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Resource depletion in Aedes aegypti mosquitoes infected by the microsporidia Vavraia culicis

Published online by Cambridge University Press:  18 July 2007

A. RIVERO ,
P. AGNEW ,
S. BEDHOMME ,
C. SIDOBRE  and
Y. MICHALAKIS
A. RIVERO*
Affiliation:
Génetique et Evolution des Maladies Infectieuses (CNRS-IRD UMR 2724), 911 Avenue Agropolis, Montpellier 34394, France Department of Evolutionary Ecology, Consejo Superior de Investigaciones Científicas (CSIC), José Gutiérrez Abascal 2, 28006 Madrid, Spain
P. AGNEW
Affiliation:
Génetique et Evolution des Maladies Infectieuses (CNRS-IRD UMR 2724), 911 Avenue Agropolis, Montpellier 34394, France
S. BEDHOMME
Affiliation:
Génetique et Evolution des Maladies Infectieuses (CNRS-IRD UMR 2724), 911 Avenue Agropolis, Montpellier 34394, France
C. SIDOBRE
Affiliation:
Génetique et Evolution des Maladies Infectieuses (CNRS-IRD UMR 2724), 911 Avenue Agropolis, Montpellier 34394, France
Y. MICHALAKIS
Affiliation:
Génetique et Evolution des Maladies Infectieuses (CNRS-IRD UMR 2724), 911 Avenue Agropolis, Montpellier 34394, France
*
*Corresponding author: Génetique et Evolution des Maladies Infectieuses (CNRS-IRD UMR 2724), 911 Avenue Agropolis, Montpellier 34394, France. Tel: +34 914 111 328. Fax: +34 915 645 078. E-mail: [email protected]
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Summary

Parasitic infection is often associated with changes in host life-history traits, such as host development. Many of these life-history changes are ultimately thought to be the result of a depletion or reallocation of the host's resources driven either by the host (to minimize the effects of infection) or by the parasite (to maximize its growth rate). In this paper we investigate the energetic budget of Aedes aegypti mosquito larvae infected by Vavraia culicis, a microsporidian parasite that transmits horizontally between larvae, and which has been previously shown to reduce the probability of pupation of its host. Our results show that infected larvae have significantly less lipids, sugars and glycogen than uninfected larvae. These differences in resources were not due to differences in larval energy intake (feeding rate) or expenditure (metabolic rate). We conclude that the lower energetic resources of infected mosquitoes are the result of the high metabolic demands that microsporidian parasites impose on their hosts. Given the fitness advantages for the parasite of maintaining the host in a larval stage, we discuss whether resource depletion may also be a parasite mechanism to prevent the pupation of the larvae and thus maximize its own transmission.

