Cuticular melanisation and immune response in a butterfly: Local adaptation and lack of correlation

Ecological Entomology

Volumn 35, Issue 4, 2010, Pages 523-528

  Karl, Isabell ^a,b   Hoffmann, Klaus H ^a   Fischer, Klaus ^a  

^a UNIVERSITY OF BAYREUTH   (Germany)

^b UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

Altitudinal variation; Geographic variation; Immune defence; Implant encapsulation rate; Lycaena tityrus; Melanin pathway; Pupal melanisation; Thermal melanism; Trade off

Indexed keywords

ALTITUDINAL ZONATION; BUTTERFLY; CORRELATION; GEOGRAPHICAL VARIATION; IMMUNE RESPONSE; LOCAL ADAPTATION; PHENOTYPIC PLASTICITY; TRADE-OFF;

ANIMALIA; INVERTEBRATA; LYCAENA TITYRUS;

EID: 77955259660     PISSN: 03076946     EISSN: 13652311     Source Type: Journal    
DOI: 10.1111/j.1365-2311.2010.01211.x     Document Type: Article

References (58)

1. Barnes AI, Siva-Jothy MT. Density-dependent prophylaxis in the mealworm beetle Tenebrio molitor (Coleoptera: Tenebrionidae): cuticular melanization is an indicator of investment in immunity. Proceedings of the Royal Society of London, Series B 2000, 267:177-182.
2. Baucom R, Mauricio R. The evolution of novel herbicide tolerance in a noxious weed: the geographic mosaic of selection. Evolutionary Ecology 2007, 22:85-101.
3. Berggren A. Effect of landscape and population variables on immune response in experimentally introduced bush-cricket populations. Landscape Ecology 2009, 24:749-757.
4. Blanckenhorn WU, Demont M. Bergmann and converse Bergmann latitudinal clines in arthropods: two ends of a continuum? Integrative and Comparative Biology 2004, 44:413-424.
5. Blanford S, Thomas MB, Pugh C, Pell JK. Temperature checks the Red Queen? Resistance and virulence in a fluctuating environment. Ecology Letters 2003, 6:2-5.
6. Bonneaud C, Mazuc J, Gonzalez G, Haussy C, Chastel O, Faivre B. Assessing the cost of mounting an immune response. American Naturalist 2003, 161:367-379.
7. Brodie ED, Ridenhour BJ, Brodie ED. The evolutionary response of predators to dangerous prey: hotspots and coldspots in the geographic mosaic of coevolution between garter snakes and newts. Evolution 2002, 56:2067-2082.
8. Brown C. Offspring size-number trade-off in scorpions: an empirical test of the van Noordwijk and DeJong model. Evolution 2003, 57:2184-2190.
9. Carton Y, Nappi AJ. Drosophila cellular immunity against parsitoids. Parasitology Today 1997, 13:218-225.
10. Chown SL, Klok C. Altitudinal body size clines: latitudinal effects associated with changing seasonality. Ecography 2003, 26:445-455.
11. Civantos E, Ahnesjö J, Forsman A. Immune function, parasitization and extended phenotypes in colour polymorphic pygmy grasshoppers. Biological Journal of the Linnean Society 2005, 85:373-383.
12. Clusella-Trullas S, van Wyk JH, Spotila JR. Thermal melanism in ectotherms. Journal of Thermal Biology 2007, 32:235-245.
13. Cornet S, Biard C, Moret Y. Variation in immune defence among populations of Gammarus pulex (Crustacea: Amphipoda). Oecologia 2009, 159:257-269.
14. De Block M, Slos S, Johansson F, Stoks R. Integrating life history and physiology to understand latitudinal size variation in a damselfly. Ecography 2008, 31:115-123.
15. Ebert G, Rennwald E. Die Schmetterlinge Baden-Württembergs 1991, Vol 2., Ulmer, Stuttgart, Germany
16. Espeland M, Aagaard K, Balstad T, Hindar K. Ecomorphological and genetic divergence between lowland and montane forms of the Pieris napi species complex (Pieridae, Lepidoptera). Biological Journal of the Linnean Society 2007, 92:727-745.
