Insect immune priming: ecology and experimental evidences

Ecological Entomology

Volumn 41, Issue 4, 2016, Pages 351-366

  Contreras Garduño, Jorge ^a,d   Lanz Mendoza, Humberto ^b   Franco, Bernardo ^a   Nava, Adriana ^c   Pedraza Reyes, Mario ^a   Canales Lazcano, Jorge ^c  

^a UNIVERSITY OF GUANAJUATO   (Mexico)

^b INSTITUTO NACIONAL DE SALUD PÚBLICA   (Mexico)

^c INSTITUTO DE ECOLOGÍA   (Mexico)

^d INSTITUTO DE MATEMÁTICAS   (Mexico)

Author keywords

Ecoimmunology; evolutionary immunology; host parasite interaction; immune memory; immune priming; immune response; immune specificity

Indexed keywords

ADAPTIVE MANAGEMENT; BACTERIUM; ECOLOGICAL APPROACH; EXPERIMENTAL STUDY; HOST-PARASITE INTERACTION; HOST-PATHOGEN INTERACTION; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOASSAY; INSECT; PARASITE RESISTANCE; PATHOGEN; VERTEBRATE;

BACTERIA (MICROORGANISMS); HEXAPODA; INVERTEBRATA; VERTEBRATA;

EID: 84963959925     PISSN: 03076946     EISSN: 13652311     Source Type: Journal    
DOI: 10.1111/een.12300     Document Type: Review

References (138)

