Chapter 6 Variation of Leptopilina boulardi Success in Drosophila Hosts. What is Inside the Black Box?

Advances in Parasitology

Volumn 70, Issue , 2009, Pages 147-188

  Dubuffet, A ^a   Colinet, D ^b   Anselme, C ^b   Dupas, S ^d,e   Carton, Y ^d   Poirie M ^c  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b CEMAGREF   (France)

^c Institut Sophia Agrobiotech   (France)

^d CNRS   (France)

^e PONTIFICIA UNIVERSIDAD CATÓLICA DEL ECUADOR   (Ecuador)

Author keywords

[No Author keywords available]

Indexed keywords

ASOBARA TABIDA; DROSOPHILA; ENCAPSULATION; GENETIC VARIABILITY; HEREDITY; HOST; HOST PARASITE INTERACTION; HOST RESISTANCE; INTERSPECIFIC RELATIONSHIP; LEPTOPILINA BOULARDI; MOLECULAR EVOLUTION; MOLECULAR MECHANICS; NONHUMAN; PARASITE; PARASITOID; PHYSIOLOGY; PRIORITY JOURNAL; REVIEW; VIRULENCE; ANIMAL; DROSOPHILA MELANOGASTER; GENETICS; INNATE IMMUNITY; METABOLISM; PARASITOLOGY; PATHOGENICITY; WASP;

ASOBARA TABIDA; LEPTOPILINA BOULARDI;

VIRULENCE FACTOR; WASP VENOM;

ANIMALS; DROSOPHILA; DROSOPHILA MELANOGASTER; GENETIC VARIATION; HOST-PARASITE INTERACTIONS; IMMUNITY, INNATE; VIRULENCE FACTORS; WASP VENOMS; WASPS;

EID: 70349164362     PISSN: 0065308X     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0065-308X(09)70006-5     Document Type: Review

References (114)

