Selection for cuticular melanism reveals immune function and life-history trade-offs in Spodoptera littoralis

Journal of Evolutionary Biology

Volumn 21, Issue 6, 2008, Pages 1744-1754

  Cotter, S C ^a,c   Myatt, J P ^b,c   Benskin, C M H ^c   Wilson, K ^c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c LANCASTER UNIVERSITY   (United Kingdom)

Author keywords

Ecological immunology; Host parasite interaction; Insect; Lepidoptera; Lysozyme; Melanism; Phenoloxidase; Phenotypic plasticity; Selection; Trade offs

Indexed keywords

LYSOZYME; MONOPHENOL MONOOXYGENASE; PLASMA PROTEIN;

CUTICLE; ENZYME ACTIVITY; HOST-PARASITE INTERACTION; IMMUNE RESPONSE; LIFE HISTORY; MELANISM; MOTH; PHENOTYPIC PLASTICITY;

ANIMAL; ARMYWORM; ARTICLE; BODY WEIGHT; ENZYMOLOGY; GENETIC SELECTION; GROWTH, DEVELOPMENT AND AGING; HEMOLYMPH; IMMUNOLOGY; LIFE CYCLE; METABOLISM; PHYSIOLOGY; PIGMENTATION;

ANIMALS; BLOOD PROTEINS; BODY WEIGHT; HEMOLYMPH; LIFE CYCLE STAGES; MONOPHENOL MONOOXYGENASE; MURAMIDASE; PIGMENTATION; SELECTION (GENETICS); SPODOPTERA;

HEXAPODA; LEPIDOPTERA; SPODOPTERA LITTORALIS;

EID: 54049085460     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2008.01587.x     Document Type: Article

References (61)