1. Armitage, S.A., Peuß, R. & Kurtz, J. (2015) Dscam and pancrustacean immune memory: a review of the evidence. Developmental & Comparative Immunology, 48, 315–323.
2. Barrangou, R. & Marraffini, L.A. (2014) CRISPR–Cas systems: prokaryotes upgrade to adaptive immunity. Molecular Cell, 54, 234–244.
3. Best, A., Tidbury, H., White, A. & Boots, M. (2013) The evolutionary dynamics of within-generation immune priming in invertebrate hosts. Journal of the Royal Society Interface, 6, 1742–5662.
4. Bolte, S., Roth, O., Philipp, E.E., Saphörster, J., Rosenstiel, P. & Reusch, T.B. (2013) Specific immune priming in the invasive ctenophore Mnemiopsis leidyi. Biology Letters, 9, 20130864.
5. Boots, M. & Bowers, R.G. (2004) The evolution of resistance through costly acquired immunity. Proceedings of the Royal Society of London Series B: Biological Sciences, 271, 715–723.
6. Boots, M., Donnelly, R. & White, A. (2013) Optimal immune defence in the light of variation in lifespan. Parasite Immunology, 35, 331–338.
7. Bossdorf, O., Richards, C.L. & Pigliucci, M. (2008) Epigenetics for ecologists. Ecology Letters, 11, 106–115.
8. Brehélin, M. & Roch, P. (2008) Specificity, learning and memory in the innate immune response. Invertebrate Survival Journal, 5, 103–109.
9. Brey, P.T. (1998) The contributions of Pasteur school of insect immunology. Molecular Mechanisms of Immune Responses in Insects (ed. by P. T. Brey and D. Hultmark), pp. 1–39. Chapman & Hall, London, U.K.
10. Brownlie, J.C. & Johnson, K.N. (2009) Symbiont-mediated protection in insect hosts. Trends in Microbiology, 17, 348–354.
11. Buchon, N., Silverman, N. & Cherry, S. (2014) Immunity in Drosophila melanogaster [mdash] from microbial recognition to whole-organism physiology. Nature Reviews Immunology, 14, 796–810.
12. Christofi, T. & Apidianakis, Y. (2013) Drosophila immune priming against Pseudomonas aeruginosa is short-lasting and depends on cellular and humoral immunity. FlOOOResearch, 2, 76.
13. Cong, M., Song, L., Wang, L., Zhao, J., Qiu, L., Li, L. et al. (2008) The enhanced immune protection of Zhikong scallop Chlamys farreri on the secondary encounter with Listonella anguillarum. Comparative Biochemistry and Physiology Part B, 151, 191–196.
14. Contreras-Garduño, J., Rodríguez, M.C., Rodríguez, M.H., Alvarado-Delgado, A. & Lanz-Mendoza, H. (2014) Cost of immune priming within generations: trade-off between infection and reproduction. Microbes and Infection, 16, 261–267.
15. Contreras-Garduño, J., Rodríguez, M.C., Martínez, S.H., Barnetche, J.M., Alvarado, A., Izquierdo, J. et al. (2015) Plasmodium berghei induced priming in Anopheles albimanus independently of bacterial co-infection. Developmental & Comparative Immunology, 52, 172–181.
16. Cooper, E.L. (1992) Overview of immunoevolution. Bolletino di Zoologia, 59, 119–128.
17. Cooper, M.D. & Alder, M.N. (2006) The evolution of adaptive immune systems. Cell, 124, 815–822.
18. Cooper, E.L. & Roch, P. (1986) Second-set allograft responses in the earthworm Lumbriculus terrestris. Transplantation, 4, 514–520.
19. Corbet, P.S. (1999) Dragonflies Behavior and Ecology of Odonata. Cornell University Press, New York, New York.
20. Dong, Y., Taylor, H.E. & Dimopoulos, G. (2006) AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biology, 4, e229.
21. Dubovskiy, I.M., Whitten, M.M.A., Yaroslavtseva, O.N., Greig, C., Kryukov, V.Y., Kryukov, V.Y. et al. (2013) Can insects develop resistance to insect pathogenic fungi? PLoS ONE, 8, e60248.
22. Eggert, H., Kurtz, J. & Diddens-de Buhr, M.F. (2014) Different effects of paternal trans-generational immune priming on survival and immunity in step and genetic offspring. Proceedings of the Royal Society of London Series B: Biological Sciences, 281, 20142089.
23. Eggert, H., Diddens-de Buhr, M.F. & Kurtz, J. (2015) A temperature shock can lead to trans-generational immune priming in the Red Flour Beetle, Tribolium castaneum. Ecology and Evolution, 5, 1318–1326.
