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Effect of temperature on Wolbachia density and impact on cytoplasmic incompatibility

Published online by Cambridge University Press:  13 September 2005

L. MOUTON
Affiliation:
Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558, Université Lyon 1, 43 Bd du 11 Novembre 1918, 69622 Villeurbanne Cedex, France
H. HENRI
Affiliation:
Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558, Université Lyon 1, 43 Bd du 11 Novembre 1918, 69622 Villeurbanne Cedex, France
M. BOULETREAU
Affiliation:
Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558, Université Lyon 1, 43 Bd du 11 Novembre 1918, 69622 Villeurbanne Cedex, France
F. VAVRE
Affiliation:
Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558, Université Lyon 1, 43 Bd du 11 Novembre 1918, 69622 Villeurbanne Cedex, France

Abstract

The outcome and the evolution of host-symbiont associations depend on environmental constraints, but responses are difficult to predict since they arise from a complex interaction between the host, the parasite and the environment. The situation can be even more complex when multiple parasite genotypes, with potentially different responses to environmental changes, coexist within a single host. In this paper, we investigated the effect of the temperature (from 14 to 26 °C) during the host development on the density of 3 strains of the intracellular bacterium Wolbachia that coexist within the wasp Leptopilina heterotoma. In this species, Wolbachia induces cytoplasmic incompatibility, a sperm-egg incompatibility that allows it to spread and persist in host populations. Using real-time quantitative PCR we found that (i) Wolbachia density is temperature-specific and highest at 26 °C; (ii) the order of the abundance of the 3 Wolbachia strains does not vary with temperature changes; (iii) the response of bacterial density to temperature occurs within a single insect generation, during the egg-to-adult developmental period; (iv) in this species, temperature-related changes in Wolbachia density do not influence cytoplasmic incompatibility.