17. Ferguson HM, Read AF. Genetic and environmental determinants of malaria parasite virulence in mosquitoes. Proceedings of the Royal Society of London, Series B 2002, 269:1217-1224.
18. Fischer K, Fiedler K. Sex-related differences in reaction norms in the butterfly Lycaena tityrus (Lepidoptera: Lycaenidae). Oikos 2000, 90:372-380.
19. Freitak D, Vanatoa A, Ots I, Rantala MJ. Formation of melanin-based wing patterns is influenced by condition and immune challenge in Pieris brassicae. Entomologia Experimentalis et Applicata 2005, 116:237-243.
20. Gillespie JP, Kanost MR, Trenczek T. Biological mediators of insect immunity. Annual Review of Entomology 1997, 42:611-643.
21. Jacot A, Scheuber H, Brinkhof MWG. Costs of an induced immune response on sexual display and longevity in field crickets. Evolution 2004, 58:2280-2286.
22. James AC, Partridge L. Thermal evolution of rate of larval development in Drosophila melanogaster in laboratory and field populations. Journal of Evolutionary Biology 1995, 8:315-330.
23. Karl I, Fischer K. Why get big in the cold? Towards a solution to a life-history puzzle. Oecologia 2008, 155:215-225.
24. Karl I, Janowitz SA, Fischer K. Altitudinal life-history variation and thermal adaptation in the copper butterfly Lycaena tityrus. Oikos 2008, 117:778-788.
25. Karl I, Sørensen JG, Loeschcke V, Fischer K. HSP70 expression in the Copper butterfly Lycaena tityrus across altitudes and temperatures. Journal of Evolutionary Biology 2009a, 22:172-178.
26. Karl I, Schmitt T, Fischer K. Genetic differentiation between alpine and lowland populations of a butterfly is related to PGI enzyme genotype. Ecography 2009b, 32:488-496.
27. Karl I, Geister TL, Fischer K. Intraspecific variation in wing and pupal melanization in copper butterflies (Lepidoptera: Lycaenidae). Biological Journal of the Linnean Society 2009c, 98:301-312.
28. Kraaijeveld AR, Godfray HCJ. Selection for resistance to a fungal pathogen in Drosophila melanogaster. Heredity 2008, 100:400-406.
29. Kurtz J, Sauer KP. Gender differences in phenoloxidase activity of Panorpa vulgaris hemocytes. Journal of Invertebrate Pathology 2001, 78:53-55.
30. Little TJ, Killick SC. Evidence for a cost of immunity when the crustacean Daphnia magna is exposed to the bacterial pathogen Pasteuria ramosa. Journal of Animal Ecology 2007, 76:1202-1207.
31. Lorioux S, Bonnet X, Brischoux F, De Crignis M. Is melanism adaptive in sea kraits? Amphibia-Reptilia 2008, 29:1-5.
32. Nappi AJ, Carton Y, Frey F. Parasite-induced enhancement of hemolymph tyrosinase activity in a selected immune reactive strain of Drosophila melanogaster. Archives of Insect Biochemistry and Physiology 1991, 18:159-168.
33. Rajpurohit S, Parkash R, Ramniwas S, Singh S. Variations in body melanisation, ovariole number and fecundity in highland and lowland populations of Drosophila melanogaster from the Indian subcontinent. Insect Science 2008, 15:553-561.
34. Rantala MJ, Roff DA. An analysis of trade-offs in immune function, body size and development time in the Mediterranean Field Cricket, Gryllus bimaculatus. Functional Ecology 2005, 19:323-330.
35. Rantala MJ, Roff DA. Inbreeding and extreme outbreeding cause sex differences in immune defence and life history traits in Epirrita autumnata. Heredity 2007, 98:329-336.
36. Rantala MJ, KoskimÌki J, Taskinen J, Tynkkynen J, Suhonen J. Immunocompetence, developmental stability and wingspot size in the damselfly Calopteryx splendens L. Proceedings of the Royal Society of London, Series B 2000, 267:2453-2457.
