An inherited virus influences the coexistence of parasitoid species through behaviour manipulation

Ecology Letters

Volumn 15, Issue 6, 2012, Pages 603-610

  Patot, Sabine ^a,b   Allemand, Roland ^a,b   Fleury, Frédéric ^a,b   Varaldi, Julien ^a,b  

^a UNIVERSITÉ LYON 1   (France)

^b UNIVERSITÉ DE LYON   (France)

Author keywords

Behaviour; Coexistence; Competition; Egg load; Keystone parasite; Manipulation; Parasitoid; Superparasitism; Symbiont; Virus

Indexed keywords

BEHAVIORAL RESPONSE; COEXISTENCE; DENSITY DEPENDENCE; EGG PRODUCTION; EXPERIMENTAL STUDY; FLY; HERITABILITY; HORIZONTAL TRANSMISSION; INTERSPECIFIC COMPETITION; KEYSTONE SPECIES; PARASITOID; PATHOGEN; SUPERPARASITISM; SYMBIONT; VIRUS; WASP;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; COMPETITIVE BEHAVIOR; DROSOPHILA; EGG LAYING; FEMALE; HOST PARASITE INTERACTION; PARASITE LOAD; PARASITOLOGY; PHYSIOLOGY; VIROLOGY; WASP;

ANIMALS; BEHAVIOR, ANIMAL; COMPETITIVE BEHAVIOR; DROSOPHILA; FEMALE; HOST-PARASITE INTERACTIONS; OVIPOSITION; PARASITE LOAD; WASPS;

LEPTOPILINA; LEPTOPILINA BOULARDI; LEPTOPILINA HETEROTOMA;

EID: 84860662013     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/j.1461-0248.2012.01774.x     Document Type: Article

References (50)