24. Eleftherianos, I., Atri, J., Accetta, J. & Castillo, J.C. (2013) Endosymbiotic bacteria in insects: guardians of the immune system? Frontiers in Physiology, 4, 46.
25. Elrod-Erickson, M., Mishra, S. & Schneider, D. (2000) Interactions between the cellular and humoral immune responses in Drosophila. Current Biology, 10, 781–784.
26. Faulhaber, L.M. & Karp, R.D. (1992) A diphasic immune response against bacteria in the American cockroach. Immunology, 75, 378–381.
27. Feldhaar, H. (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecological Entomology, 36, 533–543.
28. Fisher, J.J. & Hajek, A.E. (2015) Maternal exposure of a beetle to pathogens protects offspring against fungal disease. PLoS ONE, 10, e0125197.
29. Freitak, D., Heckel, D.G. & Vogel, H. (2009) Dietary-dependent trans-generational immune priming in an insect herbivore. Proceedings of the Royal Society of London B: Biological Sciences, 276, 2617–2624.
30. Freitak, D., Schmidtberg, H., Dickel, F., Lochnit, G., Vogel, H. & Vilcinskas, A. (2014) The maternal transfer of bacteria can mediate trans-generational immune priming in insects. Virulence, 5, 547–554.
31. Futo, M., Armitage, S.A.O. & Kurtz, J. (2016) Microbiota plays a role in oral immune priming in Tribolium castaneum. Frontiers in Microbiology, 6, 1383. DOI: 10.3389/fmicb.2015.01383.
32. Gálvez, D. & Chapuisat, M. (2014) Immune priming and pathogen resistance in ant queens. Ecology and Evolution, 4, 1761–1767.
33. Garbutt, J.S., O'Donoghue, A.J., McTaggart, S.J., Wilson, P.J. & Little, T.J. (2014) The development of pathogen resistance in Daphnia magna: implications for disease spread in age-structured populations. Journal of Experimental Biology, 217, 3929–3934.
34. Garnier, R., Boulinier, T. & Gandon, S. (2013) Evolution of the temporal persistence of immune protection. Biology Letters, 9, 20130017.
35. González-Tokman, D.M., González-Santoyo, I., Lanz-Mendoza, H. & Córdoba Aguilar, A. (2010) Territorial damselflies do not show immunological priming in the wild. Physiological Entomology, 35, 364–372.
36. Goren, M., Yosef, I., Edgar, R. & Qimron, U. (2012) The bacterial CRISPR/Cas system as analog of the mammalian adaptive immune system. RNA Biology, 9, 549–554.
37. Hartmann, R.S. & Karp, R.D. (1989) Short-term immunological memory in the allograft response of the American cockroach, Periplaneta americana. Transplantation, 43, 920–922.
38. Hauton, C., Brockton, V. & Smith, V.J. (2007) Changes in immune gene expression and resistance to bacterial infection in lobster (Homarus gammarus) post-larval stage VI following acute or chronic exposure to immune stimulating compounds. Molecular Immunology, 44, 443–450.
39. Hauton, C. & Smith, V.J. (2007) Adaptive immunity in invertebrates: a straw house without a mechanistic foundation. BioEssays, 29, 1138–1146.
40. Henter, H.J. & Via, S. (1995) The potential for coevolution in a host- parasitoid system. I. Genetic variation within an aphid population in susceptibility to a parasitic wasp. Evolution, 49, 427–438.
41. Hernández-Martínez, S., Román-Martínez, U., Martínez-Barnetche, J., Garrido, E., Rodríguez, M. H., & Lanz-Mendoza, H. (2006). Induction of DNA synthesis in Anopheles albimanus tissue cultures in response to a Saccharomyces cerevisiae challenge. Archives of insect biochemistry and physiology, 63(4), 147–158.
42. Hernández-López, J., Schuehly, W., Crailsheim, K. & Riessberger-Gallé, U. (2014) Trans-generationalimmune priming in honeybees. Proceedings of the Royal Society of London Series B: Biological Sciences, 281, 20140454.
43. Hernández-Martínez, P., Naseri, B., Navarro-Cerrillo, G., Escriche, B., Ferré, J. & Herrero, S. (2010) Increase in midgut microbiota load induces an apparent immune priming and increases tolerance to Bacillus thuringiensis. Environmental Microbiology, 12, 2730–2737.
