Lack of Phenotypic and Evolutionary Cross-Resistance against Parasitoids and Pathogens in Drosophila melanogaster

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Kraaijeveld, Alex R ^a,b   Layen, Sophie J ^a   Futerman, Peter H ^a   Godfray, H Charles J ^a,c  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; ASOBARA TABIDA; BEAUVERIA BASSIANA; CONTROLLED STUDY; CROSS REACTION; DROSOPHILA MELANOGASTER; ENCAPSULATION; EVOLUTIONARY ADAPTATION; HOST PARASITE INTERACTION; IMMUNE RESPONSE; NONHUMAN; PARASITE; PARASITISM; PARASITOID; PHENOTYPE; SURVIVAL RATE; TUBULINOSEMA KINGI;

ANIMALS; APANSPOROBLASTINA; BEAUVERIA; DISEASE RESISTANCE; DROSOPHILA MELANOGASTER; EVOLUTION, MOLECULAR; HOST-PATHOGEN INTERACTIONS; HYMENOPTERA; MICROBIAL INTERACTIONS; PHENOTYPE;

ASOBARA TABIDA; CORDYCEPS BASSIANA; DROSOPHILA MELANOGASTER; FUNGI; INVERTEBRATA; TUBULINOSEMA KINGI;

EID: 84871350502     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053002     Document Type: Article

References (55)