1. Allemand, R., Fleury, F., Lemaitre, C. & Boulétreau, M. (1999). Population dynamics and competitive interactions in two species of Leptopilina (Hymenoptera: Figitidae) which parasitize Drosophila in the Rhône valley (S-E France). Ann. Soc. Entomol. Fr., 35, 97-103.
2. Beckage, N.E. & Drezen, J.-M. (2012). Parasitoid Viruses. Symbionts and Pathogens. Academic Press, Amsterdam.
3. Bensadia, F., Boudreault, S., Guay, J.-F., Michaud, D. & Cloutier, C. (2006). Aphid clonal resistance to a parasitoid fails under heat stress. J. Insect Physiol., 52, 146-157.
4. Boulétreau, M. & Fouillet, P. (1982). Variabilité génétique intrapopulation de l'aptitude de Drosophila melanogasterà permettre le développement d'un hyménoptère parasite. C. R. Acad. Sci., 295, 775-778.
5. Dale, C. & Welburn, S.C. (2001). The endosymbionts of tsetse flies: manipulating host-parasite interactions. Int. J. Parasitol., 31, 628-631.
6. Fenton, A. & Brockhurst, M.A. (2008). The role of specialist parasites in structuring host communities. Ecol. Res., 23, 795-804.
7. Ferrari, J. & Vavre, F. (2011). Bacterial symbionts in insects or the story of communities affecting communities. Philos. T. R. Soc. B, 366, 1389-1400.
8. Fleuriet, A. (1981). Comparison of various physiological traits in flies (Drosophila melanogaster) of wild origin, infected or uninfected by the hereditary Rhabdovirus sigma. Arch. Virol., 69, 261-272.
9. Fleury, F., Allemand, R., Vavre, F., Fouillet, P. & Boulétreau, M. (2000). Adaptive significance of a circadian clock: temporal segregation of activities reduces intrinsic competitive inferiority in Drosophila parasitoids. Proc. R. Soc. Lond. B, 267, 1005-1010.
10. 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.
11. Fleury, F., Gibert, P., Ris, N. & Allemand, R. (2009). Ecology and life history evolution of frugivorous Drosophila parasitoids. Adv. Parasitol., 70, 3-44.
12. Gandon, S., Rivero, A. & Varaldi, J. (2006). Superparasitism evolution: adaptation or manipulation? Am. Nat., 167, E1-E22.
13. Hatcher, M.J., Dick, J.T.A. & Dunn, A.M. (2006). How parasites affect interactions between competitors and predators. Ecol. Lett., 9, 1253-1271.
14. Hatcher, M.J., Dick, J.T.A. & Dunn, A.M. (2008). A keystone effect for parasites in intraguild predation? Biol. Lett., 4, 534-537.
15. Hedges, L.M., Brownlie, J.C., O'Neill, S.L. & Johnson, K.N. (2008). Wolbachia and virus protection in insects. Science, 322, 702.
16. Hudson, P. & Greenman, J. (1998). Competition mediated by parasites: biological and theoretical progress. Trends Ecol. Evol., 13, 387-390.
17. Hudson, P.J., Dobson, A.P. & Lafferty, K.D. (2006). Is a healthy ecosystem one that is rich in parasites? Trends Ecol. Evol., 21, 381-385.
18. Jaenike, J., Unckless, R., Cockburn, S.N., Boelio, L.M. & Perlman, S.J. (2010). Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science, 329, 212-215.
19. Kaiser, W., Huguet, E., Casas, J., Commin, C. & Giron, D. (2010). Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts. Proc. R. Soc. Lond. B, 277, 2311-2319.
20. Litchman, E. (2010). Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems. Ecol. Lett., 13, 1560-1572.
21. Mangel, M. (2008). Uncertainty in ecology: a retrospective and prospective. Bull. Br. Ecol. Soc., 39, 25-28.
22. Mertz, D.B., Cawthon, D.A. & Park, T. (1976). An experimental analysis of competitive indeterminacy in Tribolium. Proc. Natl Acad. Sci. USA, 73, 1368-1372.
23. Montllor, C., Maxmen, A. & Purcell, A. (2002). Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol. Entomol., 27, 189-195.
24. Moran, N. & McCutcheon, J. (2008). Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet., 42, 165-190.
25. Moreira, L.A., Iturbe-Ormaetxe, I., Jeffery, J.A., Lu, G., Pyke, A.T., Hedges, L.M. et al. (2009). A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell, 139, 1268-1278.
26. Mouritsen, K.N. & Poulin, R. (2005). Parasites boosts biodiversity and changes animal community structure by trait-mediated indirect effects. Oikos, 108, 344-350.
27. Oliver, K.M., Russell, J.A., Moran, N.A. & Hunter, M.S. (2003). Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Natl Acad. Sci. USA, 100, 1803-1807.
28. Oliver, K.M., Campos, J., Moran, N.A. & Hunter, M.S. (2008). Population dynamics of defensive symbionts in aphids. Proc. R. Soc. Lond. B, 275, 293-299.
29. O'Neill, S.L., Hoffmann, A.A. & Werren, J.H. (1997). Influential Passengers: Inherited Microorganisms and Arthropod Reproduction. Oxford University Press, Oxford.
30. Patot, S., Lepetit, D., Charif, D., Varaldi, J. & Fleury, F. (2009). Molecular detection, penetrance, and transmission of an inherited virus responsible for behavioral manipulation of an insect parasitoid. Appl. Environ. Microbiol., 75, 703-710.
31. Patot, S., Martinez, J., Allemand, R., Gandon, S., Varaldi, J. & Fleury, F. (2010). Prevalence of a virus inducing behavioural manipulation near species range border. Mol. Ecol., 19, 2995-3007.
32. Roossinck, M.J. (2011). The good viruses: viral mutualistic symbioses. Nat. Rev. Microbiol., 9, 99-108.
33. Russell, J.A. & Moran, N.A. (2006). Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc. R. Soc. Lond. B, 273, 603-610.
34. Scarborough, C.L., Ferrari, J. & Godfray, H.C.J. (2005). Aphid protected from pathogen by endosymbiont. Science, 310, 1781.
35. Schall, J. (1992). Parasite-mediated competition in Anolis lizards. Oecologia, 92, 58-64.
36. Scott, J.J., Oh, D.-C., Yuceer, M.C., Klepzig, K.D., Clardy, J. & Currie, C.R. (2008). Bacterial protection of beetle-fungus mutualism. Science, 322, 63.
37. Teixeira, L., Ferreira, A. & Ashburner, M. (2008). The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol., 6, 2753-2763.
38. Thomas, F., Adamo, S. & Moore, J. (2005). Parasitic manipulation: where are we and where should we go? Behav. Process., 68, 185-199.
39. Tsuchida, T., Koga, R. & Fukatsu, T. (2004). Host plant specialization governed by facultative symbiont. Science, 303, 1989.
40. Varaldi, J., Fouillet, P., Ravallec, M., Lopez-Ferber, M., Boulétreau, M. & Fleury, F. (2003). Infectious behavior in a parasitoid. Science, 302, 1930.
41. Varaldi, J., Boulétreau, M. & Fleury, F. (2005a). Cost induced by viral particles manipulating superparasitism behaviour in the parasitoid Leptopilina boulardi. Parasitology, 131, 161-168.
42. Varaldi, J., Fouillet, P., Boulétreau, M. & Fleury, F. (2005b). Superparasitism acceptance and patch-leaving mechanisms in parasitoids: a comparison between two sympatric wasps. Anim. Behav., 69, 1227-1234.
43. Varaldi, J., Gandon, S., Rivero, A., Patot, S. & Fleury, F. (2006a). A newly discovered virus manipulates superparasitism behavior in a parasitoid wasp. In: Insect Symbiosis, Volume 2 (ed. Miller, T.A. & Bourtzis, K.). CRC Press, Boca Raton, FL, pp. 119-139.
44. Varaldi, J., Petit, S., Boulétreau, M. & Fleury, F. (2006b). The virus infecting the parasitoid Leptopilina boulardi exerts a specific action on superparasitism behaviour. Parasitology, 132, 747-756.
45. Varaldi, J., Ravallec, M., Labrosse, C., Lopez-Ferber, M., Boulétreau, M. & Fleury, F. (2006c). Artifical transfer and morphological description of virus particles associated with superparasitism behaviour in a parasitoid wasp. J. Insect Physiol., 52, 1202-1212.
46. Vavre, F., Fleury, F., Lepetit, D., Fouillet, P. & Boulétreau, M. (1999). Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Mol. Biol. Evol., 16, 1711-1723.
47. Werren, J.H., Baldo, L. & Clark, M.E. (2008). Wolbachia: master manipulators of invertebrate biology. Nat. Rev. Microbiol., 6, 741-751.
48. Wood, C.L., Byers, J.E., Cottingham, K.L., Altman, I., Donahue, M.J. & Blakeslee, A.M.H. (2007). Parasites alter community structure. Proc. Natl Acad. Sci. USA, 104, 9335-9339.
49. Xie, J., Vilchez, I. & Mateos, M. (2010). Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma. PLoS ONE, 5, e12149.
50. Yan, G., Stevens, L. & Goodnight, C. (1998). Effects of a tapeworm parasite on the competition of Tribolium beetles. Ecology, 79, 1093-1103.