Costs of immunity in insects: An induced immune response increases metabolic rate and decreases antimicrobial activity

Functional Ecology

Volumn 26, Issue 3, 2012, Pages 732-739

  Ardia, Daniel R ^a   Gantz, Jacob E ^a   Schneider, Brent C ^a,b   Strebel, Stefanie ^a  

^a FRANKLIN AND MARSHALL COLLEGE   (United States)

^b GEORGE WASHINGTON UNIVERSITY   (United States)

Author keywords

Costs of immunity; Encapsulation; Life history trade offs; Lysozyme; Metabolic rate; Phenoloxidase; Wounding

Indexed keywords

ANTIMICROBIAL ACTIVITY; BODY FLUID; CARBON DIOXIDE; ENCAPSULATION; ENZYME ACTIVITY; EVOLUTIONARY BIOLOGY; IMMUNE RESPONSE; IMMUNITY; INSECT; LIFE HISTORY THEORY; PROTEIN; TRADE-OFF; WOUNDING;

ACHETA DOMESTICUS; COTINIS NITIDA; HEXAPODA; PERIPLANETA AMERICANA; TENEBRIO MOLITOR;

EID: 84862073898     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/j.1365-2435.2012.01989.x     Document Type: Article

References (37)

1. Adamo, S.A. (2004) Estimating disease resistance in insects: phenoloxidase and lysozyme-like activity and disease resistance in the cricket Gryllus texensis. Journal of Insect Physiology, 50, 209-216.
2. Adamo, S.A., Roberts, J.L., Easy, R.H. & Ross, N.W. (2008) Competition between immune function and lipid transport for the protein apolipophorin III leads to stress-induced immunosuppression in crickets. Journal of Experimental Biology, 211, 531-538.
3. Ardia, D.R., Parmentier, H.K. & Vogel, L.A. (2011) The role of constraints and limitation in driving individual variation in immune response. Functional Ecology, 25, 61-73.
4. Armitage, S.A.O. & Siva-Jothy, M.T. (2005) Immune function responds to selection for cuticular colour in Tenebrio molitor. Heredity, 94, 650-656.
5. Cotter, S.C., Kruuk, L.E.B. & Wilson, K. (2004) Costs of resistance: genetic correlations and potential tradeoffs in an insect immune system. Journal of Evolutionary Biology, 17, 421-429.
6. Cotter, S.C., Myatt, J.P., Benskin, C.M.H. & Wilson, K. (2008) Selection for cuticular melanism reveals immune function and life-history trade-offs in Spodoptera littoralis. Journal of Evolutionary Biology, 21, 1744-1754.
7. Da Silva, C.C.A., Dunphy, G.B. & Rau, M.E. (2000) Interaction of Xenorhabdus nematophilus (Enterobacteriaceae) with the antimicrobial defenses of the house cricket, Acheta domesticus. Journal of Invertebrate Pathology, 76, 285-292.
8. Demas, G.E., Adamo, S.A. & French, S.S. (2011) Neuroendocrine-immune crosstalk in vertebrates and invertebrates: implications for host defence. Functional Ecology, 25, 29-39.
9. Fellowes, M.D.E. & Godfray, H.C.J. (2000) The evolutionary ecology of resistance to parasitoids by Drosophila. Heredity, 84, 1-8.
10. Freitak, D., Ots, I., Vanatoa, A. & Horak, P. (2003) Immune response is energetically costly in white cabbage butterfly pupae. Proceedings of the Royal Society of London Series B-Biological Sciences, 270, S220-S222.
11. Gillespie, J.P., Kanost, M.R. & Trenczek, T. (1997) Biological mediators of insect immunity. Annual Review of Entomology, 42, 611-643.
12. Han, Y.S., Chun, J.S., Schwartz, A., Nelson, S. & Paskewitz, S.M. (1999) Induction of mosquito hemolymph proteins in response to immune challenge and wounding. Developmental and Comparative Immunology, 23, 553-562.
13. Hayes, J.P., Speakman, J.R. & Racey, P.A. (1992) Sampling bias in respirometry. Physiological Zoology, 65, 604-619.
14. Kan, H., Kim, C.H., Kwon, H.M., Park, J.W., Roh, K.B., Lee, H., Park, B.J., Zhang, R., Zhang, J., Soederhall, K., Ha, N.C. & Lee, B.L. (2008) Molecular control of phenoloxidase-induced melanin synthesis in an insect. Journal of Biological Chemistry, 283, 25316-25323.
15. Lambrechts, L., Vulule, J.M., Koella, J.C. & Day, T. (2009) Genetic correlation between melanization and antibacterial immune responses in a natural population of the malaria vector Anopheles gambiae. Evolution, 58, 2377-2381.