Type
Research Article
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Bourtzis, K., Braig, H. R. and Karr, T. L. ( 2003). Cytoplasmic incompatibility. In Insect Symbiosis ( ed. Bourtzis, K. and Mille, T. A.), pp. 217247. CRC Press, Boca Raton, Florida, USA.CrossRef
Bourtzis, K., Dobson, S. L., Braig, H. R. and O'Neill, S. L. ( 1998). Rescuing Wolbachia have been overlooked. Nature, London 391, 852853.CrossRefGoogle Scholar
Bourtzis, K., Nirgianaki, A., Markakis, G. and Savakis, C. ( 1996). Wolbachia infection and cytoplasmic incompatibility in Drosophila species. Genetics 144, 10631073.Google Scholar
Boyle, L., O'Neill, S. L., Robertson, H. M. and Karr, T. L. ( 1993). Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science 260, 17961799.CrossRefGoogle Scholar
Braig, H. R., Zhou, W., Dobson, S. L. and O'Neill, S. L. ( 1998). Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. Journal of Bacteriology 180, 23732378.Google Scholar
Breeuwer, J. A. J. ( 1997). Wolbachia and cytoplasmic incompatibility in the spider mites Tetranychus urticae and T. turkestani. Heredity 79, 4147.CrossRefGoogle Scholar
Breeuwer, J. A. J. and Werren, J. H. ( 1990). Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature, London 346, 558560.CrossRefGoogle Scholar
Breeuwer, J. A. J. and Werren, J. H. ( 1993). Cytoplasmic incompatibility and bacterial density in Nasonia vitripennis. Genetics 135, 565574.Google Scholar
Clancy, D. J. and Hoffmann, A. A. ( 1998). Environmental effects on cytoplasmic incompatibility and bacterial load in Wolbachia-infected Drosophila simulans. Entomologia Experimentalis and Applicata 86, 1324.CrossRefGoogle Scholar
David, J. R., Allemand, R., Van Heerewege, J. and Cohet, Y. ( 1983). Ecophysiology: abiotic factors. In The Genetics and Biology of Drosophila ( ed. Ashburner, M., Carson, H. L. and Thompson J. N.), pp. 106170. Academic Press, London.
Douglas, A. E. ( 1994). Symbiotic Interactions. Oxford University Press, Oxford.
Fleury, F., Ris, N., Allemand, R., Fouillet, P., Carton, Y. and Boulétreau, M. ( 2004). Ecological and genetic interactions in Drosophila-parasitoids communities: a case study with D. melanogaster, D. simulans and their common Leptopilina parasitoids in south-eastern France. Genetica 120, 181194.Google Scholar
Frank, S. A. ( 1998). Dynamics of cytoplasmic incompatibility with multiple Wolbachia infections. Journal of Theoretical Biology 192, 213218.CrossRefGoogle Scholar
Gavotte, L., Vavre, F., Henri, H., Ravallec, M., Stouthamer, R. and Boulétreau, M. ( 2004). Diversity, distribution and specificity of WO phage infection in Wolbachia of four insect species. Insect Molecular Biology 13, 147153.CrossRefGoogle Scholar
Greub, G., La Scola, B. and Raoult, D. ( 2003). Parachlamydia acanthamoeba is endosymbiotic or lytic for Acanthamoeba polyphaga depending on the incubation temperature. Annals of the New York Academy of Sciences 990, 628634.CrossRefGoogle Scholar
Hurst, G. D. D., Jiggins, F. M. and Robinson, S. J. W. ( 2001). What causes inefficient transmission of male-killing Wolbachia in Drosophila? Heredity 87, 220226.Google Scholar
Hurst, G. D. D., Johnson, A. P., von der Schulenburg, J. H. G. and Fuyama, Y. ( 2000). Male-killing Wolbachia in Drosophila: a temperature-sensitive trait with a threshold bacterial density. Genetics 156, 699709.Google Scholar
Ikeda, T., Ishikawa, H. and Sasaki, T. ( 2003). Infection density of Wolbachia and level of cytoplasmic incompatibility in the Mediterranean flour moth, Ephestia kuehniella. Journal of Invertebrate Pathology 84, 15.CrossRefGoogle Scholar
Ishikawa, H. ( 2003). Insect symbiosis: an introduction. In Insect Symbiosis ( ed. Bourtzis, K. and Mille, T. A.), pp. 122. CRC Press, Boca Raton, Florida, USA.CrossRef
Johanowicz, D. L. and Hoy, M. A. ( 1998). Experimental induction and termination of non-reciprocal reproductive incompatibilities in a parahaploid mite. Entomologia Experiantia and Applicata 87, 5158.CrossRefGoogle Scholar
McGraw, E. A., Merritt, D. J., Droller, J. N. and O'Neill, S. L. ( 2002). Wolbachia density and virulence attenuation after transfer into a novel host. Proceedings of the National Academy of Sciences, USA 99, 29182923.CrossRefGoogle Scholar
Mouton, L., Dedeine, F., Henri, H., Boulétreau, M., Profizi, N. and Vavre, F. ( 2004). Virulence, multiple infections and regulation of symbiotic population in the Wolbachia-Asobara tabida symbiosis. Genetics 168, 181189.CrossRefGoogle Scholar
Mouton, L., Henri, H., Boulétreau, M. and Vavre, F. ( 2005). Multiple infections and diversity of cytoplasmic incompatibility in a haplodiploid species. Heredity 94, 187192.CrossRefGoogle Scholar
Mouton, L., Henri, H., Boulétreau, M. and Vavre, F. ( 2003). Strain-specific regulation of intracellular Wolbachia density in multiply infected insects. Molecular Ecology 12, 34593465.CrossRefGoogle Scholar
Nishiguchi, M. K. ( 2000). Temperature affects species distribution in symbiotic populations of Vibrio spp. Applied and Environmental Microbiology 66, 35503555.CrossRefGoogle Scholar
Noda, H., Miyoshi, T., Zhang, Q., Watanabe, K., Deng, K. and Hoshizaki, S. ( 2001). Wolbachia infection shared among planthoppers (Homoptera: Delphacidae) and their endoparasite (Strepsiptera: Elenchidae): a probable case of interspecies transmission. Molecular Ecology 10, 21012106.CrossRefGoogle Scholar
Perrot-Minot, M.-J., Guo, L. R. and Werren, J. H. ( 1996). Single and double infections with Wolbachia in the parasitic wasp Nasonia vitripennis: effects on compatibility. Genetics 143, 961972.Google Scholar
Perrot-Minnot, M.-J. and Werren, J. H. ( 1999). Wolbachia infection and incompatibility dynamics in experimental selection lines. Journal of Evolutionary Biology 12, 272282.CrossRefGoogle Scholar
Poinsot, D., Bourtzis, K., Markakis, G., Savakis, C. and Merçot, H. ( 1998). Wolbachia transfer from Drosophila melanogaster into D. simulans: host effect and cytoplasmic incompatibility relationships. Genetics 150, 227237.Google Scholar
Ris, N., Allemand, R., Fouillet, P. and Fleury, F. ( 2004). The joint effect of temperature and host species induce complex genotype-by-environment interactions in the larval parasitoid of Drosophila, Leptopilina heterotoma (Hymenoptera: Figitidae). Oïkos 106, 451456.Google Scholar
Sinkins, S. P., Braig, H. R. and O'Neill, S. L. ( 1995). Wolbachia superinfections and the expression of cytoplasmic incompatibility. Proceedings of the Royal Society of London, B 261, 325330.CrossRefGoogle Scholar
Stouthamer, R., Breeuwer, J. A. J. and Hurst, G. D. D. ( 1999). Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annual Revue of Microbiology 53, 71102.CrossRefGoogle Scholar
Stouthamer, R., Luck, R. F. and Hamilton, W. D. ( 1990). Antibiotics cause parthenogenetic trichograms to revert to sex. Proceedings of the Royal Society of London, B 87, 24242427.Google Scholar
Thomas, M. B. and Blanford, S. ( 2003). Thermal biology in insect-parasite interactions. Trends in Ecology and Evolution 18, 344350.CrossRefGoogle Scholar
Van Opijnen, T. and Breeuwer, J. A. ( 1999). High temperatures eliminate Wolbachia, a cytoplasmic incompatibility inducing endosymbiont, from the two-spotted spider mite. Experimental and Applied Acarology 23, 871881.CrossRefGoogle Scholar
Vavre, F., Dedeine, F., Quillon, M., Fouillet, P., Fleury, F. and Boulétreau, M. ( 2001). Within-species diversity of Wolbachia-induced cytoplasmic incompatibilities in haplodiploid insects. Evolution 55, 17101714.CrossRefGoogle Scholar
Vavre, F., Fleury, F., Lepetit, D., Fouillet, P. and Boulétreau, M. ( 1999). Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoïd associations. Molecular Biology and Evolution 16, 17111723.CrossRefGoogle Scholar
Veneti, Z., Clark, M. E., Zabalou, S., Karr, T. L., Savakis, C. and Bourtzis, K. ( 2003). Cytoplasmic incompatibility and sperm cyst infection in different Drosophila-Wolbachia associations. Genetics 164, 545552.Google Scholar