44. Huang, C.C. & Song, Y.L. (1999) Maternal transmission of immunity to white spot syndrome associated virus (WSSV) in shrimp (Penaeus monodon). Developmental & Comparative Immunology, 23, 545–552.
45. Huang, W.S., Duan, L.P., Huang, B., Zhou, L.H., Liang, Y., Tu, C.L. et al. (2015) Identification of three IFN-γ inducible lysosomal thiol reductase (GILT)-like genes in mud crab Scylla paramamosain with distinct gene organisations and patterns of expression. Gene, 570, 78–88.
46. Hurst, G.D.D. & Hutchence, K.J. (2010) Host defence: getting by with a little help from our friends. Current Biology, 20, R806–R808.
47. Hutter, T., Gimbert, C., Bouchard, F. & Lapointe, F.J. (2015) Being human is a gut feeling. Microbiome, 3, 9.
48. Johnson, K.N., van Hulten, M.C. & Barnes, A.C. (2008) “Vaccination” of shrimp against viral pathogens: phenomenology and underlying mechanisms. Vaccine, 26, 4885–4892.
49. Jokela, J. (2010) Transgenerational immune priming as cryptic parental care. Journal of Animal Ecology, 79, 305–307.
50. Karp, R.D. (1990) Cell-mediated immunity in invertebrates. Bioscience, 40, 732–737.
51. Kato, L.M., Kawamoto, S., Maruya, M. & Fagarasan, S. (2014) The role of the adaptive immune system in regulation of gut microbiota. Immunological Reviews, 260, 67–75.
52. Kraaijeveld, A. & Godfray, H.C.J. (1997) Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature, 389, 278–280.
53. Kurtz, J. (2005) Specific memory within innate immune systems. Trends in Immunology, 26, 186–192.
54. Kurtz, J. & Armitage, S.A. (2006) Alternative adaptive immunity in invertebrates. Trends in Immunology, 27, 493–496.
55. Kurtz, J. & Franz, K. (2003) Innate defense: evidence for memory in invertebrate immunity. Nature, 425, 37–38.
56. Lazzaro, B.P., Sceurman, B.K. & Clark, A.G. (2004) Genetic basis of natural variation in D. melanogaster antibacterial immunity. Science, 303, 1873–1876.
57. Lin, Y.C., Chen, J.C., Morni, W.Z.W., Putra, D.F., Huang, C.L., Li, C.C. et al. (2013) Vaccination enhances early immune responses in white shrimp Litopenaeus vannamei after secondary exposure to Vibrio alginolyticus. PLoS ONE, 8, e69722.
58. Little, T.J. & Kraaijeveld, A.R. (2004) Ecological and evolutionary implications of immunological priming in invertebrates. Trends in Ecology and Evolution, 19, 58–60.
59. Little, T.J., O'Connor, B., Colegrave, N., Watt, K. & Read, A.F. (2003) Maternal transfer of strain-specific immunity in an invertebrate. Current Biology, 13, 489–492.
60. Little, T.J., Hultmark, D. & Read, A.F. (2005) Invertebrate immunity and the limits of mechanistic immunology. Nature Immunology, 6, 651–654.
61. Little, T.J., Colegrave, N., Sadd, B.M. & Schmid-Hempel, P. (2008) Studying immunity at the whole organism level. Bioessays, 30, 404–405.
62. Liu, K.J. (2000) Confidence intervals of the simple difference between the proportions of a primary infection and a secondary infection, given the primary infection. Biometrical Journal, 42, 59–69.
63. Longdon, B., Cao, C., Martinez, J. & Jiggins, F.M. (2013) Previous exposure to an RNA virus does not protect against subsequent infection in Drosophila melanogaster. PLoS ONE, 8, e73833.
64. López, S. (1998) Acquired resistance affects male sexual display and female choice in guppies. Proceedings of the Royal Society of London Series B: Biological Sciences, 265, 717–723.
65. Martin, L.B. II, Navara, K.J., Bailey, M.T., Hutch, C.R., Powell, N.D., Sheridan, J.F. et al. (2008) Food restriction compromises immune memory in deer mice (Peromyscus maniculatus) by reducing spleen-derived antibody-producing B cell numbers. Physiological and Biochemical Zoology, 81, 366–372.
66. Masri, L. & Cremer, S. (2014) Individual and social immunisation in insects. Trends in Immunology, 35, 471–482.
67. McKean, K.A. & Lazzaro, B.P. (2011) The costs of immunity and the evolution of immunological defense mechanisms. In Molecular Mechanisms of Life History Evolution (ed. by A. Heyland and T. Flatt). Oxford University Press, Oxford, U.K.