1. Adamo, S.A. 2004. Estimating disease resistance in insects: phenoloxidase and lysozyme-like activity and disease resistance in the cricket, Gryllus texensis. J. Insect Physiol. 50 : 209 216.
2. Armitage, S.A.O. Siva-Jothy, M.T. 2005. Immune function responds to selection for cuticular colour in Tenebrio molitor. Heredity 94 : 650 656.
3. Ashida, M. Brey, P.T. 1995. Role of the integument in insect defense-prophenoloxidase cascade in the cuticular matrix. Proc. Natl Acad. Sci. USA. 92 : 10698 10702.
4. Ashida, M. Brey, P.T. 1997. Recent advances in research on the insect prophenoloxidase cascade. In : Molecular Mechanisms of Immune Responses in Insects (P.T. Brey D. Hultmark, eds pp. 135 172. Chapman & Hall, London.
5. 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. Proc. R. Soc. Lond. Ser. B Biol. Sci. 267 : 177 182.
6. Bezzerides, A.L., McGraw, K.J., Parker, R.S. Husseini, J. 2007. Elytra color as a signal of chemical defense in the Asian ladybird beetle Harmonia axyridis. Behav. Ecol. Sociobiol. 61 : 1401 1408.
7. Cerenius, L. Soderhall, K. 2004. The prophenoloxidase-activating system in invertebrates. Immunol. Rev. 198 : 116 126.
8. Cotter, S.C. 2002. Trade-offs in insect disease resistance. PhD Thesis, Institute of Biological Sciences, University of Stirling.
9. Cotter, S.C. Wilson, K. 2002. Heritability of immune function in the caterpillar Spodoptera littoralis. Heredity 88 : 229 234.
10. Cotter, S.C., Hails, R.S., Cory, J.S. Wilson, K. 2004a. Density-dependent prophylaxis and condition-dependent immune function in lepidopteran larvae: a multivariate approach. J. Anim. Ecol. 73 : 283 293.
11. Cotter, S.C., Kruuk, L.E.B. Wilson, K. 2004b. Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. J. Evol. Biol. 17 : 421 429.
12. Cotter, S.C., Beveridge, M. Simmons, L.W. 2008. Male morph predicts investment in larval immune function in the dung beetle, Onthophagus taurus. Behav. Ecol. 19 : 331 337.
13. Evans, M.R., Roberts, M.L., Buchanan, K.L. Goldsmith, A.R. 2006. Heritability of corticosterone response and changes in life history traits during selection in the zebra finch. J. Evol. Biol. 19 : 343 352.
14. Falconer, D.S. Mackay, T.F.C. 1996. Introduction to Quantitative Genetics, 4th edn. Longman Group Ltd, London.
15. Freitak, D., Wheat, C.W., Heckel, D.G. Vogel, H. 2007. Immune system responses and fitness costs associated with consumption of bacteria in larvae of Trichoplusia ni. BMC Biol. 5 : 56.
16. Goulson, D. Cory, J.S. 1995. Responses of Mamestra brassicae (Lepidoptera, Noctuidae) to crowding-interactions with disease resistance, color phase and growth. Oecologia 104 : 416 423.
17. Griffith, S.C., Parker, T.H. Olson, V.A. 2006. Melanin-versus carotenoid-based sexual signals: is the difference really so black and red? Anim. Behav. 71 : 749 763.
18. Hiruma, K. Riddiford, L.M. 1988. Granular phenoloxidase involved in cuticular melanisation in the tobacco hornworm: regulation of its synthesis in the epidermis by juvenile hormone. Dev. Biol. 130 : 87 97.
19. Hodjat, S.H. 1970. Effects of crowding on colour, size and larval activity of Spodoptera littoralis (Lepidoptera: Noctuidae). Entomol. Exp. App. 13 : 97 106.
20. Jarvi, T. Bakken, M. 1984. The function of the variation in the breast stripe of the great tit (Parus major). Anim. Behav. 32 : 590 596.
21. Kauppinen, J. Mappes, J. 2003. Why are wasps so intimidating: field experiments on hunting dragonflies (Odonata: Aeshna grandis). Anim. Behav. 66 : 505 511.
22. Kettlewell, H.B.D. 1973. The Evolution of Melanism. Clarendon Press, Oxford.
23. Kose, M. Møller, A.P. 1999. Sexual selection, feather breakage and parasites: the importance of white spots in the tail of the barn swallow (Hirundo rustica). Behav. Ecol. Sociobiol. 45 : 430 436.
24. Kunimi, Y. Yamada, E. 1990. Relationship of larval phase and susceptibility of the armyworm, Pseudaletia separata Walker (Lepidoptera, Noctuidae) to a nuclear polyhedrosis virus and a granulosis virus. Appl. Entomol. Zool. 25 : 289 297.
25. Kurtz, J., Wiesner, A., Gotz, P. Sauer, K.P. 2000. Gender differences and individual variation in the immune system of the scorpionfly Panorpa vulgaris (Insecta: Mecoptera). Dev. Comp. Immunol. 24 : 1 12.
26. Lee, K.P. Wilson, K. 2006. Melanism in a larval Lepidoptera: repeatability and heritability of a dynamic trait. Ecol. Entomol. 31 : 196 205.
27. Lee, K.P., Cory, J.S., Wilson, K., Raubenheimer, D. Simpson, S.J. 2006. Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc. R. Soc. Lond. Ser. B Biol. Sci. 273 : 823 829.
28. Mackintosh, J.A. 2001. The antimicrobial properties of melanocytes, melanosomes and melanin and the evolution of black skin. J. Theor. Biol. 211 : 101 113.
29. Majerus, M.E.N. 1998. Melanism: Evolution in Action. Oxford University Press, Oxford.
30. Marmaras, V.J., Charalambidis, N.D. Zervas, C.G. 1996. Immune response in insects: the role of phenoloxidase in defense reactions in relation to melanization and sclerotization. Arch. Insect Biochem. Physiol. 31 : 119 133.
