr, A. R. Cytoplasmic incompatibility in natural populations of a mosquito, Culex pipiens L. Nature 283, 71–72 (1980)

    ADS  CAS  Article  Google Scholar 

  8. Irving-Bell, R. J. Cytoplasmic incompatibility within and between Culex molestus and Cx. quinquefasciatus (Diptera: Culicidae). J. Med. Entomol. 20, 44–48 (1983)

    Article  Google Scholar 

  9. O'Neill, S. L. & Paterson, H. E. Crossing type variability associated with cytoplasmic incompatibility in Australian populations of the mosquito Culex quinquefasciatus Say. Med. Vet. Entomol. 6, 209–216 (1992)

    CAS  Article  Google Scholar 

  10. Magnin, M., Pasteur, N. & Raymond, M. Multiple incompatibilities within populations of Culex pipiens L. in southern France. Genetica 74, 125–130 (1987)

    CAS  Article  Google Scholar 

  11. Guillemaud, T., Pasteur, N. & Rousset, F. Contrasting levels of variability between cytoplasmic genomes and incompatibility types in the mosquito Culex pipiens. Proc. R. Soc. Lond. B 264, 245–251 (1997)

    ADS  CAS  Article  Google Scholar 

  12. Zhou, W., Rousset, F. & O'Neill, S. L. Phylogeny and PCR-based classification of Wolbachia strains using WSP gene sequences. Proc. R. Soc. Lond. B 265, 509–515 (1998)

    CAS  Article  Google Scholar 

  13. Wu, M. et al. Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLOS Biol. 2, E69–E83 (2004)

    Article  Google Scholar 

  14. Elfring, L. K. et al. Drosophila PLUTONIUM protein is a specialized cell cycle regulator required at the onset of embryogenesis. Mol. Biol. Cell 8, 583–593 (1997)

    CAS  Article  Google Scholar 

  15. Caturegli, P. et al. ankA: an Ehrlichia phagocytophila group gene encoding a cytoplasmic protein antigen with ankyrin repeats. Infect. Immun. 68, 5277–5283 (2000)

    CAS  Article  Google Scholar 

  16. Callaini, G., Dallai, R. & Riparbelli, M. G. Wolbachia-induced delay of paternal chromatin condensation does not prevent maternal chromosomes from entering anaphase in incompatible crosses of Drosophila simulans. J. Cell Sci. 110, 271–280 (1997)

    CAS  PubMed  Google Scholar 

  17. Tram, U. & Sullivan, W. Role of delayed nuclear envelope breakdown and mitosis in Wolbachia-induced cytoplasmic incompatibility. Science 296, 1124–1126 (2002)

    ADS  CAS  Article  Google Scholar 

  18. Song, S. W., Zhao, T. Y., Dong, Y. D. & Lu, B. L. Hybridization of Culex pipiens complex and their relationship with the infections of Wolbachia in China. Acta Entomol. Sin. 45, 705–710 (2002)

    Google Scholar 

  19. Masui, S., Kamoda, S., Sasaki, T. & Ishikawa, H. Distribution and evolution of bacteriophage WO in Wolbachia, the endosymbiont causing sexual alterations in arthropods. J. Mol. Evol. 51, 491–497 (2000)

    ADS  CAS  Article  Google Scholar 

  20. Masui, S. et al. Bacteriophage WO and virus-like particles in Wolbachia, an endosymbiont of arthropods. Biochem. Biophys. Res. Commun. 283, 1099–1104 (2001)

    CAS  Article  Google Scholar 

  21. Wright, J. D., Sjostrand, F. S., Portaro, J. K. & Barr, A. R. The ultrastructure of the Rickettsia-like microorganism Wolbachia pipientis and associated virus-like bodies in the mosquito Culex pipiens. J. Ultrastruct. Res. 63, 79–85 (1978)

    CAS  Article  Google Scholar 

  22. Rousset, F., Raymond, M. & Kjelberg, F. Cytoplasmic incompatibilities in the mosquito Culex pipiens: how to explain a cytotype polymorphism? J. Evol. Biol. 4, 69–81 (1991)

    Article  Google Scholar 

  23. Turelli, M. Evolution of incompatibility-inducing microbes and their hosts. Evolution 48, 1500–1513 (1994)

    Article  Google Scholar 

  24. Raymond, M., Callaghan, A., Fort, P. & Pasteur, N. Worldwide migration of amplified insecticide resistance genes in mosquitoes. Nature 350, 151–153 (1991)

    ADS  CAS  Article  Google Scholar 

  25. Olson, K. E. et al. Genetically engineered resistance to dengue-2 virus transmission in mosquitoes. Science 272, 884–886 (1996)

    ADS  CAS  Article  Google Scholar 

  26. Ito, J., Ghosh, A., Moreira, L. A., Wimmer, E. A. & Jacobs-Lorena, M. Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature 417, 452–455 (2002)

    ADS  CAS  Article  Google Scholar 

  27. Sinkins, S. P. & Godfray, H. C. J. Use of Wolbachia to drive nuclear transgenes through insect populations. Proc. R. Soc. Lond. B 271, 1421–1426 (2004)

    CAS  Article  Google Scholar 

  28. Sanogo, Y. O. & Dobson, S. L. Molecular discrimination of Wolbachia in the Culex pipiens complex: Evidence for variable bacteriophage hyperparasitism. Insect Mol. Biol. 13, 365–369 (2004)

    CAS  Article  Google Scholar 

  29. Williams, E. H., Fields, S. & Saul, G. B. Transfer of incompatibility factors between stocks of Nasonia vitripennis. J. Invert. Pathol. 61, 206–210 (1993)

    CAS  Article  Google Scholar 

  30. Collins, F. H. et al. A ribosomal RNA gene probe differentiates member species of the Anopheles gambiae complex. Am. J. Trop. Med. Hyg. 37, 37–41 (1987)

    CAS  Article  Google Scholar 

Download references


We thank S. O'Neill for Wolbachia genomics input, and S. Song for providing Culex material. This research was supported by grants from the Wellcome Trust, and the UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases (TDR).

Author information

Authors and Affiliations


Corresponding author

Correspondence to Steven P. Sinkins.

Ethics declarations

Competing interests

Sequences have been deposited with NCBI GenBank under accession numbers DQ000469– DQ000472. Reprints and permissions information is available at The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Sinkins, S., Walker, T., Lynd, A. et al. Wolbachia variability and host effects on crossing type in Culex mosquitoes. Nature 436, 257–260 (2005).

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI:

Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing