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Cost induced by viral particles manipulating superparasitism behaviour in the parasitoid Leptopilina boulardi

Published online by Cambridge University Press:  18 April 2005

J. VARALDI ,
M. BOULÉTREAU  and
F. FLEURY
J. VARALDI
Affiliation:
Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558, Université Claude Bernard LYON 1, 43 Boulevard du 11 novembre 1918, 69622 Villeurbanne Cedex, France
M. BOULÉTREAU
Affiliation:
Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558, Université Claude Bernard LYON 1, 43 Boulevard du 11 novembre 1918, 69622 Villeurbanne Cedex, France
F. FLEURY
Affiliation:
Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558, Université Claude Bernard LYON 1, 43 Boulevard du 11 novembre 1918, 69622 Villeurbanne Cedex, France
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Abstract

Vertically transmitted symbionts can be maintained in a host population only if they do not reduce host fitness, unless they compensate by manipulation of their host's reproduction or have alternative mode of transmission. In Leptopilina boulardi, a parasitoid of Drosophila larvae, some females are infected by viral particles showing both maternal and horizontal transmission. Horizontal transmission occurs when larvae from infected and uninfected individuals of L. boulardi compete in the same host. This situation is facilitated by the increasing tendency to accept already parasitized hosts that viral infection induces in L. boulardi females. Estimation of the adaptive significance of this behavioural modification requires measuring the effect of viral presence on other parasitoid physiological features. Here, we show that viral infection in females imposes no cost on adult survival, a low cost on developmental rate and tibia length, and leads to a strong reduction of locomotor activity. Surprisingly, infected females show higher egg load which could be accounted for by a redirection of energy allocation to egg production. The high intensity of superparasitism in infected females induced a dramatic decrease in pre-imaginal survival of the parasitoid's offspring, representing a potential indirect cost of infection. Low overall pathogeny induced by viral particles appears to be well suited to both transmission modes, both of them requiring females ability to locate and (super)parasitize hosts.

Keywords

superparasitismvirusparasitoidcost of infectionmanipulation of host behaviourLeptopilinaparasite
Type
Research Article
Information
Parasitology , Volume 131 , Issue 2 , August 2005 , pp. 161 - 168
Copyright
2005 Cambridge University Press

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References

REFERENCES

ALLEMAND, R., POMPANON, F., FLEURY, F., FOUILLET, P. & BOULÉTREAU, M. ( 1994). Behavioural circadian rhythms measured in real-time by automatic image analysis: application in parasitoid insects. Physiological Entomology 19, 1–8.CrossRefGoogle Scholar
BOULÉTREAU, M., CHASSAIN, C. & FOUILLET, P. ( 1991). Mutual interference and spatial distribution of infestations in two sympatric Trichogramma species: T. brassicae and T. cacoeciae. Biologicol Control 1, 176–182.Google Scholar
BIGOT, Y., RABOUILLE, A., DOURY, G., SIZARET, P. Y., DELBOST, F., HAMELIN, M. H. & PERIQUET, G. ( 1997). Biological and molecular features of the relationships between Diadromus pulchellus ascovirus, a parasitoid hymenopteran wasp (Diadromus pulchellus) and its lepidopteran host, Acrolepiopsis assectella. Journal of General Virology 78, 1149–1163.CrossRefGoogle Scholar
BRONSTEIN, J. L. ( 1994). Conditional outcomes in mutualistic interactions. Trends in Ecology and Evolution 9, 214–217.CrossRefGoogle Scholar
BULL, J. J., MOLINEUX, I. J. & RICE, W. R. ( 1991). Selection for benevolence in a host-parasite system. Evolution 45, 875–882.CrossRefGoogle Scholar
DAVID, J. ( 1962). A new medium for rearing Drosophila in axenic condition. Drosophila Information Service 36, 128.Google Scholar
DRIESSEN, G. & HEMERIK, L. ( 1991). Aggregative responses of parasitoids and parasitism in popultions of Drosophila breeding in fungi. OIKOS 61, 96–107.CrossRefGoogle Scholar
DUPAS, S., BREHELIN, M., FREY, F. & CARTON, Y. ( 1996). Immune suppressive virus like particles in a Drosophila parasitoid: significance of their intraspecific morphological variations. Parasitology 113, 207–212.CrossRefGoogle Scholar
EBERT, D. & HERRE, E. A. ( 1996). The evolution of parasitic desease. Parasitology Today 12, 96–101.CrossRefGoogle Scholar
ELLERS, J., SEVENSTER, J. G. & DRIESSEN, G. ( 2000). Egg load evolution in parasitoids. The American Naturalist 156, 650–665.CrossRefGoogle Scholar
FIELD, S. A., KELLER, M. & CALBERT, G. ( 1997). The pay-off from superparasitism in the egg parasitoid Trissolcus basalis, in relation to patch defence. Ecological Entomology 22, 142–149.CrossRefGoogle Scholar
FLEURY, F., VAVRE, F., RIS, N., FOUILLET, P. & BOULÉTREAU, M. ( 2000 a). Physiological cost induced by the maternally-transmitted endosymbiont Wolbachia in the Drosophila parasitoid, Leptopilina heterotoma. Parasitology 121, 493–500.Google Scholar
FLEURY, F., ALLEMAND, R., VAVRE, F., FOUILLET, P. & BOULÉTREAU, M. ( 2000 b). Adaptive significance of a circadian clock: temporal segregation of activities reduces intrinsic competitive inferiority in Drosophila parasitoids, Proceedings of the Royal Society of London, B 265, 1005–1010.Google Scholar
FLEURY, F., RIS, N., ALLEMAND, R., FOUILLET, P., CARTON, Y. & 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, 181–194.Google Scholar
HAMILTON, W. D. ( 1967). Extraordinary sex-ratios. Science 156, 477–488.CrossRefGoogle Scholar
HERRE, E. A. ( 1993). Population structure and the evolution of virulence in nematode parasites of fig wasps. Science 259, 1442–1445.CrossRefGoogle Scholar
HURD, H. ( 2001). Host fecundity reduction: a strategy for damage limitation? Trends in Parasitology 17, 363–367.Google Scholar
HURD, H., WARR, E. & POLWART, A. ( 2001). A parasite that increases host lifespan. Proceedings of the Royal Society of London, B 268, 1749–1753.CrossRefGoogle Scholar
KOELLA, J. & AGNEW, P. ( 1999). A correlated response of a parasite's virulence and life cycle to selection on its host's life cycle. Journal of Evolutionary Biology 12, 70–79.CrossRefGoogle Scholar
LABROSSE, C., CARTON, Y., DUBUFFET, A., DREZEN, J. M. & POIRIE, M. ( 2003). Active suppression of D. melanogaster immune response by long gland products of the parasitic wasp Leptopilina boulardi. Journal of Insect Physiology 49, 513–522.Google Scholar
MESSENGER, S. L., MOLINEUX, I. J. & BULL, J. J. ( 1999). Virulence evolution in a virus obeys a trade-off. Proceedings of the Royal Society of London, B 266, 397–404.CrossRefGoogle Scholar
O'NEILL, S. L., HOFFMANN, A. A. & WERREN, J. H. ( 1997). Influencial Passengers. Inherited Microorganisms and Arthropod Reproduction. Oxford University Press, New York.
VAN ALPHEN, J. J. M. & VISSER, M. E. ( 1990). Superparasitism as an adaptive strategy for insect parasitoids. Annual Revue of Entomology 35, 59–79.CrossRefGoogle Scholar
VAN BAAREN, J., LANDRY, B. L. & BOIVIN, G. ( 1999). Sex allocation and larval competition in a superparasitizing solitary egg parasitoid: competing strategies for an optimal sex ratio. Functional Ecology 13, 166–171.CrossRefGoogle Scholar
VARALDI, J., FOUILLET, P., RAVALLEC, M., LOPEZ-FERBER, M., BOULÉTREAU, M. & FLEURY, F. ( 2003). Infectious behavior in a parasitoid. Science 302, 1930. doi:10·1126/science.1088798.Google Scholar
VAVRE, F., FLEURY, F., VARALDI, J., FOUILLET, P. & BOULÉTREAU, M. ( 2000). Evidence for female mortality in Wolbachia-mediated cytoplasmic incompatibility in haplodiploid insects, epidemiologic and evolutionary consequences. Evolution 54, 191–200.CrossRefGoogle Scholar
VISSER, M. E. ( 1995). The effect of competition on oviposition decisions for Leptopilina heterotoma (Hymenoptera: Eucoilidae). Animal Behaviour 49, 1677–1687.CrossRefGoogle Scholar
VISSER, M. E., LUYCKX, B., NELL, H. W. & BOSKAMP, J. F. ( 1992 a). Adaptive superparasitism in solitary parasitoids: marking of parasitized hosts in relation to the pay-off from superparsitism. Ecological Entomology 17, 76–82.Google Scholar
VISSER, M. E., VAN ALPHEN, J. J. M. & HEMERIK, L. ( 1992 b). Adaptive superparasitism and patch time allocation in solitary parasitoids: an ESS model. Journal of Animal Ecology 61, 93–101.Google Scholar
WERTHEIM, B., SEVENSTER, J. G., EIJS, I. E. & VAN ALPHEN, J. J. M. ( 2000). Species diversity in a micophagous insect community: the case of spatial aggregation vs. resource partitioning. Journal of Animal Ecology 69, 335–351.Google Scholar
WHITFIELD, J. B. & ASGARI, S. ( 2003). Virus or not? Phylogenetics of polydnaviruses and their wasp carriers. Journal of Insect Physiology 49, 397–405.CrossRefGoogle Scholar