1. Asgari S., Zhang G., Zareie R., and Schmidt O. A serine proteinase homolog venom protein from an endoparasitoid wasp inhibits melanization of the host hemolymph. Insect Biochem. Mol. Biol. 33 (2003) 1017-1024
2. Baker D.A., Mille-Baker B., Wainwright S.M., Ish-Horowicz D., and Dibb N.J. Mae mediates MAP kinase phosphorylation of Ets transcription factors in Drosophila. Nature 411 (2001) 330-334
3. Barratt B.I.P., Evans A.A., Stoltz D.B., Vinson S.B., and Easingwood R. Virus-like particles in the ovaries of Microctonus aethiopoides Loan (Hymenoptera: Braconidae), a parasitoid of adult weevils (Coleoptera: Curculionidae). J. Invert. Pathol. 73 (1999) 182-188
4. Beck M.H., and Strand M.R. A novel polydnavirus protein inhibits the insect prophenoloxidase activation pathway. Proc. Natl. Acad. Sci. USA 104 (2007) 19267-19272
5. Benassi V., Frey F., and Carton Y. A new specific gene for wasp cellular immune resistance in Drosophila. Heredity 80 (1998) 347-352
6. Bensadia F., Boudreault S., Guay J.-F., Michaud D., and Cloutier C. Aphid clonal resistance to a parasitoid fails under heat stress. J. Insect Physiol. 52 (2006) 146-157
7. Bezier A., Annaheim M., Herbiniere J., Wetterwald C., Gyapay G., Bernard-Samain S., et al. Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science 323 (2009) 926-930
8. Blumberg D. Parasitoid encapsulation as a defense mechanism in the Coccoidea (Homoptera) and its importance in biological control. Biol. Control. 8 (1997) 225-236
9. Blumberg D., and Van Driesche R.G. Encapsulation rates of three encyrtid parasitoids by three mealybug species (Homoptera: Pseudococcidae) found commonly as pests in commercial greenhouses. Biol. Control. 22 (2001) 191-199
10. Brodeur J., and Vet L.E.M. Relationships between parasitoid host range and host defence: a comparative study of egg encapsulation in two related parasitoid species. Physiol. Entomol. 20 (1995) 7-12
11. Calatayud P.A., Polania M.A., Seligmann C.D., and Bellotti A.C. Influence of water-stressed cassava on Phenacoccus herreni and three associated parasitoids. Entomol. Exp. Appl. 102 (2002) 163-175
12. Carius H.J., Little T.J., and Ebert D. Genetic variation in a host-parasite association: potential for coevolution and frequency-dependant selection. Evolution 55 (2001) 1136-1145
13. Carton Y., and Boulétreau M. Encapsulation ability of Drosophila melanogaster: a genetic analysis. Dev. Comp. Immunol. 9 (1985) 211-219
14. Carton Y., and Kitano H. Evolutionary relationships to parasitism by seven species of the Drosophila melanogaster subgroup. Biol. J. Linn. Soc. 16 (1981) 227-241
15. Carton Y., Capy P., and Nappi A.J. Genetic variability of host-parasite relationship traits: utilisation of isofemale lines on a Drosophila parasitic wasp. Genet. Select. Evol. 21 (1989) 437-446
16. Carton Y., Frey F., and Nappi A.J. Genetic determinism of the cellular immune reaction in Drosophila melanogaster. Heredity 69 (1992) 393-399
17. Carton Y., Nappi A., and Poirié M. Genetics of anti-parasite resistance in invertebrates. Dev. Comp. Immunol. 29 (2005) 9-32
18. Carton Y., Poirié M., and Nappi A.J. Insect immune resistance to parasitoids. Insect Sci. 15 (2008) 67-87
19. Cerenius L., Lee B.L., and Soderhall K. The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol. 29 (2008) 263-271
20. Chiu H., Morales J., and Govind S. Identification and immuno-electron microscopy localization of p40, a protein component of immunosuppressive virus-like particles from Leptopilina heterotoma, a virulent parasitoid wasp of Drosophila. J. Gen. Virol. 87 (2006) 461-470
21. Chiu H., Sorrentino R.P., and Govind S. Suppression of the Drosophila cellular immune response by Ganaspis xanthopoda. Adv. Exp. Med. Biol. 484 (2000) 161-167
22. Colinet D., Dubuffet A., Cazes D., Moreau S., Drezen J.M., and Poirié M. A serpin from the parasitoid wasp Leptopilina boulardi targets the Drosophila phenoloxidase cascade. Dev. Comp. Immunol. 33 (2009) 681-689
23. Colinet D., Schmitz A., Depoix D., Crochard D., and Poirié M. Convergent use of RhoGAP toxins by eukaryotic parasites and bacterial pathogens. PLoS Pathog. 3 (2007) e203