31. Marples, N.M., Vanveelen, W. Brakefield, P.M. 1994. The relative importance of color, taste and smell in the protection of an aposematic insect Coccinella septempunctata. Anim. Behav. 48 : 967 974.
32. McKean, K.A. Nunney, L. 2008. Sexual selection and immune function in Drosophila melanogaster. Evolution 62 : 386 400.
33. Mitsui, J. Kunimi, Y. 1988. Effect of larval phase on susceptibility of the armyworm, Pseudaletia separata Walker (Lepidoptera, Noctuidae) to an entomogeneous Deuteromycete, Nomuraea rileyi. Jpn. J. Appl. Entomol. Zool. 32 : 129 134.
34. Moller, A.P. 1988. Badge size in the house sparrow Passer domesticus- effects of intrasexual and intersexual selection. Behav. Ecol. Sociobiol. 22 : 373 378.
35. Montefiori, D.C. Zhou, J.Y. 1991. Selective antiviral activity of synthetic soluble l-tyrosine and l-dopa melanins against human-immunodeficiency- virus in vitro. Antiviral Res. 15 : 11 26.
36. Moret, Y. Schmid-Hempel, P. 2001. Entomology - immune defence in bumble-bee offspring. Nature 414 : 506.
37. Moret, Y. Siva-Jothy, M.T. 2003. Adaptive innate immunity? Responsive-mode prophylaxis in the mealworm beetle, Tenebrio molitor. Proc. R. Soc. Lond. Ser. B Biol. Sci. 270 : 2475 2480.
38. Nappi, A.J. Vass, E. 1993. Melanogenesis and the generation of cytotoxic molecules during insect cellular immune-reactions. Pigment Cell. Res. 6 : 117 126.
39. van Noordwijk, A.J. de Jong, G. 1986. Acquisition and allocation of resources-their influence on variation in life-history tactics. Am. Nat. 128 : 137 142.
40. Rantala, M.J. Kortet, R. 2003. Courtship song and immune function in the field cricket Gryllus bimaculatus. Biol. J. Linn. Soc. 79 : 503 510.
41. Reeson, A.F., Wilson, K., Gunn, A., Hails, R.S. Goulson, D. 1998. Baculovirus resistance in the noctuid Spodoptera exempta is phenotypically plastic and responds to population density. Proc. R. Soc. Lond. Ser. B Biol. Sci. 265 : 1787 1791.
42. Reznick, D., Nunney, L. Tessier, A. 2000. Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol. Evol. 15 : 421 425.
43. Rolff, J. 2002. Bateman's principle and immunity. Proc. R. Soc. Lond. Ser. B Biol. Sci. 269 : 867 872.
44. Rosen, R.F. Tarvin, K.A. 2006. Sexual signals of the male American goldfinch. Ethology 112 : 1008 1019.
45. Saegrov, H., Hobaek, A. LabeeLund, J.H. 1996. Vulnerability of melanic Daphnia to brown trout predation. J. Plankton Res. 18 : 2113 2118.
46. Schwarzenbach, G.A. Ward, P.I. 2006. Responses to selection on phenoloxidase activity in yellow dung flies. Evolution 60 : 1612 1621.
47. Sheldon, B.C. Verhulst, S. 1996. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11 : 317 321.
48. Simmonds, M.S.J. Blaney, W.M. 1986. Effects of rearing density on development and feeding behavior in larvae of Spodoptera exempta. J. Insect Physiol. 32 : 1043 1053.
49. Siva-Jothy, M.T. 2000. A mechanistic link between parasite resistance and expression of a sexually selected trait in a damselfly. Proc. R. Soc. Lond. Ser. B Biol. Sci. 267 : 2523 2527.
50. Söderhall, K. Ajaxon, R. 1982. Effect of quinones and melanin on mycelial growth of Aphanomyces spp and extracellular protease of Aphanomyces astaci a parasite on crayfish. J. Invertebr. Pathol. 39 : 105 109.
51. Spitze, K. 1991. Chaoborus predation and life-history evolution in Daphnia pulex-temporal pattern of population diversity, fitness, and mean life-history. Evolution 45 : 82 92.
52. St. Leger, R.J., Cooper, R.M. Charnley, A.K. 1988. The effect of melanization of Manduca sexta cuticle on growth and infection by Metarhizium anisopliae. J. Invertebr. Pathol. 52 : 459 470.
53. Svensson, E.I. Friberg, M. 2007. Selective predation on wing morphology in sympatric damselflies. Am. Nat. 170 : 101 112.
54. Vermeulen, C.J. Bijlsma, R. 2006. Changes in genetic architecture during relaxation in Drosophila melanogaster selected on divergent virgin life span. J. Evol. Biol. 19 : 216 227.
55. Wiklund, C. Sillen-Tullberg, B. 1985. Why distasteful butterflies have aposematic larvae and adults, but cryptic pupae-evidence from predation experiments on the monarch and the European swallowtail. Evolution 39 : 1155 1158.
56. Wilson, K. 2000. How the locust got its stripes: the evolution of density-dependent aposematism. Trends Ecol. Evol. 14 : 88 90.
57. Wilson, K. Cotter, S.C. 2008. Density-dependent prophylaxis in insects. In : Insects and Phenotypic Plasticity: Mechanisms and Consequences (T.N. Ananthakrishnan D.W. Whitman, eds pp. 137 176. Science Publishers Inc, Plymouth, UK.
58. Wilson, K. Reeson, A.F. 1998. Density-dependent prophylaxis: evidence from Lepidoptera-baculovirus interactions? Ecol. Entomol. 23 : 100 101.
59. Wilson, K., Cotter, S.C., Reeson, A.F. Pell, J.K. 2001. Melanism and disease resistance in insects. Ecol. Lett. 4 : 637 649.
60. Wilson, K., Thomas, M.B., Blanford, S., Doggett, M., Simpson, S.J. Moore, S.L. 2002. Coping with crowds: density-dependent disease resistance in desert locusts. Proc. Natl Acad. Sci. USA. 99 : 5471 5475.
61. Zahavi, A. 1975. Mate selection - a selection for a handicap. J. Theor. Biol. 53 : 205 214.