Immunocompetence increases with larval body size in a phytophagous moth

Physiological Entomology

Volumn 38, Issue 3, 2013, Pages 219-225

  Vogelweith, Fanny ^a   Thiery, Denis ^b,c   Moret, Yannick ^a   Moreau, Jérôme ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b BORDEAUX SCIENCES AGRO   (France)

^c UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Eupoecilia ambiguella; Haemocyte count; Immune challenged larvae; Larval body size; Larval immune defence; Phenoloxidase enzyme cascade

Indexed keywords

BODY SIZE; ENZYME; IMMUNE SYSTEM; IMMUNOCOMPETENCE; LARVA; MOTH; PATHOGEN; VINE;

BACTERIA (MICROORGANISMS); EUPOECILIA AMBIGUELLA; HEXAPODA; LEPIDOPTERA;

EID: 84881551403     PISSN: 03076962     EISSN: 13653032     Source Type: Journal    
DOI: 10.1111/phen.12025     Document Type: Article

References (60)

1. Barnes, A.I. & Siva-Jothy, M.T. (2000) Density-dependent prophylaxis in the mealworm beetle Tenebrio molitor L (Coleoptera: Tenebrionidae): cuticular melanization is an indicator of investment in immunity. Proceedings of the Royal Society of London Series B, Biological Sciences, 267, 177-182.
2. Blumberg, D. (1997) Parasitoid encapsulation as a defense mechanism in the Coccoidea (Homoptera) and its importance in biological control. Biological Control, 8, 225-236.
3. Blumberg, D. & Luck, R.F. (1990) Differences in the rates of superparasitism between two strains of Comperiella bifasciata (Howard) (Hymenoptera: Encyrtidae) parasitizing California red scale (Homoptera: Diapididae): an adaptation to circumvent encapsulation? Annals of the Entomological Society of America, 83, 591-597.
4. Bukovinszky, T., Poelman, E., Gols, R. et al. (2009) Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism. Oecologia, 160, 299-308.
5. Carton, Y., Poirié, M. & Nappi, A.J. (2008) Insect immune resistance to parasitoids. Insect Science, 15, 67-87.
6. Cerenius, L. & Söderhäll, K. (2004) The prophenoloxidase-activating system in invertebrates. Immunological Reviews, 199, 116-126.
7. Cheon, H.M., Shin, S.W., Bian, G. et al. (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.
8. Cornet, S., Biard, C. & Moret, Y. (2009) Variation in immune defence among populations of Gammarus pulex (Crustacea: Amphipoda). Oecologia, 159, 257-269.
9. Delbac, L., Lecharpentier, P. & Thiéry, D. (2010) Larval instars determination for the European grapevine moth (Lepidoptera: Tortricidae) based on the frequency distribution of head capsule widths. Crop Protection, 29, 623-630.
10. Eleftherianos, I. & Revenis, C. (2011) Role and importance of phenoloxidase in insect hemostasis. Journal of Innate Immunity, 3, 28-33.
11. Eleftherianos, I., Baldwin, H., ffrench-Constant, R.H. et al. (2008) Developmental modulation of immunity: changes within the feeding period of the fifth larval stage in the defence reactions of Manduca sexta to infection by Photorhabdus. Journal of Insect Physiology, 54, 309-318.
12. Eslin, P. & Prevost, G. (1998) Hemocyte load and immune resistance to Asobara tabida are correlated in species of the Drosophila melanogaster subgroup. Journal of Insect Physiology, 44, 807-816.
13. Eslin, P., Giordanengo, P., Fourdrain, Y. et al. (1996) Avoidance of encapsulation in the absence of VLP by a braconid parasitoid of Drosophila larvae: an ultrastructural study. Canadian Journal of Zoology, 74, 2193-2198.
14. Fuentes-Contreras, J.E., Powell, W., Wadhams, L.J. et al. (1996) Influence of wheat and oat cultivars on the development of the cereal aphid parasitoid Aphidius rhopalosiphi and the generalist aphid parasitoid Ephedrus plagiator. Annals of Applied Biology, 128, 181-187.
15. Glazier, D.S. (2005) Beyond the '3/4-power law': variation in the intra- and interspecific scaling of metabolic rate in animals. Biological Reviews, 80, 611-662.
16. Godin, J., Maltais, P. & Gaudet, S. (2002) Head capsule width as an instar indicator for larvae of the cranberry fruitworm (Lepidoptera: Pyralidae) in southeastern New Brunswick. Journal of Economic Entomology, 95, 1308-1313.