24. David J.R., Gibert P., Legout H., Petavy G., Capy P., and Moreteau B. Isofemale lines in Drosophila: an empirical approach to quantitative trait analysis in natural populations. Heredity 94 (2005) 3-12
25. De Gregorio E., Han S.-J., Lee W.-J., Baek M.-J., Osaki T., Kawabata S.-I., et al. An immune-responsive serpin regulates the melanization cascade in Drosophila. Dev. Cell. 3 (2002) 581-592
26. Delpuech J.M., Frey F., and Carton Y. Action of insecticides on the cellular immune reaction of Drosophila melanogaster against the parasitoid Leptopilina boulardi. Environ. Toxicol. Chem. 15 (1996) 2267-2271
27. Dubuffet A., Doury G., Labrousse C., Drezen J.M., Carton Y., and Poirié M. Variation of success of Leptopilina boulardi in Drosophila yakuba: the mechanisms explored. Dev. Comp. Immunol. 32 (2008) 597-602
28. Dubuffet A., Dupas S., Frey F., Drezen J.-M., Poirié M., and Carton Y. Genetic interactions between the parasitoid wasp Leptopilina boulardi and its Drosophila hosts. Heredity 98 (2007) 21-27
29. Dupas S., and Boscaro M. Geographic variation and evolution of immunosuppressive genes in a Drosophila parasitoid. Ecography 22 (1999) 284-291
30. Dupas S., and Carton Y. Two non-linked genes for specific virulence of Leptopilina boulardi against Drosophila melanogaster and D. yakuba. Evol. Ecol. 13 (1999) 211-220
31. Dupas S., Brehélin M., Frey F., and Carton Y. Immune suppressive virus-like particles in a Drosophila parasitoid: significance of their intraspecific morphological variations. Parasitology 113 (1996) 207-212
32. Dupas S., Carton Y., and Poirié M. Genetic dimension of the coevolution of virulence-resistance in Drosophila-parasitoid wasp relationships. Heredity 90 (2003) 83-89
33. Dupas S., Frey F., and Carton Y. A single parasitoid segregating factor controls immune suppression in Drosophila. J. Heredity 89 (1998) 306-311
34. Dupas S., Gitau C.W., Branca A., Le Ru B.P., and Silvain J.F. Evolution of a polydnavirus gene in relation to parasitoid-host species immune resistance. J. Heredity 99 (2008) 491-499
35. Eslin P., and Doury G. The fly Drosophila subobscura: a natural case of innate immunity deficiency. Dev. Comp. Immunol. 30 (2006) 977-983
36. Eslin P., and Prévost G. Hemocyte load and immune resistance to Asobara tabida are correlated in species of the Drosophila melanogaster subgroup. J. Insect Physiol. 44 (1998) 807-816
37. Espagne E., Dupuy C., Huguet E., Cattolico L., Provost B., Martins N., et al. Genome sequence of a polydnavirus: insights into symbiotic virus evolution. Science 306 (2004) 286-289
38. Fellowes M.D., Kraaijeveld A.R., and Godfray H.C. Trade-off associated with selection for increased ability to resist parasitoid attack in Drosophila melanogaster. Proc. R. Soc. Lond. B 265 (1998) 1553-1558
39. Fellowes M.D.E., Kraaijeveld A.R., and Godfray H.C.J. Cross-resistance following artificial selection for increased defense against parasitoids in Drosophila melanogaster. Evolution 53 (1999) 966-972
40. Fleury F., Ris N., Allemand R., Fouillet P., Carton Y., and Boulétreau M. Ecological and genetic interactions in Drosophila-parasitoids communities: a case study with D. melanogaster, D. simulans and their common Leptopilina parasitoids in south-eastern France. Genetica 120 (2004) 181-194
41. Fytrou A., Schofield P.G., Kraaijeveld A.R., and Hubbard S.F. Wolbachia infection suppresses both host defence and parasitoid counter-defence. Proc. R. Soc. Lond. B 273 (2006) 791-796
42. Gitau C.W., Dupas S., Ngi-Song A.J., Mbugi J.P., and Schulthess F. Calyx fluid proteins of two Cotesia sesamiae (Cameron) (Hymenoptera: Braconidae) biotypes in Kenya: implications to biological control of the stem borer Busseola fusca (Fuller) (Lepidoptera: Noctuidae). Ann. Soc. Entomol. France 42 (2006) 433-441
43. Gitau C.W., Gundersen-Rindal D., Pedroni M., Mbugi J.P., and Dupas S. Differential expression of the CrV1 haemocyte inactivation-associated polydnavirus gene in the African maize stem borer Busseola fusca (Fuller) parasitized by two biotypes of the endoparasitoid Cotesia sesamiae (Cameron). J. Insect Physiol. 53 (2007) 676-684
44. Glatz R.V., Asgari S., and Schmidt O. Evolution of polydnaviruses as insect immune suppressors. Trends Microbiol. 12 (2004) 545-554
45. Govind S. Innate immunity in Drosophila: pathogens and pathways. Insect Sci. 15 (2008) 29-43