16. Lessells, C.M. & Boag, P.T. (1987) Unrepeatable repeatabilities. Auk, 104, 116-121.
17. Martin, L.B., Weil, Z.M. & Nelson, R.J. (2008) Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philosophical Transactions of the Royal Society B-Biological Sciences, 363, 321-339.
18. Moret, Y. & Schmid-Hempel, P. (2001) Immune defence in bumble-bee offspring. Nature, 414, 506-506.
19. Moret, Y. & Siva-Jothy, M.T. (2003) Adaptive innate immunity? Responsive-mode prophylaxis in the mealworm beetle, Tenebrio molitor. Proceedings of the Royal Society of London B, 1532, 2475-2480.
20. Morishima, I., Horiba, T., Iketani, M., Nishioka, E. & Yamano, Y. (1995) Parallel induction of cecropin and lysozyme in larvae of the silkworm, Bombyx mori. Developmental and Comparative Immunology, 19, 357-363.
21. Park, J.W., Je, B.R., Piao, S., Inamura, S., Fujimoto, Y., Fukase, K., Kusumoto, S., Soderhall, K., Ha, N.C. & Lee, B.L. (2006) A synthetic peptidoglycan fragment as a competitive inhibitor of the melanization cascade. Journal of Biological Chemistry, 281, 7747-7755.
22. Poulsen, M., Bot, A.N.M., Nielsen, M.G. & Boomsma, J.J. (2002) Experimental evidence for the costs and hygienic significance of the antibiotic metapleural gland secretion in leaf-cutting ants. Behavioral Ecology and Sociobiology, 52, 151-157.
23. Rantala, M.J. & Kortet, R. (2003) Courtship song and immune function in the field cricket Gryllus bimaculatus. Biological Journal of the Linnean Society, 79, 503-510.
24. Rantala, M.J. & Roff, D.A. (2005) An analysis of trade-offs in immune function, body size and development time in the Mediterranean Field Cricket, Gryllus bimaculatus. Functional Ecology, 19, 323-330.
25. Rantala, M.J. & Roff, D.A. (2006) Analysis of the importance of genotypic variation, metabolic rate, morphology, sex and development time on immune function in the cricket, Gryllus firmus. Journal of Evolutionary Biology, 19, 834-843.
26. Rantala, M.J. & Roff, D.A. (2007) Inbreeding and extreme outbreeding cause sex differences in immune defence and life history traits in Epirrita autumnata. Heredity, 98, 329-336.
27. Rantala, M.J., Vainikka, A. & Kortet, R. (2003) 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 B, 270, 2257-2261.
28. Rao, X.-J., Ling, E. & Yu, X.-Q. (2010) The role of lysozyme in the prophenoloxidase activation system of Manduca sexta: an in vitro approach. Developmental & Comparative Immunology, 34, 264-271.
29. Rolff, J. & Siva-Jothy, M.T. (2003) Invertebrate ecological immunology. Science, 301, 472-475.
30. Schmid-Hempel, P. (2005) Evolutionary ecology of insect immune defenses. Annual Review of Entomology, 50, 529-551.
31. Siva-Jothy, M.T., Moret, Y., Rolff, J. & Simpson, S.J. (2005) Insect immunity: an evolutionary ecology perspective. Advances in Insect Physiology, 32, 1-48.
32. Smilanich, A.M., Dyer, L.A. & Gentry, G.L. (2009) The insect immune response and other putative defenses as effective predictors of parasitism. Ecology, 90, 1434-1440.
33. Strand, M.R. (2008) The insect cellular immune response. Insect Science, 15, 1-14.
34. Vilmos, P. & Kurucz, V. (1998) Insect immunity: evolutionary roots of the mammalian innate immune system. Immunology Letters, 62, 59-66.
35. Whiting, M.F., Carpenter, J.C., Wheeler, Q.D. & Wheeler, W.C. (1997) The strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology, 46, 1-68.
36. Yang, S., Ruuhola, T. & Rantala, M.J. (2007) Impacts of starvation on immune defense and other life history traits of an outbreaking geometrid, Epirrita autumnata: a possible ultimate trigger of the crash phase of population cycle. Annales Zoologici Fennici, 44, 89-96.
37. Zhang, Y., Huang, J., Zhou, B., Zhang, C., Liu, W., Miao, X. & Huang, Y. (2009) Up-regulation of lysozyme gene expression during metamorphosis and immune challenge of the cotton bollworm, Helicoverpa armigera. Archives of Insect Biochemistry and Physiology, 70, 18-29.