17. González-Santoyo, I. & Córdoba-Aguilar, A. (2012) Phenoloxidase: a key component of the insect immune system. Entomologia Expermientalis et Applicata, 142, 1-16.
18. Grove, M.J. & Hoover, K. (2007) Intrastadial developmental resistance of third instar gypsy moths (Lymantria dispar L.) to L. dispar nucleopolyhedrovirus. Biological Control, 40, 355-361.
19. Gwynn, D.M., Callaghan, A., Gorham, J. et al. (2005) Resistance is costly: trade-offs between immunity, fecundity and survival in the pea aphid. Proceedings of the Royal Society of London Series B, Biological Sciences, 272, 1803-1808.
20. Haine, E.R., Moret, Y., Siva-Jothy, M.T. et al. (2008) Antimicrobial defense and persistent infection in insects. Science, 322, 1257-1259.
21. Hawkins, B.A., Cornell, H.V. & Hochberg, M.E. (1997) Predators, parasitoids, and pathogens as mortality agents in phytophagous insect populations. Ecology, 78, 2145-2152.
22. Helms, S.E., Connelly, S.J. & Hunter, M.D. (2004) Effects of variation among plant species on the interaction between a herbivore and its parasitoid. Ecological Entomology, 29, 44-51.
23. Jiang, H., Vilcinskas, A. & Kanost, M.R. (2010) Immunity in lepidopteran insects. Advances in Experimental Medicine and Biology, 708, 181-204.
24. Kapari, L., Haukioja, E., Rantala, M.J. et al. (2006) Defoliating insect immune defense interacts with induced plant defense during a population outbreak. Ecology, 87, 291-296.
25. Karimzadeh, J. & Wright, D.J. (2008) Bottom-up cascading effects in a tritrophic system: interactions between plant quality and host-parasitoid immune responses. Ecological Entomology, 33, 45-52.
26. Klemola, N., Klemola, T., Rantala, M.J. et al. (2007) Natural host-plant quality affects immune defence of an insect herbivore. Entomologia Experimentalis et Applicata, 123, 167-176.
27. Kraaijeveld, A.R., Limentani, E.C. & Godfray, H.C.J. (2001) Basis of the trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Proceedings of the Royal Society of London Series B, Biological Sciences, 268, 259-261.
28. Lai, S.C., Chen, C.C. & Hou, R.F. (2002) Immunolocalization of prophenoloxidase in the process of wound healing in the mosquito Armigeres subalbatus (Diptera: Culicidae). Journal of Medical Entomology, 39, 266-274.
29. Lavine, M.D. & Strand, M.R. (2002) Insect hemocytes and their role in immunity. Insect Biochemistry and Molecular Biology, 32, 1295-1309.
30. Lee, K.P., Simpson, S.J. & Wilson, K. (2008) Dietary protein-quality influences melanization and immune function in an insect. Functional Ecology, 22, 1052-1061.
31. Linder, J.E., Owers, K.A. & Promislow, D.E.L. (2008) The effects of temperature on host-pathogen interactions in D. melanogaster: who benefits? Journal of Insect Physiology, 54, 297-308.
32. Lynn, D.C. & Vinson, S.B. (1977) Effect of temperature, host age, and hormones upon the encapsulation of Cardiochiles nigriceps eggs by Heliothis spp. Journal of Invertebrate Pathology, 29, 50-55.
33. McNeil, J., Cox-Foster, D., Gardner, M. et al. (2010) Pathogenesis of Lymantria dispar multiple nucleopolyhedrovirus in L. dispar and mechanisms of developmental resistance. Journal of General Virology, 91, 1590-1600.
34. Moreau, J., Benrey, B. & Thiéry, D. (2006a) Assessing larval food quality for phytophagous insects: are the facts as simple as they appear? Functional Ecology, 20, 592-600.
35. Moreau, J., Benrey, B. & Thiéry, D. (2006b) Grape variety affects larval performance and also female reproductive performance of the European grapevine moth (Lobesia botrana). Bulletin of Entomological Research, 96, 205-212.
36. Moreau, J., Villemant, C., Benrey, B. et al. (2010) Species diversity of larval parasitoids of the European grapevine moth (Lobesia botrana, Lepidoptera: Tortricidae): the influence of region and cultivar. Biological Control, 54, 300-306.
