Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-30T20:03:31.641Z Has data issue: false hasContentIssue false

Genetic variation in Drosophila melanogaster pathogen susceptibility

Published online by Cambridge University Press:  24 February 2006

M. C. TINSLEY
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK
S. BLANFORD
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK
F. M. JIGGINS
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK

Abstract

Genetic variation in susceptibility to pathogens is a central concern both to evolutionary and medical biologists, and for the implementation of biological control programmes. We have investigated the extent of such variation in Drosophila melanogaster, a major model organism for immunological research. We found that within populations, different Drosophila genotypes show wide-ranging variation in their ability to survive infection with the entomopathogenic fungus Beauveria bassiana. Furthermore, striking divergence in susceptibility has occurred between genotypes from temperate and tropical African locations. We hypothesize that this may have been driven by adaptation to local differences in pathogen exposure or host ecology. Genetic variation within populations may be maintained by temporal or spatial variation in the costs and benefits of pathogen defence. Insect pathogens are employed widely as biological control agents and entomopathogenic fungi are currently being developed for reducing malaria transmission by mosquitoes. Our data highlight the need for concern about resistance evolution to these novel biopesticides in vector populations.

Type
Research Article
Copyright
2006 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Blanford, S., Thomas, M. B., Pugh, C. and Pell, J. K. ( 2003). Temperature checks the Red Queen? Resistance and virulence in a fluctuating environment. Ecology Letters 6, 25.CrossRefGoogle Scholar
Blanford, S., Chan, B. H. K., Jenkins, N., Sim, D., Turner, R. J., Read, A. F. and Thomas, M. B. ( 2005). Fungal pathogen reduces potential for malaria transmission. Science 308, 16381641.CrossRefGoogle Scholar
Brun, G. and Plus, N. ( 1980). The viruses of Drosophila. In The Genetics and Biology of Drosophila ( ed. Ashburner, M. and Wright, T. R. F.), pp. 625702. Academic Press, New York.
Bush, A. O., Fernandez, J. C., Esch, G. W. and Seed, J. R. ( 2001). Parasitism: The Diversity and Ecology of Animal Parasites. Cambridge University Press, Cambridge.
Capy, P., Pla, E. and David, J. R. ( 1993). Phenotypic and genetic variability of morphometrical traits in natural populations of Drosophila melanogaster and Drosophila simulans. 1. Geographic variations. Genetics Selection Evolution 25, 517536.CrossRefGoogle Scholar
Collins, F. H., Sakai, R. K., Vernick, K. D., Paskewitz, S. M., Seeley, D. C., Miller, L. H., Collins, W. E., Campbell, C. C. and Gwadz, R. W. ( 1986). Genetic selection of a Plasmodium-refractory strain of the malaria vector Anopheles gambiae. Science 234, 607610.CrossRefGoogle Scholar
Contamine, D., Petitjean, A. M. and Ashburner, M. ( 1989). Genetic resistance to viral infection: the molecular cloning of a Drosophila gene that restricts infection by the rhabdovirus sigma. Genetics 123, 525533.Google Scholar
David, J. R. and Capy, P. ( 1988). Genetic variation of Drosophila melanogaster natural populations. Trends in Genetics 4, 106111.CrossRefGoogle Scholar
Dupas, S., Carton, Y. and Poirie, M. ( 2003). Genetic dimension of the coevolution of virulence – resistance in Drosophila – parasitoid wasp relationships. Heredity 90, 8489.CrossRefGoogle Scholar
Ebert, D., Zschokke-Rohringer, C. D. and Carius, H. J. ( 1998). Within- and between-population variation for resistance of Daphnia magna to the bacterial endoparasite Pasteuria ramosa. Proceedings of the Royal Society of London, B 265, 21272134.CrossRefGoogle Scholar
Fellowes, M. D. E., Kraaijeveld, A. R. and Godfray, H. C. J. ( 1998). Trade-off associated with selection for increased ability to resist parasitoid attack in Drosophila melanogaster. Proceedings of the Royal Society of London, B 265, 15531558.CrossRefGoogle Scholar
Fellowes, M. D. E., Kraaijeveld, A. R. and Godfray, H. C. J. ( 1999). Cross-resistance following artificial selection for increased defence against parasitoids in Drosophila melanogaster. Evolution 53, 966972.CrossRefGoogle Scholar
Ferrandon, D., Jung, A. C., Criqui, M. C., Lemaitre, B., Uttenweiler-Joseph, S., Michaut, L., Reichhart, J. M. and Hoffmann, J. A. ( 1998). A drosomycin-GFP reporter transgene reveals a local immune response in Drosophila that is not dependent on the toll pathway. EMBO Journal 17, 12171227.CrossRefGoogle Scholar
Ferrari, J., Muller, C. B., Kraaijeveld, A. R. and Godfray, H. C. J. ( 2001). Clonal variation and covariation in aphid resistance to parasitoids and a pathogen. Evolution 55, 18051814.CrossRefGoogle Scholar