68. McNamara, K.B., Lieshout, E. & Simmons, L.W. (2014) The effect of maternal and paternal immune challenge on offspring immunity and reproduction in a cricket. Journal of Evolutionary Biology, 27, 1020–1028.
69. McTaggart, S.J., Wilson, P.J. & Little, T.J. (2012) Daphnia magna shows reduced infection upon secondary exposure to a pathogen. Biology Letters, 8, 972–975.
70. Mikonranta, L., Mappes, J., Kaukoniitty, M. & Freitak, D. (2014) Insect immunity: oral exposure to a bacterial pathogen elicits free radical response and protects from a recurring infection. Frontiers in Zoology, 11, 23.
71. Milutinović, B., Fritzlar, S. & Kurtz, J. (2014) Increased survival in the red flour beetle after oral priming with bacteria-conditioned media. Journal of Innate Immunity, 6, 306–314.
72. Miyashita, A., Kizaki, H., Kawasaki, K., Sekimizu, K. & Kaito, C. (2014) Primed immune responses to gram-negative peptidoglycans confer infection resistance in silkworms. The Journal of Biological Chemistry, 289, 14412–14421.
73. Moreau, J., Martinaud, G., Troussard, J.-P., Zanchi, C. & Moret, Y. (2012) Trans-generational immune priming is constrained by the maternal immune response in an insect. Oikos, 121, 1828–1832.
74. Moreno-García, M., Recio-totoró, B., Claudio-Piedras, F. & Lanz-Mendoza, H. (2014) Injury and immune response: applying the danger theory to mosquitoes. Frontiers in Plant Science, 5, 451.
75. Moret, Y. (2006) Trans-generational immune priming: specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor. Proceedings of the Royal Society of London Series B: Biological Sciences, 273, 1399–1405.
76. Moret, Y. & Schmid-Hempel, P. (2001) Facultative increase of offspring innate immune response after paternal challenge in an insect. Nature, 414, 506.
77. 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: Biological Sciences, 270, 2475–2480.
78. Morgan, X.C. & Huttenhower, C. (2014) Meta'omic analytic techniques for studying the intestinal microbiome. Gastroenterology, 146, 1437–1448.
79. Netea, M.G., Quintin, J. & van der Meer, J.W.M. (2011) Trained Immunity: A Memory for Innate Host Defense. Cell Host & Microbe, 9, 355–361.
80. Ng, T.H., Hung, H.Y., Chiang, Y.A., Lin, J.H., Chen, Y.N., Chuang, Y.C. et al. (2014) WSSV-induced crayfish Dscam shows durable immune behavior. Fish & Shellfish Immunology, 40, 78–90.
81. Norouzitallab, P., Baruah, K., Vandegehuchte, M., Van Stappen, G., Catania, F., Bussche, J.V. et al. (2014) Environmental heat stress induces epigenetic transgenerational inheritance of robustness in parthenogenetic Artemia model. FASEB Journal, 28, 3552–3563.
82. Norouzitallab, P., Biswas, P., Baruah, K. & Bossier, P. (2015) Multigenerational immune priming in an invertebrate parthenogenetic Artemia to a pathogenic Vibrio campbellii. Fish & Shellfish Immunology, 42, 426–429.
83. Ottaviani, E. (2015) Invertebrate immunological memory: could the epigenetic changes play the part of lymphocytes? Invertebrate Survival Journal, 12, 1–4.
84. Paust, S. & von Andrian, U.H. (2011) Natural killer cell memory. Nature Immunology, 12, 500–508.
85. Pham, L.N. & Schneider, D.S. (2008) Evidence for specificity and memory in the insect innate immune response. Insect Immunology, 97–127.
86. Pham, L.N., Dionne, M.S., Shirasu-Hiza, M. & Schneider, D.S. (2007) A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathogens, 3, e26.
87. Pope, E.C., Powell, A., Roberts, E.C., Shields, R.J., Wardle, R. & Rowley, A.F. (2011) Enhanced cellular immunity in shrimp (Litopenaeus vannamei) after vaccination. PLoS ONE, 6, e20960.
88. Portela, J., Duval, D., Rognon, A., Galinier, R., Boissier, J., Coustau, C. et al. (2013) Evidence for specific genotype-dependet immune priming in the Lophotrochozoan Biomphalaria glabrata snail. Journal of Innate Immunity, 5, 261–276.