Keywords

energy budgetpupationmetabolic ratefeeding rateimmunity
Type
Research Article
Information
Parasitology , Volume 134 , Issue 10 , September 2007 , pp. 1355 - 1362
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Agnew, P., Bedhomme, S., Haussy, C. and Michalakis, Y. (1999). Age and size at maturity of the mosquito Culex pipiens infected by the microsporidian parasite Vavraia culicis. Proceedings of the Royal Society of London, B 266, 947–952.CrossRefGoogle Scholar
Agnew, P., Hide, M., Sidobre, C. and Michalakis, Y. (2002). A minimalist approach to the effects of density-dependent competition on insect life-history traits. Ecological Entomology 27, 396–402.CrossRefGoogle Scholar
Ahmed, A. M., Baggot, S. L., Maingon, R. and Hurd, H. (2002). The costs of mounting an immune response are reflected in the reproductive fitness of the mosquito Anopheles gambiae. Oikos 97, 371–377.CrossRefGoogle Scholar
Armitage, S. A. O., Thompson, J. J. W., Rolff, J. and Siva-Jothy, M. T. (2003). Examining costs of induced and constitutive immune investment in Tenebrio molitor. Journal of Evolutionary Biology 16, 1038–1044.CrossRefGoogle ScholarPubMed
Ballabeni, P. (1995). Parasite-induced gigantism in a snail: A host adaptation? Functional Ecology 9, 887–893.CrossRefGoogle Scholar
Beckage, N. E. (1997). New insights: how parasites and pathogens alter the endocrine physiology and development of insect hosts. In Parasites and Pathogens: Effects of Host Hormones and Behaviour (ed. Beckage, N. E.), pp. 3–36. Chapman and Hall, New York.CrossRefGoogle Scholar
Becnel, J. J. and Andreadis, T. G. (1999). Microsporidia in insects. In Microsporidia and Microsporidiosis (ed. Wittner, M. and Weiss, L. M.), pp. 447–501. American Society for Microbiology, Washington D.C.Google Scholar
Bedhomme, S., Agnew, P., Sidobre, C. and Michalakis, Y. (2004). Virulence reaction norms across a food gradient. Proceedings of the Royal Society of London, B 271, 739–744.CrossRefGoogle ScholarPubMed
Biron, D. G., Agnew, P., Marche, L., Renault, L., Sidobre, C. and Michalakis, Y. (2005). Proteome of Aedes aegypti larvae in response to infection by the intracellular parasite Vavraia culicis. International Journal for Parasitology 35, 1385–1397.Google ScholarPubMed
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.Google ScholarPubMed
Chadwick, W. and Little, T. J. (2005). A parasite-mediated life-history shift in Daphnia magna. Proceedings of the Royal Society of London, B 272, 505–509.Google ScholarPubMed
Chambers, G. M. and Klowden, M. J. (1990). Correlation of nutritional reserves with a critical weight for pupation in larval Aedes aegypti mosquitos. Journal of the American Mosquito Control Association 6, 394–399.Google Scholar
Cheon, H. M., Shin, S. W., Bian, G. W., Park, J. H. and Raikhel, A. S. (2006). Regulation of lipid metabolism genes, lipid carrier protein lipophorin, and its receptor during immune challenge in the mosquito Aedes aegypti. Journal of Biological Chemistry 281, 8426–8435.CrossRefGoogle ScholarPubMed
Clements, A. N. (1992). The Biology of Mosquitoes: Development, Nutrition and Reproduction. Chapman and Hall, London.CrossRefGoogle Scholar
Crawley, M. J. (1993). GLIM for Ecologists. Blackwell, Oxford.Google Scholar
Davidowitz, G., D'Amico, L. J. and Nijhout, H. F. (2003). Critical weight in the development of insect body size. Evolution and Development 5, 188–197.Google ScholarPubMed
Ebert, D., Carius, H. J., Little, T. and Decaestecker, E. (2004). The evolution of virulence when parasites cause host castration and gigantism. American Naturalist 164 (Suppl.), S19–S32.CrossRefGoogle ScholarPubMed
El Alaoui, H., Bata, J., Bauchart, D., Dore, J. C. and Vivares, C. P. (2001). Lipids of three microsporidian species and multivariate analysis of the host-parasite relationship. Journal of Parasitology 87, 554–559.Google ScholarPubMed
Freitak, D., Ots, I., Vanatoa, A. and Horak, P. (2003). Immune response is energetically costly in white cabbage butterfly pupae. Proceedings of the Royal Society of London, B 270 (Suppl.), S220–S222.CrossRefGoogle ScholarPubMed
Fukuda, T., Willis, O. R. and Barnard, D. R. (1997). Parasites of the Asian tiger mosquito and other container-inhabiting mosquitoes (Diptera: Culicidae) in northcentral Florida. Journal of Medical Entomology 34, 226–233.CrossRefGoogle ScholarPubMed
Guiguère, L. A. (1981). Food assimilation efficiency as a function of temperature and meal size in larvae of Chaborus trivittatus (Diptera: Chaoboridae). Journal of Animal Ecology 50, 103–109.CrossRefGoogle Scholar
Hoch, G., Schafellner, C., Henn, M. W. and Schopf, A. (2002). Alterations in carbohydrate and fatty acid levels of Lymantria dispar larvae caused by a microsporidian infection and potential adverse effects on a co-occurring endoparasitoid, Glyptapanteles liparidis. Archives of Insect Biochemistry and Physiology 50, 109–120.CrossRefGoogle ScholarPubMed
Hurd, H. (1998). Parasite manipulation of insect reproduction: who benefits? Parasitology 116 (Suppl.), S13–S21.CrossRefGoogle ScholarPubMed
Jokela, J., Uotila, L. and Taskinen, J. (1993). Effect of the castrating trematode parasite Rhipidocotyle fennica on energy allocation of fresh-water clam Anodonta piscinalis. Functional Ecology 7, 332–338.Google Scholar
Jones, D., Jones, G. and Bhaskaran, G. (1981). Dietary sugars, hemolymph trehalose levels, and supernumerary molting of Manduca sexta larvae. Physiological Zoology 54, 260–266.CrossRefGoogle Scholar