46. Haine E.R. Symbiont-mediated protection. Proc. R. Soc. Lond. B 275 (2008) 353-361
47. Henter H.J. The potential for coevolution in a host-parasitoid system. II. Genetic variation within a population of wasps in the ability to parasitize an aphid population. Evolution 49 (1995) 439-445
48. Hita M., Espagne E., Huguet E., Pascual L., and Poirié M. Mapping candidate genes for Drosophila melanogaster resistance to the parasitoid wasp Leptopilina boulardi. Genet. Res. 88 (2006) 81-91
49. Hita M.T., Poirié M., Leblanc N., Lemeunier F., Lutcher F., Frey F., et al. Genetic localization of a Drosophila melanogaster resistance gene to a parasitoid wasp and physical mapping of the region. Genome Res. 9 (1999) 471-481
50. Irving P., Ubeda J.-M., Doucet D., Troxler L., Lagueux M., Zachary D., et al. New insights into Drosophila larval haemocyte functions through genome-wide analysis. Cell. Microbiol. 7 (2005) 335-350
51. Jiang H., Wang Y., Yu X.-Q., Zhu Y., and Kanost M.R. Prophenoloxidase-activating proteinase-3 (PAP-3) from Manduca sexta hemolymph: a clip-domain serine proteinase regulated by serpin-1J and serine proteinase homologs. Insect Biochem. Mol. Biol. 33 (2003) 1049-1060
52. Kanost M.R., Jiang H., and Yu X.-Q. Innate immune responses of a lepidopteran insect: Manduca sexta. Immunol. Rev. 198 (2004) 97-105
53. Karimzadeh J., and Wright D.J. Bottom-up cascading effects in a tritrophic system: interactions between plant quality and host-parasitoid immune responses. Ecol. Entomol. 33 (2008) 45-52
54. Kraaijeveld A.R. Kleptoparasitism as an exploitation for paradoxical oviposition decisions of the parasitoid Asobara tabida. J. Evol. Biol. 12 (1999) 123-133
55. Kraaijeveld A.R., and Godfray H.C.J. Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389 (1997) 278-280
56. Kraaijeveld A.R., and Godfray H.C.J. Geographic patterns in the evolution of resistance and virulence in Drosophila and its parasitoids. Am. Nat. 153 (1999) S61-S74
57. Kraaijeveld A.R., and Godfray H.C.J. Is there local adaptation in Drosophila-parasitoid interactions?. Evol. Ecol. 3 (2001) 107-116
58. Kraaijeveld A.R., and van Alphen J.J.M. Geographical variation in resistance of the parasitoid A. tabida against encapsulation by D. melanogaster larvae: the mechanism explored. Physiol. Entomol. 19 (1994) 9-14
59. Kraaijeveld A.R., and van Alphen J.J.M. Geographical variation in encapsulation ability of Drosophila melanogaster larvae and evidence for parasitoid-specific components. Evol. Ecol. 9 (1995) 10-17
60. Kraaijeveld A.R., Limentani E.C., and Godfray H.C.J. Basis of the trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Proc. R. Soc. Lond. B 268 (2001) 259-261
61. Kraaijeveld A.R., van Alphen J.J.M., and Godfray H.C.J. The coevolution of host resistance and parasitoid virulence. Parasitology 116 (1998) S29-S45
62. Labrosse C., Carton Y., Dubuffet A., Drezen J.M., and Poirié M. Active suppression of D. melanogaster immune response by long gland products of the parasitic wasp Leptopilina boulardi. J. Insect Physiol. 49 (2003) 513-522
63. Labrosse C., Eslin P., Doury G., Drezen J.-M., and Poirié M. 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. Insect Physiol. 51 (2005) 161-170
64. Labrosse C., Stasiak K., Lesobre J., Grangeia A., Huguet E., Drezen J.-M., et al. A RhoGAP protein as a main immune suppressive factor in the Leptopilina boulardi (Hymenoptera, Figitidae)-Drosophila melanogaster interaction. Insect Biochem. Mol. Biol. 35 (2005) 93-103
65. Lambrechts L., Halbert J., Durand P., Gouagna L.C., and Koella J.C. Host genotype by parasite genotype interactions underlying the resistance of anopheline mosquitoes to Plasmodium falciparum. Malaria J. 4 3 (2005) 16-23
66. Lanot R., Zachary D., Holder F., and Meister M. Postembryonic hematopoiesis in Drosophila. Dev. Biol. 230 (2001) 243-257
67. Law R.H.P., Zhang Q., McGowan S., Buckle A.M., Silverman G.A., Wong W., et al. An overview of the serpin superfamily. Genome Biol. 7 5 (2006) 216
68. Lazzaro B.P., and Little T.J. Immunity in a variable world. Philosophical Trans. R. Soc. B 364 (2009) 15-26