89. Ramirez, J.L., de Almeida Oliveira, G., Calvo, E., Dalli, J., Colas, R.A., Serhan, C.N. et al. (2015) A mosquito lipoxin/lipocalin complex mediates innate immune priming in Anopheles gambiae. Nature Communications, 6, 7403.
90. Reber, A. & Chapuisat, M. (2012) No evidence for immune priming in ants exposed to a fungal pathogen. PLoS ONE, 7, e35372.
91. Rodrigues, J., Brayner, F.A., Alves, L.C., Dixit, R. & Barillas-Mury, C. (2010) Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science, 329, 1353–1355.
92. Rolff, J. & Siva-Jothy, M.T. (2003) Invertebrate ecological immunology. Science, 301, 472–475.
93. Rosengaus, R.B., Malak, T. & MacKintosh, C. (2013) Immune-priming in ant larvae: social immunity does not undermine individual immunity. Biology Letters, 9, 20130563.
94. Roth, O. & Kurtz, J. (2009) Phagocytosis mediates specificity in the immune defence of an invertebrate, the woodlouse Porcellio scaber (Crustacea: Isopoda). Developmental & Comparative Immunology, 33, 1151–1155.
95. Roth, O., Sadd, B.M., Schmid-Hempel, P. & Kurtz, J. (2009) Strain-specific immune priming in the red flour beetle, Tribolium castaneum. Proceedings of the Royal Society of London Series B: Biological Sciences, 276, 145–151.
96. Roth, O., Joop, G., Eggert, H., Hilbert, J., Daniel, J., Schmid-Hempel, P. et al. (2010) Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum. Journal of Animal Ecology, 79, 403–413.
97. Sadd, B.M. & Schmid-Hempel, P. (2006) Insect immunity shows specificity in protection upon secondary pathogen exposure. Current Biology, 16, 1206–1210.
98. Sadd, B.M. & Schmid-Hempel, P. (2007) Facultative but persistent transgenerational immunity via the mother's eggs in bumblebees. Current Biology, 17, R1046–R1047.
99. Sadd, B.M. & Schmid-Hempel, P. (2009a) Ecological and evolutionary implications of specific immune responses. Insect Infection and Immunity. Evolution, Ecology and Mechanism (ed. by J. Rolff and S. E. Reynolds), pp. 225–240. Oxford University Press, New York, New York.
100. Sadd, B.M. & Schmid-Hempel, P. (2009b) A distinct infection cost associated with trans-generational priming of antibacterial immunity in bumble-bees. Biology Letters, 5, 798–801.
101. Sadd, B.M., Kleinlogel, Y., Schmid-Hempel, R. & Schmid-Hempel, P. (2005) Trans-generational immune priming in a social insect. Biology Letters, 1, 386–388.
102. Salmela, H., Amdam, G.V. & Freitak, D. (2015) Transfer of immunity from mother to offspring is mediated via egg-yolk protein vitellogenin. PLoS Pathogens, 11, e1005015.
103. Schmid-Hempel, P. (2003) Variation in immune defense as a question in evolutionary ecology. Proceedings of the Royal Society of London Series B: Biological Sciences, 270, 357–366.
104. Schmid-Hempel, P. (2005a) Evolutionary ecology of insect immune defenses. Annual Review of Entomology, 50, 529–551.
105. Schmid-Hempel, P. (2005b) Natural insect host-parasite systems show immune priming and specificity–puzzles to be solved. BioEssays, 27, 1026–1034.
106. Schmid-Hempel, P. (2011) Evolutionary Parasitology. Oxford University Press, Oxford, U.K.
107. Schulenburg, H., Boehnisch, C. & Michiels, N.K. (2007) How do invertebrates generate a highly specific innate immune response? Molecular Immunology, 44, 3338–3344.
108. Shi, Z.H., Lin, Y.T. & Hou, Y.M. (2014) Mother-derived trans-generational immune priming in the red palm weevil, Rhynchophorus ferrugineus Olivier (Coleoptera, Dryophthoridae). Bulletin of Entomological Research, 104, 742–750.
109. Spoel, S.H. & Dong, X. (2012) How do plants achieve immunity? Defence without specialized immune cells. Nature Reviews Immunology, 12, 89–100.
110. Sun, J. & Deng, W.M. (2007) Hindsight mediates the role of notch in suppressing hedgehog signaling and cell proliferation. Developmental Cell, 12, 431–442.
111. Sun, J.C., Beilke, J.N. & Lanier, L.L. (2009) Adaptive immune features of natural killer cells. Nature, 457, 557–561.