1. Levin DA, (1976) The chemical defenses of plants to pathogens and herbivores. Ann Rev Ecol Syst 7: 121-159.
2. Maleck K, Dietrich PA, (1999) Defense on multiple fronts: how do plants cope with diverse enemies? Trends Plant Sci 4: 215-219.
3. Hunter GW, Weinmann CJ, Hoffmann RG, (2004) Studies on schistosomiasis. XVII. Non-reciprocal acquired resistance between Schistosoma mansoni and Schistosomatium douthitti in mice. Exp Parasitol 11: 133-140.
4. Rigby MC, Jokela J, (2000) Predator avoidance and immune defence: costs and trade-offs in snails. Proc Roy Soc Lond B 267: 171-176.
5. Kurtz J, Franz K, (2003) Evidence for memory in invertebrate immunity. Nature 425: 37-38.
6. Little TJ, O'Connor B, Colegrave N, Watt K, Read AF, (2003) Maternal transfer of strain-specific immunity in an invertebrate. Curr Biol 13: 489-492.
7. Sadd BM, Kleinlogel Y, Schmid-Hempel R, Schmid-Hempel P, (2005) Trans-generational immune priming in a social insect. Biol Lett 1: 386-388.
8. He W, Neil S, Kulkarni H, Wright E, Agan BK, Marconi VC, Dolan MJ, Weiss RA, Ahuja SK, (2008) Duffy Antigen Receptor for Chemokines mediates trans-infection of HIV-1 from red blood cell to target cells and affects HIV-AIDS susceptibility. Cell Host & Micr 4: 52-62.
9. Kraaijeveld AR, Godfray HCJ (2009) Evolution of host resistance and parasitoid counter-resistance. In: Prévost G, editor. Advances in Parasitology. Vol 70: Parasitoids of Drosophila. Academic Press, Burlington: 257-280.
10. Kraaijeveld AR, Wertheim B (2009) Costs and genomic aspects of Drosophila immunity to parasites and pathogens. In: Rolff J, Reynolds S, editors. Insect Infection and Immunity. Oxford University Press, Oxford: 187-205.
11. Carton Y, Boulétreau M, van Alphen JJM, van Lenteren JC (1986). The Drosophila parasitic wasps. In: Ashburner M, Carson HL, Thompson JN, editors. The Genetics and Biology of Drosophila, Vol. 3e. Academic Press, London: 347-394.
12. Kraaijeveld AR, van der Wel NN, (1994) Geographic variation in reproductive success of the parasitoid Asobara tabida in larvae of several Drosophila species. Ecol Ent 19: 221-229.
13. Nappi AJ, (1981) Cellular immune response of Drosophila melanogaster against Asobara tabida. Parasitology 83: 319-324.
14. Rizki TM, Rizki RM (1984). The cellular defense system of Drosophila melanogaster. In: King RC, Akai H, editors. Insect Ultrastructure. Vol. 2. Plenum Publishing Co, New York: 579-603.
15. Lavine MD, Strand MR, (2002) Insect hemocytes and their role in immunity. Ins Biochem Mol Biol 32: 1295-1309.
16. Meister M, Lagueux M, (2003) Drosophila blood cells. Cell Microbiol 5: 573-580.
17. Kraaijeveld AR, van Alphen JJM, (1994) Geographical variation in resistance of the parasitoid Asobara tabida against encapsulation by Drosophila melanogaster larvae: the mechanism explored. Physiol Ent 19: 9-14.
18. Eslin P, Giordanengo P, Fourdrain Y, Prévost G, (1996) Avoidance of encapsulation in the absence of VLP by a braconid parasitoid of Drosophila larvae: an ultrastructural study. Can J Zool 74: 2193-2198.
19. Rizki TM, Rizki RM, (1994) Parasitoid-induced cellular immune deficiency in Drosophila. Ann NY Acad Sci 712: 178-194.
20. Russo J, Brehelin M, Carton Y, (2001) Haemocyte changes in resistant and susceptible strains of D. melanogaster caused by virulent and avirulent strains of the parasitic wasp Leptopilina boulardi. J Ins Physiol 47: 167-172.
21. Labrosse C, Carton Y, Dubuffet A, Drezen JM, Poirié M, (2003) Active suppression of D. melanogaster immune response by long gland products of the parasitic wasp Leptopilina boulardi. J Ins Physiol 49: 513-522.
22. Labrosse C, Eslin P, Doury G, Drezen JM, Poirié M, (2005) Haemocyte changes in D. melanogaster in response to long gland components of the parasitoid wasp Leptopilina boulardi: a Rho-GAP protein as an important factor. J Ins Physiol 51: 161-170.
23. Kraaijeveld AR, van Alphen JJM, (1995) Geographic variation in encapsulation ability of Drosophila melanogaster larvae and evidence for parasitoid-specific components. Evol Ecol 9: 10-17.
24. Boulétreau M, Wajnberg E, (1986) Comparative responses of two sympatric parasitoid cynipids to the genetic and epigenetic variations of the larvae of their host, Drosophila melanogaster. Ent exp appl 41: 107-114.
25. Delpuech JM, Frey F, Carton Y, (1994) Genetic and epigenetic variation in suitability of a Drosophila host to three parasitoid species. Can J Zool 71: 584-594.
26. Fellowes MDE, Kraaijeveld AR, Godfray HCJ, (1999) Cross-resistance following artificial selection for increased defence against parasitoids in Drosophila melanogaster. Evolution 53: 966-972.
27. Fraenkel G, Rudall KM, (1947) The structure of insect cuticles. Proc Roy Soc Lond B 134: 111-143.