69. Ling E., and Yu X.-Q. Prophenoloxidase binds to the surface of hemocytes and is involved in hemocyte melanization in Manduca sexta. Insect Biochem. Mol. Biol. 35 (2005) 1356-1366
70. Markus R., Laurinyecz B., Kurucz E., Honti V., Bajusz I., Sipos B., et al. Sessile hemocytes as a hematopoietic compartment in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 106 12 (2009) 4805-4809
71. Mochiah M.B., Ngi-Song A.J., Overholt W.A., and Stouthamer R. Effects of calyx fluid from two populations of Cotesia sesamiae on Busseola fusca (Lepidoptera: Noctuidae). Insect Sci. Appl. 21 (2002) 369-374
72. Mohamed S.A., Overholt W.A., Wharton R.A., Lux S.A., and Eltoum E.M. Host specificity of Psyttalia cosyrae (Hymenoptera: Braconidae) and the effect of different host species on parasitoid fitness. Biol. Cont. 28 (2003) 155-163
73. Morales J., Chiu H., Oo T., Plaza R., Hoskins S., and Govind S. Biogenesis, structure, and immune-suppressive effects of virus-like particles of a Drosophila parasitoid, Leptopilina victoriae. J. Insect Physiol. 51 (2005) 181-195
74. Moreau S.J.M., and Guillot S. Advances and prospects on biosynthesis, structures and functions of venom proteins from parasitic wasps. Insect Biochem. Mol. Biol. 35 (2005) 1209-1223
75. Nam H.J., Jang I.H., Asano T., and Lee W.J. Involvement of pro-phenoloxidase 3 in lamellocyte-mediated spontaneous melanization in Drosophila. Mol. Cells. 26 6 (2008) 606-610
76. Nappi A.J. Defense reactions of Drosophila euronotus larvae against the hymenopterous parasite Pseudeucoila bochei. J. Invert. Pathol. 16 (1970) 408-418
77. Nappi A.J., Frey F., and Carton Y. Drosophila serpin 27A is a likely target for immune suppression of the blood cell-mediated melanotic encapsulation response. J. Insect Physiol. 51 (2005) 197-205
78. Ngi-Song A.J., Overholt W.A., and Stouthamer R. Suitability of Busseola fusca and Sesamia calamistis (Lepidoptera: Noctuidae) for the development of two populations of Cotesia sesamiae (Hymenoptera: Braconidae) in Kenya. Biol. Cont. 12 (1998) 208-214
79. Ojala K., Julkunen-Tiitto R., Lindstrom L., and Mappes J. Diet affects the immune defense and life-history traits of an Artiid moth Parasemia plantaginis. Evol. Ecol. Res. 7 (2005) 1153-1170
80. Oliver K.M., Russell J.A., Moran N.A., and Hunter M.S. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Natl. Acad. Sci. USA 100 (2003) 1803-1807
81. Orr H.A., and Irving S. The genetics of adaptation - the genetic basis of resistance to wasp parasitism in Drosophila melanogaster. Evolution 51 (1997) 1877-1885
82. Pennacchio F., and Strand M.R. Evolution of developmental strategies in parasitic hymenoptera. Ann. Rev. Entomol. 51 (2006) 233-258
83. Poirié M., Carton Y., and Dubuffet A. Virulence strategies in parasitoid Hymenoptera as an example of adaptive diversity. C. R. Biol. 332 (2009) 311-320
84. Poirié M., Frey F., Hita M., Huguet E., Lemeunier F., Periquet G., and Carton Y. Drosophila resistance genes to parasitoids: chromosomal location and linkage analysis. Proc. R. Soc. Lond. B 267 (2000) 1417-1421
85. Prévost G., Eslin P., Doury G., Moreau S.J.M., and Guillot S. Asobara, braconid parasitoids of Drosophila larvae: unusual strategies to avoid encapsulation without VLPs. J. Insect Physiol. 51 (2005) 171-179
86. Reineke A., Asgari S., and Schmidt O. Evolutionary Origin of Venturia canescens virus-like particles. Arch. Insect Biochem. Physiol. 61 (2006) 123-133
87. Reineke A., Asgari S., Ma G., Beck M., and Schmidt O. Sequence analysis and expression of a viral-like particle protein, VLP2, from the parasitoid wasp Venturia canescens. Insect Mol. Biol. 11 (2002) 233-239
88. Renault S., Stasiak K., Federici B., and Bigot Y. Commensal and mutualistic relationships of reoviruses with their parasitoid wasp hosts. J. Insect Physiol. 51 (2005) 137-148
89. Rizki R.M., and Rizki T.M. Selective destruction of a host blood cell type by a parasitoid wasp. Proc. Natl. Acad. Sci. USA 81 (1984) 6154-6158
90. Rizki R.M., and Rizki T.M. Parasitoid virus-like particles destroy Drosophila cellular immunity. Proc. Natl. Acad. Sci. USA 87 (1990) 8388-8392
91. Rizki R.M., and Rizki T.M. Effects of lamellolysin from a parasitoid wasp on Drosophila blood cells in vitro. J. Exp. Zool. 257 (1991) 236-244