37. Nappi, A.J. & Christensen, B.M. (2005) Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochemistry and Molecular Biology, 35, 443-459.
38. Ode, P.J. (2006) Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annual Review of Entomology, 51, 163-185.
39. Ojala, K., Julkunen-Tiitto, R., Lindström, L. et al. (2005) Diet affects the immune defence and life-history traits of an Arctiid moth Parasemia plantaginis. Evolutionary Ecology, 7, 1153-1170.
40. Panzavolta, T. (2007) Instar determination for Pissodes castaneus (Coleoptera: Curculionidae) using head capsule widths and lengths. Environmental Entomology, 36, 1054-1058.
41. Rantala, M.J., Kortet, R., Kotiaho, J.S. et al. (2003a) Condition dependence of pheromones and immune function in the grain beetle Tenebrio molitor. Functional Ecology, 17, 534-540.
42. Rantala, M.J., Kortet, R. & Vainikka, A. (2003b) The role of juvenile hormone in immune function and pheromone production trade-offs: a test of the immunocompetence handicap principle. Proceedings of the Royal Society of London Series B, Biological Sciences, 270, 2257-2261.
43. Ratcliffe, N.A., Rowley, A.F., Fitzgerald, S.W. et al. (1985) Invertebrate immunity: basic concepts and recent advances. International Review of Cytology, 97, 186-350.
44. Rolff, J. & Siva-Jothy, M.T. (2003) Invertebrate ecological immunology. Science, 301, 472-475.
45. Ryder, J.J. & Siva-Jothy, M.T. (2001) Quantitative genetics of immune function and body size in the house cricket, Acheta domesticus. Journal of Evolutionary Biology, 14, 646-653.
46. Sadd, B.M. & Schmid-Hempel, P. (2009) Principles of ecological immunology. Evolutionary Applications, 2, 113-121.
47. Schmid-Hempel, P. (2005) Evolutionary ecology of insect immune defenses. Annual Review of Entomology, 50, 529-551.
48. Schulenburg, H., Kurtz, J., Moret, Y. et al. (2009) Introduction. Ecological immunology. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences, 364, 3-14.
49. Shikano, I., Ericsson, J.D., Cory, J.S. et al. (2010) Indirect plant-mediated effects on insect immunity and disease resistance in a tritrophic system. Basic and Applied Ecology, 11, 15-22.
50. Siva-Jothy, M.T. & Thompson, J.J.W. (2002) Short-term nutrient deprivation affects immune function. Physiological Entomology, 27, 206-212.
51. Siva-Jothy, M.T., Moret, Y. & Rolff, J. (2005) Insect immunity: an evolutionary ecology perspective. Advances in Insect Physiology, 32, 1-48.
52. Smilanich, A.M., Dyer, L.A., Chambers, J.Q. et al. (2009) Immunological cost of chemical defence and the evolution of herbivore diet breadth. Ecology Letters, 12, 612-621.
53. Strand, M.R. (2008) The insect cellular immune response. Insect Science, 15, 1-14.
54. Strand, M.R. & Pech, L.L. (1995) Immunological basis for compatibility in parasitoid-host relationships. Annual Review of Entomology, 40, 31-56.
55. Thiéry, D. & Moreau, J. (2005) Relative performance of European grapevine moth (Lobesia botrana) on grapes and other hosts. Oecologia, 143, 548-557.
56. Thompson, S.N., Redak, R.A. & Wang, L.W. (2005) Host nutrition determines blood nutrient composition and mediates parasites developmental success: Manduca sexta L. parasitized by Cotesia congregata (Say). Journal of Experimental Biology, 208, 625-635.
57. Timmermann, S.E. & Briegel, H. (1999) Larval growth and biosynthesis of reserves in mosquitoes. Differentiation, 45, 461-470.
58. Vogelweith, F., Thiéry, D., Quaglietti, B. et al. (2011) Host plant variation plastically impacts different traits of the immune system of a phytophagous insect. Functional Ecology, 25, 1241-1247.
59. Yang, S., Ruuhola, T. & Rantala, M.J. (2007) Impact of starvation on immune defense and other life-history traits of an outbreaking geometrid, Epirrita autumanata: a possible causal trigger for the crash phase of population cycle. Annales Zoolici Fennici, 44, 89-96.
60. Zuk, M. & Stoehr, A.M. (2002) Immune defense and host life history. American Naturalist, 160 (Suppl), 9-22.