Keas, B. E. and Esch, G. W. (1997). The effect of diet and reproductive maturity on the growth and reproduction of Helisoma anceps (Pulmonata) infected by Halipegus occidualis (Trematoda). Journal of Parasitology 83, 96–104.CrossRefGoogle ScholarPubMed
Kelly, J. F., Anthony, D. W. and Dillard, C. R. (1981). A laboratory evaluation of the microsporidian Vavraia culicis as an agent for mosquito control. Journal of Invertebrate Pathology 37, 117–122.CrossRefGoogle Scholar
Kirkwood, T. B. L. (1977). Evolution of aging. Nature, London 270, 301–304.Google Scholar
Koella, J. C. and Sorensen, F. L. (2002). Effect of adult nutrition on the melanization immune response of the malaria vector Anopheles stephensi. Medical and Veterinary Entomology 16, 316–320.CrossRefGoogle ScholarPubMed
Lan, Q. and Grier, C. A. (2004). Critical period for pupal commitment in the yellow fever mosquito, Aedes aegypti. Journal of Insect Physiology 50, 667–676.CrossRefGoogle ScholarPubMed
MacWhinnie, S. G. B., Allee, J. P., Nelson, C. A., Riddiford, L. M., Truman, J. W. and Champlin, D. T. (2005). The role of nutrition in creation of the eye imaginal disc and initiation of metamorphosis in Manduca sexta. Developmental Biology 285, 285–297.CrossRefGoogle ScholarPubMed
Minchella, D. J. (1985). Host life history variation in response to parasitism. Parasitology 90, 205–216.CrossRefGoogle Scholar
Moret, Y. and Schmid-Hempel, P. (2000). Survival for immunity: activation of immune system has a price for bumblebee workers. Science 290, 1166–1168.CrossRefGoogle Scholar
Nijhout, H. F. (1999). Hormonal control in larval development and evolution in insects. In The Origin and Evolution of Larval Forms (ed. Hall, B. K. and Wake, M. H.), pp. 217–255. Academic Press, San Diego.CrossRefGoogle Scholar
O'Reilly, D. R. (1995). Baculovirus-encoded ecdysteroid UDP-glucosyltransferases. Insect Biochemistry and Molecular Biology 25, 541–550.CrossRefGoogle Scholar
Rivero, A. and Ferguson, H. (2003). The energetic budget of Anopheles stephensi infected by Plasmodium chabaudi: Is energy depletion a mechanism for virulence? Proceedings of the Royal Society of London, B 270, 1365–1371.CrossRefGoogle ScholarPubMed
Schultz, E. T., Topper, M. and Heins, D. C. (2006). Decreased reproductive investment of female threespine stickleback Gastrosteus aculeatus infected with the cestode Schistocephalus solidus: parasite adaptation, host adaptation or side effect? Oikos 114, 303–310.CrossRefGoogle Scholar
Schwartz, A. and Koella, J. C. (2004). The cost of immunity in the yellow fever mosquito, Aedes aegypti depends on immune activation. Journal of Evolutionary Biology 17, 834–840.CrossRefGoogle ScholarPubMed
Siva-Jothy, M. T. and Thompson, J. J. W. (2002). Short-term nutrient deprivation affects immune function. Physiological Entomology 27, 206–212.CrossRefGoogle Scholar
Sokal, R. R. and Rohlf, F. J. (1995). Biometry. W. H. Freeman and Company, New York.Google Scholar
Sorensen, R. E. and Minchella, D. J. (2001). Snail-trematode life history interactions: past trends and future directions. Parasitology 123 (Suppl.), S3–S18.Google ScholarPubMed
Sumanochitrapon, W., Strickman, D., Sithiprasasna, R., Kittayapong, P. and Innis, B. L. (1998). Effect of size and geographic origin of Aedes aegypti on oral infection with Dengue-2 virus. American Journal of Tropical Medicine and Hygiene 58, 283–286.CrossRefGoogle ScholarPubMed
Timmermann, S. E. and Briegel, H. (1999). Larval growth and biosynthesis of reserves in mosquitoes. Journal of Insect Physiology 45, 461–470.CrossRefGoogle ScholarPubMed
Tolmasky, D. S., Rabossi, A. and Quesada-Allue, L. A. (2001). Synthesis and mobilization of glycogen during metamorphosis of the medfly Ceratitis capitata. Archives of Biochemistry and Biophysics 392, 38–47.CrossRefGoogle ScholarPubMed
Undeen, A. H. and Vander Meer, R. K. (1999). Microsporidian intrasporal sugars and their role in germination. Journal of Invertebrate Pathology 73, 294–302.CrossRefGoogle ScholarPubMed
van Handel, E. (1965). The obese mosquito. Journal of Physiology 181, 478–486.CrossRefGoogle ScholarPubMed
van Handel, E. (1985 b). Rapid determination of glycogen and sugars in mosquitoes. Journal of the American Mosquito Control Association 1, 299–301.Google ScholarPubMed
van Handel, E. (1985 a). Rapid determination of total lipids in mosquitoes. Journal of the American Mosquito Control Association 1, 302–304.Google ScholarPubMed
van Handel, E. (1988). Assay of lipids, glycogen and sugars in individual mosquitoes: correlations with wing length in field-collected Aedes vexans. Journal of the American Mosquito Control Association 4, 549–550.Google ScholarPubMed
Weidner, E., Findley, A. M., Dolgikh, V. and Sokolova, J. (1999). Microsporidian biochemistry and physiology. In Microsporidia and Microsporidiosis (ed. Wittner, M. and Weiss, L. M.), pp. 172–195. American Society for Microbiology, Washington D.C.Google Scholar
Xue, R. D., Edman, J. D. and Scott, T. W. (1995). Age and body-size effects on blood meal size and multiple blood feeding by Aedes aegypti (Diptera, Culicidae). Journal of Medical Entomology 32, 471–474.CrossRefGoogle ScholarPubMed
Yearsley, J. M., Kyriazakis, A., Gordon, I. J., Johnston, S. L., Speakman, J. R., Tolkamp, B. J. and Illius, A. W. (2005). A life history model of somatic damage associated with resource acquisition: damage protection or prevention? Journal of Theoretical Biology 235, 305–317.CrossRefGoogle ScholarPubMed