Comparing constitutive and induced costs of symbiont-conferred resistance to parasitoids in aphids

Ecology and Evolution

Volumn 3, Issue 3, 2013, Pages 706-713

  Vorburger, Christoph ^a,b   Ganesanandamoorthy, Pravin ^b   Kwiatkowski, Marek ^a,b  

^a ETH ZURICH   (Switzerland)

^b SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

Author keywords

Aphis fabae; Hamiltonella defensa; Lysiphlebus fabarum; Parasitoid; Resistance; Symbiosis

Indexed keywords

EID: 84880698116     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.491     Document Type: Article

References (43)

1. Armitage, S.A.O., J.J.W. Thompson, J. Rolff, and M.T. Siva-Jothy 2003. Examining costs of induced and constitutive immune investment in Tenebrio molitor. J. Evol. Biol., 16:1038-1044.
2. Beckage, N.E., and D.B. Gelman 2004. Wasp parasitoid disruption of host development: implications for new biologically based strategies for insect control. Annu. Rev. Entomol., 49:299-330.
3. Belshaw, R., D.L.J. Quicke, W. Völkl, and H.C.J. Godfray 1999. Molecular markers indicate rare sex in a predominantly asexual parasitoid wasp. Evolution, 53:1189-1199.
4. Bensadia, F., S. Boudreault, J.F. Guay, D. Michaud, and C. Cloutier 2006. Aphid clonal resistance to a parasitoid fails under heat stress. J. Insect Physiol., 52:146-157.
5. Blackman, R.L., and V.F. Eastop 2000. Aphids on the World's Crops: An Identification and Information Guide, 2nd edn. John Wiley and Sons, Chichester.
6. von Burg, S., J. Ferrari, C.B. Müller, and C. Vorburger 2008. Genetic variation and covariation of susceptibility to parasitoids in the aphid Myzus persicae - no evidence for trade-offs. Proc R. Soc. B Biol. Sci., 275:1089-1094.
7. Chen, D.Q., and A.H. Purcell 1997. Occurrence and transmission of facultative endosymbionts in aphids. Curr. Microbiol., 34:220-225.
8. Dion, E., S.E. Polin, J.C. Simon, and Y. Outreman 2011a. Symbiont infection affects aphid defensive behaviours. Biol. Lett., 7:743-746.
9. Dion, E., F. Zele, J.C. Simon, and Y. Outreman 2011b. Rapid evolution of parasitoids when faced with the symbiont-mediated resistance of their hosts. J. Evol. Biol., 24:741-750.
10. Ferrari, J., J.A. West, S. Via, and H.C.J. Godfray 2012. Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex. Evolution, 66:375-390.
11. Gwynn, D.M., A. Callaghan, J. Gorham, K.F.A. Walters, and M.D.E. Fellowes 2005. Resistance is costly: trade-offs between immunity, fecundity and survival in the pea aphid. Proc. R. Soc. London Ser. B Biol. Sci., 272:1803-1808.
12. Hedges, L.M., J.C. Brownlie, S.L. O'Neill, and K.N. Johnson 2008. Wolbachia and virus protection in insects. Science, 322:702-702.
13. Henter, H.J., and S. Via 1995. The potential for coevolution in a host-parasitoid system. I. Genetic variation within an aphid population in susceptibility to a parasitic wasp. Evolution, 49:427-438.
14. Jaenike, J., R. Unckless, S.N. Cockburn, L.M. Boelio, and S.J. Perlman 2010. Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science, 329:212-215.
15. Kraaijeveld, A.R., and H.C.J. Godfray 1997. Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature, 389:278-280.
16. Kraaijeveld, A.R., J. Ferrari, and H.C.J. Godfray 2002. Costs of resistance in insect-parasite and insect-parasitoid interactions. Parasitology, 125:S71-S82.
17. Kwiatkowski, M., and C. Vorburger 2012. Modeling the ecology of symbiont-mediated protection against parasites. Am. Nat., 179:595-605.
18. Moret, Y., and P. Schmid-Hempel 2000. Survival for immunity: the price of immune system activation for bumblebee workers. Science, 290:1166-1168.
19. Oliver, K.M., J.A. Russell, N.A. Moran, and M.S. Hunter 2003. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Natl Acad. Sci. USA, 100:1803-1807.