Fleuriet, A. ( 1996). Polymorphism of the Drosophila melanogaster – sigma virus system. Journal of Evolutionary Biology 9, 471484.CrossRefGoogle Scholar
Gillespie, J. P., Bailey, A. M., Cobb, B. and Vilcinskas, A. ( 2000). Fungi as elicitors of insect immune responses. Archives of Insect Biochemistry and Physiology 44, 4968.3.0.CO;2-F>CrossRefGoogle Scholar
Goettel, M. S. ( 1992). Fungal agents for biocontrol. In Biological Control of Locusts and Grasshoppers ( ed. Lomer, C. J. and Prior, C.), pp. 122130. CAB International, Wallingford, UK.
Griffitts, J. S. and Aroian, R. V. ( 2005). Many roads to resistance: how invertebrates adapt to Bt toxins. Bioessays 27, 614624.CrossRefGoogle Scholar
Guernier, V., Hochberg, M. E. and Guegan, J. F. O. ( 2004). Ecology drives the worldwide distribution of human diseases. PLoS Biology 2, 740746.CrossRefGoogle Scholar
Haldane, J. B. S. ( 1949). Disease and evolution. La Ricerca Scientifica 19 (Suppl.), S68S76.Google Scholar
Hamilton, W. D. ( 1980). Sex vs. non-sex vs. parasite. Oikos 35, 282290.Google Scholar
Hamilton, W. D. and Zuk, M. ( 1982). Heritable true fitness and bright birds – a role for parasites. Science 218, 384387.CrossRefGoogle Scholar
Henter, H. J. and Via, S. ( 1995). The potential for coevolution in a host-parasitoid system.1. Genetic-variation within an aphid population in susceptibility to a parasitic wasp. Evolution 49, 427438.Google Scholar
Hoffmann, J. A. ( 2003). The immune response of Drosophila. Nature, London 426, 3338.CrossRefGoogle Scholar
James, A. C., Azevedo, R. B. R. and Partridge, L. ( 1995). Cellular basis and developmental timing in a size cline of Drosophila melanogaster. Genetics 140, 659666.Google Scholar
Kauer, M., Zangerl, B., Dieringer, D. and Schlotterer, C. ( 2002). Chromosomal patterns of microsatellite variability contrast sharply in African and non-African populations of Drosophila melanogaster. Genetics 160, 247256.Google Scholar
Kraaijeveld, A. and Van Alphen, J. ( 1995). Geographic variation in encapsulation ability of Drosophila melanogaster larvae and evidence for parasitoid-specific components. Evolutionary Ecology 9, 1017.CrossRefGoogle Scholar
Kraaijeveld, A. R. and Godfray, H. C. J. ( 1997). Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature, London 389, 278280.CrossRefGoogle Scholar
Kraaijeveld, A. R., Ferrari, J. and Godfray, H. C. J. ( 2002). Costs of resistance in insect-parasite and insect-parasitoid interactions. Parasitology 125 (Suppl.), S71S82.CrossRefGoogle Scholar
Lazzaro, B. P., Sceurman, B. K. and Clark, A. G. ( 2004). Genetic basis of natural variation in D. melanogaster antibacterial immunity. Science 303, 18731876.Google Scholar
Leclerc, V. and Reichhart, J. M. ( 2004). The immune response of Drosophila melanogaster. Immunological Reviews 198, 5971.CrossRefGoogle Scholar
Lemaitre, B., Reichhart, J. M. and Hoffmann, J. A. ( 1997). Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proceedings of the National Academy of Sciences, USA 94, 1461414619.CrossRefGoogle Scholar
Lewis, E. B. ( 1960). A new standard food medium. Drosophila Information Service 34, 117118.Google Scholar
Lomer, C. J., Bateman, R. P., Johnson, D. L., Langewald, J. and Thomas, M. ( 2001). Biological control of locusts and grasshoppers. Annual Review of Entomology 46, 667702.CrossRefGoogle Scholar
Meister, M. and Lagueux, M. ( 2003). Drosophila blood cells. Cellular Microbiology 5, 573580.CrossRefGoogle Scholar
Roberts, D. B. and Standen, G. N. ( 1998). The elements of Drosophila biology and genetics. In Drosophila: A Practical Approach ( ed. Roberts, D. B.), pp. 154. Oxford University Press, Oxford.
Scholte, E. J., Knols, B. G. J., Samson, R. A. and Takken, W. ( 2004). Entomopathogenic fungi for mosquito control: a review. Journal of Insect Science 4, 124.Google Scholar
Scholte, E. J., Ng'habi, K., Kihonda, J., Takken, W., Paaijmans, K., Abdulla, S., Killeen, G. F. and Knols, B. G. J. ( 2005). An entomopathogenic fungus for control of adult African malaria mosquitoes. Science 308, 16411642.CrossRefGoogle Scholar
Soderhall, K. and Cerenius, L. ( 1998). Role of the prophenoloxidase-activating system in invertebrate immunity. Current Opinion in Immunology 10, 2328.CrossRefGoogle Scholar
Sultan, R., Stampas, A., Goldberg, M. B. and Baker, N. E. ( 2001). Drug resistance of bacteria commensal with Drosophila melanogaster in laboratory cultures. Drosophila Information Service 84, 175180.Google Scholar
Thomas-Orillard, M., Jeune, B. and Cusset, G. ( 1995). Drosophila-host genetic control of susceptibility to Drosophila C virus. Genetics 140, 12891295.Google Scholar
Torchin, M. E., Lafferty, K. D., Dobson, A. P., Mckenzie, V. J. and Kuris, A. M. ( 2003). Introduced species and their missing parasites. Nature, London 421, 628630.CrossRefGoogle Scholar