37. Rantala MJ, Roff DA, Rantala LM. Forceps size and immune function in the earwig Forficula auricularia L. Biological Journal of the Linnean Society 2007, 90:509-516.
38. Rhamhalinghan M. Variations in the realized fecundity of melanics of Coccinella septempunctata L. in relation to degree of elytral pigmentation and radiant heat level. Journal of Insect Science 1999, 12:22-26.
39. Rolff J. Bateman's principle and immunity. Proceedings of the Royal Society London, Series B 2002, 269:867-872.
40. Rolff J, Siva-Jothy MT. Copulation corrupts immunity: a mechanism for a cost of mating in insects. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:9916-9918.
41. Rolff J, Siva-Jothy MT. Invertebrate ecological immunology. Science 2003, 301:472-475.
42. Ryder JJ, Siva-Jothy MT. Quantitative genetics of immune function and body size in the house cricket, Acheta domesticus. Journal of Evolutionary Biology 2001, 14:646-653.
43. Schmid-Hempel P. Variation in immune defence as a question of evolutionary ecology. Proceedings of the Royal Society London, Series B 2003, 270:357-366.
44. Schmid-Hempel P. Evolutionary ecology of insect immune defenses. Annual Review of Entomology 2005, 50:529-551.
45. Schulte-Hostedde AI, Millar JS, Hickling GJ. Evaluating body condition in small mammals. Canadian Journal of Zoology 2001, 79:1021-1029.
46. Schwartz A, Koella JC. The cost of immunity in the yellow fever mosquito, Aedes aegypti depends on immune activation. Journal of Evolutionary Biology 2004, 17:834-840.
47. Sheldon BC, Verhulst S. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 1996, 11:317-321.
48. Siva-Jothy M. A mechanistic link between parasite resistance and expression of a sexually selected trait in a damselfly. Proceedings of the Royal Society London, Series B 2000, 267:2523-2527.
49. Stoehr AM. Inter- and intra-sexual variation in immune defence in the cabbage white butterfly, Pieris rapae L. (Lepidoptera: Pieridae). Ecological Entomology 2007, 32:188-193.
50. Sugumaran M, Nellaiappan K, Valivittan K. A new mechanism for the control of phenoloxidase activity: inhibition and complex formation with quinone isomerase. Archives of Biochemistry and Biophysics 2000, 379:252-260.
51. Talloen W, Van Dyck H, Lens L. The cost of melanization: butterfly wing coloration under environmental stress. Evolution 2004, 58:360-366.
52. Tolman T, Lewington R. Die Tagfalter Europas und Nordwestafrikas 1998, Franckh-Kosmos, Stuttgart, Germany
53. True JR. Insect melanism: the molecules matter. Trends in Ecology and Evolution 2003, 18:640-647.
54. Van't Land JP, van Putten P, Zwaan B, Kamping A, van Delden W. Latitudinal variation in wild populations of Drosophila melanogaster: heritabilities and reaction norms. Journal of Evolutionary Biology 1999, 12:222-232.
55. Verhoog MD, Van Boven A, Brakefield PM. Melanic moths and the ability to encapsulate parasitoid eggs and larvae. Proceedings of the Netherland Entomological Society 1996, 7:127-133.
56. Vijendravarma RK, Kraaijeveld AR, Godfray HCJ. Experimental evolution shows Drosophila melanogaster resistance to a microsporidian pathogen has fitness costs. Evolution 2009, 63:104-114.
57. Wilson K, Cotter SC, Reeson AF, Pell JK. Melanism and disease resistance in insects. Ecology Letters 2001, 4:637-649.
58. Zuk M, McKean KA. Sex differences in parasite infections: patterns and processes. International Journal of Parasitology 1996, 26:1009-1023.