20. Oliver, K.M., N.A. Moran, and M.S. Hunter 2005. Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc. Natl Acad. Sci. USA, 102:12795-12800.
21. Oliver, K.M., N.A. Moran, and M.S. Hunter 2006. Costs and benefits of a superinfection of facultative symbionts in aphids. Proc. R. Soc. B Biol. Sci., 273:1273-1280.
22. Oliver, K.M., J. Campos, N.A. Moran, and M.S. Hunter 2008. Population dynamics of defensive symbionts in aphids. Proc. R. Soc. B Biol. Sci., 275:293-299.
23. Oliver, K.M., P.H. Degnan, M.S. Hunter, and N.A. Moran 2009. Bacteriophages encode factors required for protection in a symbiotic mutualism. Science, 325:992-994.
24. Oliver, K.M., K. Noge, E.M. Huang, J.M. Campos, J.X. Becerra, and M.S. Hunter 2012. Parasitic wasp responses to symbiont-based defense in aphids. BMC Biol., 10:11.
25. Outreman, Y., A. Ralec Le, M. Plantegenest, B. Chaubet, and J.S. Pierre 2001. Superparasitism limitation in an aphid parasitoid: cornicle secretion avoidance and host discrimination ability. J. Insect Physiol., 47:339-348.
26. R Development Core Team. 2011. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org.
27. Rouchet, R., and C. Vorburger 2012. Strong specificity in the interaction between parasitoids and symbiont-protected hosts. J. Evol. Biol., 25:2369-2375.
28. Sandrock, C., and C. Vorburger 2011. Single-locus recessive inheritance of asexual reproduction in a parasitoid wasp. Curr. Biol., 21:433-437.
29. Sandrock, C., A. Gouskov, and C. Vorburger 2010. Ample genetic variation but no evidence for genotype specificity in an all-parthenogenetic host-parasitoid interaction. J. Evol. Biol., 23:578-585.
30. Schmid, M., R. Sieber, Y.S. Zimmermann, and C. Vorburger 2012. Development, specificity and sublethal effects of symbiont-conferred resistance to parasitoids in aphids. Funct. Ecol., 26:207-215.
31. Schmid-Hempel, P. 2003. Variation in immune defence as a question of evolutionary ecology. Proc. R. Soc. B Biol. Sci., 270:357-366.
32. Schmid-Hempel, P. 2005. Evolutionary ecology of insect immune defenses. Annu. Rev. Entomol., 50:529-551.
33. Schmid-Hempel, P. 2011. Evolutionary Parasitology. Oxford University Press, Oxford, New York.
34. Sheldon, B.C., and S. Verhulst 1996. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol., 11:317-321.
35. Simon, J.C., S. Carre, M. Boutin, N. Prunier-Leterme, B. Sabater-Munoz, A. Latorre, et al. 2003. Host-based divergence in populations of the pea aphid: insights from nuclear markers and the prevalence of facultative symbionts. Proc. R. Soc. B Biol. Sci., 270:1703-1712.
36. Simon, J.C., S. Boutin, T. Tsuchida, R. Koga, J.F. Gallic Le, A. Frantz, et al. 2011. Facultative symbiont infections affect aphid reproduction. PLoS ONE, 6:e21831.
37. Starý, P. 1999. Biology and distribution of microbe-associated thelytokous populations of aphid parasitoids (Hym., Braconidae, Aphidiinae). J. Appl. Entomol., 123:231-235.
38. Starý, P. 2006. Aphid Parasitoids of the Czech Republic (Hymenoptera: Braconidae, Aphidiinae). Academia, Praha.
39. Teixeira, L., A. Ferreira, and M. Ashburner 2008. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol., 6:2753-2763.
40. Vorburger, C., and A. Gouskov 2011. Only helpful when required: a longevity cost of harbouring defensive symbionts. J. Evol. Biol., 24:1611-1617.
41. Vorburger, C., S.E. Gegenschatz, G. Ranieri, and P. Rodriguez 2008. Limited scope for maternal effects in aphid defence against parasitoids. Ecol. Entomol., 33:189-196.
42. Vorburger, C., C. Sandrock, A. Gouskov, L.E. Castañeda, and J. Ferrari 2009. Genotypic variation and the role of defensive endosymbionts in an all-parthenogenetic host-parasitoid interaction. Evolution, 63:1439-1450.
43. Vorburger, C., B. Eugster, J. Villiger, and C. Wimmer 2010. Host genotype affects the relative success of competing lines of aphid parasitoids under superparasitism. Ecol. Entomol., 35:77-83.