28. Rizki TM, Rizki RM, Grell EH, (1980) A mutant affecting the crystal cells in Drosophila melanogaster. Wm Roux's Arch Devel. Biol. 188: 91-99.
29. Fellowes MDE, Masnatta P, Kraaijeveld AR, Godfray HCJ, (1998) Pupal parasitoid attack influences the relative fitness of Drosophila that have encapsulated larval parasitoids. Ecol Ent 23: 281-284.
30. Kraaijeveld AR, Ferrari J, Godfray HCJ, (2002) Costs of resistance in insect-parasite and insect-parasitoid interactions. Parasitology 125: S71-S82.
31. Tinsley MC, Blanford S, Jiggins FM, (2006) Genetic variation in Drosophila melanogaster pathogen susceptibility. Parasitology 132: 767-773.
32. Kraaijeveld AR, Godfray HCJ, (2008) Selection for resistance to a fungal pathogen in Drosophila melanogaster. Heredity 100: 400-406.
33. Lemaitre B, Reichhart J-M, Hoffmann JA, (1997) Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc Natl Acad Sci USA 94: 14614-14619.
34. Tzou P, De Gregorio E, Lemaitre B, (2002) How Drosophila combats microbial infection: a model to study innate immunity and host-pathogen interactions. Curr Opin Microbiol 5: 102-110.
35. Hoffmann JA, (2003) The immune response of Drosophila. Nature 426: 33-38.
36. Wang L, Ligoxygakis P, (2006) Pathogen recognition and signalling in the Drosophila innate immune response. Immunobiology 211: 251-261.
37. Agaisse H, Petersen U-M, Boutros M, Mathey-Prevot B, Perrimon N, (2003) Signaling role of hemocytes in Drosophila JAK/STAT-dependent response to septic injury. Dev Cell 5: 441-450.
38. Irving P, Ubeda J-M, Doucet D, Troxler L, Lagueux M, Zachary D, Hoffmann JA, Hetru C, Meister M, (2005) New insights into Drosophila larval hemocyte functions through genome-wide analysis. Cell Microbiol 7: 335-350.
39. Futerman PH, Layen SJ, Franzen C, Kraaijeveld AR, Godfray HCJ, (2006) Fitness effects and transmission routes of a microsporidian parasite infecting Drosophila and its parasitoids. Parasitology 132: 479-492.
40. Vijendravarma RK, Kraaijeveld AR, Godfray HCJ, (2009) Experimental evolution shows Drosophila melanogaster resistance to a microsporidian pathogen has fitness costs. Evolution 63: 104-114.
41. David L, Weiser J, (1994) Role of hemocytes in the propagation of a microsporidian infection in larvae of Galleria mellonella. J Invert Path 63: 212-213.
42. Becnel JJ, Andreadis TG (1999). Microsporidia in insects. In: Wittner M, Weiss LM, editors. The Microsporidia and Microsporidiosis. Washington DC: ASM Press: 447-501.
43. Kurtz J, Nahif AA, Sauer KP, (2000) Phacocytosis of Vairimorpha sp. (Microsporida, Nosematidae) spores by Plutella xylostella and Panorpa vulgaris hemocytes. J Invert Path 75: 237-239.
44. Hoch G, Schopf A, (2001) Effects of Glyptapanteles liparidis (Hym.: Braconidae) parasitism, polydnavirus, and venom on development of microsporidia-infected and uninfected Lymantria dispar (Lep.: Lymatriidae) larvae. J Invert Path 77: 37-43.
45. Wertheim B, Kraaijeveld AR, Schuster E, Blanc E, Hopkins M, Pletcher SD, Strand MR, Partridge L, Godfray HCJ, (2005) Genome-wide gene expression in response to parasitoid attack in Drosophila. Genome Biology 6: R94.
46. Kraaijeveld AR, Godfray HCJ, (1997) Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389: 278-280.
47. Fytrou A, Schofield PG, Kraaijeveld AR, Hubbard SF, (2006) Wolbachia suppresses both host defence and parasitoid counter-defence. Proc Roy Soc Lond B 273: 791-796.
48. Moret Y, Siva-Jothy M (20030 Adaptive innate immunity? Responsive-mode prophylaxis in the mealworm beetle, Tenebrio molitor. Proc Roy Soc Lond B 270: 2475-2480.
49. Moret Y, Schmid-Hempel P, (2001) Immune defence in bumble-bee offspring. Nature 414: 506.
50. Hoch G, Schopf A, Maddox JV, (2000) Interactions between an entomopathogenic microsporidium and the endoparasitoid Glyptapanteles liparidis with their host, the gypsy moth larva. J Invert Path 75: 59-68.
51. Hoch G, Solter LF, Schopf A, (2004) Hemolymph melanization and alterations in hemocyte numbers in Lymantria dispar larvae following infections with different entomopathogenic microsporidia. Ent exp appl 113: 77-86.
52. Fuxa JR (1993) Insect resistance to viruses. In: Beckage NE, Thompson SN, Federici BA, editors. Parasites and Pathogens of Insects. Vol. 2: Pathogens. Academic Press, San Diego: 197-209.
53. Ferrari J, Müller CB, Kraaijeveld AR, Godfray HCJ, (2001) Clonal variation and covariation in aphid resistance to parasitoids and a pathogen. Evolution 55: 1805-1814.
54. Cotter SC, Kruuk LEB, Wilson K, (2004) Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. J Evol Biol 17: 421-429.
55. Poitrineau K, Brown SP, Hochberg ME, (2003) Defence against multiple enemies. J Evol Biol 16: 1319-1327.