92. Rizki T., Rizki R., and Grell E. A mutant affecting the crystal cells in Drosophila melanogaster. Wilhelm Roux's Arch. 188 (1980) 91-99
93. Rizki T.M., and Rizki R.M. Paracristalline inclusions of Drosophila melanogaster hemocytes have prophenoloxidases. Genetics 110 (1985) 598
94. Rizki T.M., and Rizki R.M. Lamellocyte differentiation in Drosophila larvae parasitized by Leptopilina. Dev. Comp. Immunol. 16 (1992) 103-110
95. Rizki T.M., and Rizki R.M. Parasitoid-induced cellular immune deficiency in Drosophila. Ann. N. Y. Acad. Sci. 712 (1994) 178-194
96. Rizki T.M., Rizki R.M., and Carton Y. Leptopilina heterotoma and L. boulardi: strategies to avoid cellular defense responses of Drosophila melanogaster. Exp. Parasitol. 70 (1990) 466-475
97. Rogge R., Green P.J., Urano J., Horn-Saban S., Mlodzik M., Shilo B.Z., Hartenstein V., and Banerjee U. The role of yan in mediating the choice between cell division and differentiation. Development 121 (1995) 3947-3958
98. Russo J., Brehélin M., and Carton Y. Haemocyte changes in resistant and susceptible strains of D. melanogaster caused by virulent and avirulent strains of the parasitic wasp Leptopilina boulardi. J. Insect Physiol. 47 (2001) 167-172
99. Sagarra L.A., Peterkin D.D., Vincent C., and Stewart R.K. Immune response of the hibiscus mealybug, Maconellicoccus hirsutus Green (Homoptera: Pseudococcidae), to oviposition of the parasitoid Anagyrus kamali Moursi (Hymenoptera: Encyrtidae). J. Insect Physiol. 46 (2000) 647-653
100. Satoh D., Horii A., Ochiai M., and Ashida M. Prophenoloxidase-activating enzyme of the silkworm, Bombyx mori. Purification, characterization, and cDNA cloning. J. Biol. Chem. 274 (1999) 7441-7453
101. Schlenke T.A., Morales J., Govind S., and Clark A.G. Contrasting infection strategies in generalist and specialist wasp parasitoids of Drosophila melanogaster. PLoS Pathog. 3 (2007) e158
102. Schmidt O., Theopold U., and Strand M. Innate immunity and its evasion and suppression by hymenopteran endoparasitoids. Bioessays 23 (2001) 344-351
103. Serbielle C., Chowdhury S., Pichon S., Dupas S., Lesobre J., Purisima E.O., et al. Viral cystatin evolution and three-dimensional structure modelling: a case of directional selection acting on a viral protein involved in a host-parasitoid interaction. BMC Biol. 6 (2008) 38
104. Sorrentino R.P., Carton Y., and Govind S. Cellular immune response to parasite infection in the Drosophila lymph gland is developmentally regulated. Dev. Biol. 243 (2002) 65-80
105. Suzuki M., and Tanaka T. Virus-like particles in venom of Meteorus pulchricornis induce host hemocyte apoptosis. J. Insect Physiol. 52 (2006) 602-613
106. Thompson J.N. The geographic mosaic of coevolution (2005), University of Chicago Press, Chicago, IL
107. Vass E., Nappi A.J., and Carton Y. Comparative study of immune competence and host susceptibility in Drosophila melanogaster parasitized by Leptopilina boulardi and Asobara tabida. J. Parasitol. 79 (1993) 106-112
108. Vorburger C., Sandrock C., Gouskov A., Castañeda L.E., and Ferrari J. Genotypic variation and the role of defensive endosymbionts in all-parthenogenetic host-parasitoid interaction. Evolution 63 6 (2009) 1439-1450
109. Walker I. Die Abwehrreaktion des Wirtes Drosophila melanogaster gegen die zoophage Cynipidae Pseudocoila bochei Weld. Rev. Suisse Zool. 66 (1959) 569-632
110. Wertheim B., Kraaijeveld A.R., Schuster E., Blanc E., Hopkins M., Pletcher S.D., Strand M.R., Partridge L., and Godfray H.C.J. Genome-wide gene expression in response to parasitoid attack in Drosophila. Genome Biol. 6 (2005) R94
111. Wilfert L., and Schmid-Hempel P. The genetic architecture of susceptibility to parasites. BMC Evol. Biol. 8 (2008) 187
112. Williams M.J., Ando I., and Hultmark D. Drosophila melanogaster Rac2 is necessary for a proper cellular immune response. Genes Cells 10 (2005) 813-823
113. Williams M.J., Wiklund M.-L., Wikman S., and Hultmark D. Rac1 signalling in the Drosophila larval cellular immune response. J. Cell Sci. 119 (2006) 2015-2025
114. Zettervall C.-J., Anderl I., Williams M.J., Palmer R., Kurucz E., and Andó I. A directed screen for genes involved in Drosophila blood cell activation. Proc. Natl. Acad. Sci. USA 101 (2004) 14192-14197