112. Tate, A.T. & Graham, A.L. (2015) Trans-generational priming of resistance in wild flour beetles reflects the primed phenotypes of laboratory populations and is inhibited by co-infection with a common parasite. Functional Ecology, 29, 1059–1069.
113. Tate, A.T. & Rudolf, V.H.W. (2012) Immune priming across life stages and generations: implications for infectious disease dynamics in insects. Oikos, 121, 1083–1092.
114. Thaiss, C.A., Zeevi, D., Levy, M., Zilberman-Schapira, G., Suez, J., Tengeler, A.C. et al. (2014) Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis. Cell, 159, 514–529.
115. Thomas, A.M. & Rudolf, V.H.W. (2010) Challenges of metamorphosis in invertebrate hosts: maintaining parasite resistance across life-history stages. Ecological Entomology, 35, 200–205.
116. Tidbury, H.J., Pedersen, A.B. & Boots, M. (2011) Within and transgenerational immune priming in an insect to a DNA virus. Proceedings of the Royal Society of London Series B: Biological Sciences, 278, 871–876.
117. Tidbury, H.J., Best, A. & Boost, M. (2012) The epidemiological consequences of immune priming. Proceedings of the Royal Society of London Series B: Biological Sciences, 279, 4505–4512.
118. Trauer, U. & Hilker, M. (2013) Parental legacy in insects: variation of transgenerational immune priming during offspring development. PLoS ONE, 8, e63392.
119. Valdez, A., Yepiz-Plascencia, G., Ricca, E. & Olmos, J. (2014) First Litopenaeus vannamei WSSV 100% oral vaccination protection using CotC::Vp26 fusion protein displayed on Bacillus subtilis spores surface. Journal of Applied Microbiology, 117, 347–357.
120. Valtonen, T.M., Kleino, A., Rämet, M. & Rantala, M.J. (2010) Starvation reveals maintenance cost of humoral immunity. Evolutionary Biology, 37, 49–57.
121. Vantaux, A., Dabiré, K.R., Cohuet, A. & Lefèvre, T. (2014) A heavy legacy: offspring of malaria-infected mosquitoes show reduced disease resistance. Malaria Journal, 13, 442.
122. Viney, M.E., Riley, E.M. & Buchanan, K.L. (2005) Optimal immune responses: immunocompetence revisited. Trends in Ecology & Evolution, 20, 665–669.
123. Voordouw, M.J., Lambrechts, L. & Koella, J. (2008) No maternal effects after stimulation of the melanization response in the yellow fever mosquito Aedes aegypti. Oikos, 117, 1269–1279.
124. Vorburger, C., Gegenschatz, S.E., Ranieri, G. & Rodriguez, P. (2008) Limited scope for maternal effects in aphid defence against parasitoids. Ecological Entomology, 33, 189–196.
125. Wang, L., Yue, F., Song, X. & Song, L. (2015) Maternal immune transfer in mollusc. Developmental & Comparative Immunology, 48, 354–359.
126. Watson, F.L., Puttmann-Holgado, R., Thomas, F., Lamar, D.L., Hughes, M., Kondo, M. et al. (2005) Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science, 309, 1874–1878.
127. Wilson, K. & Graham, R.I. (2015) Transgenerational effects modulate density-dependent prophylactic resistance to viral infection in a lepidopteran pest. Biology Letters, 11, 20150012.
128. Weiss, B. & Aksoy, S. (2011) Microbiome influences on insect host vector competence. Trends in Parasitology, 27, 514–522.
129. West, C.E., Renz, H., Jenmalm, M.C., Kozyrskyj, A.L., Allen, K.J., Vuillermin, P. et al. (2015) The gut microbiota and inflammatory noncommunicable diseases: associations and potentials for gut microbiota therapies. Journal of Allergy and Clinical Immunology, 135, 3–13.
130. Witteveldt, J., Cifuentes, C.C., Vlak, J.M. & van Hulten, M.C.W. (2004) Protection of Penaeus monodon against white spot syndrome virus by oral vaccination. Journal of Virology, 78, 2057–2061.
131. Wu, G., Zhao, Z., Liu, C. & Qiu, L. (2014) Priming Galleria mellonella (Lepidoptera: Pyralidae) larvae with heat-killed bacterial cells induced an enhanced immune protection against Photorhabdus luminescens TT01 and the role of innate immunity in the process. Journal of Economic Entomology, 107, 559–569.
132. Wu, G., Li, M., Liu, Y., Ding, Y. & Yi, Y. (2015a) The specificity of immune priming in silkworm, Bombyx mori, is mediated by the phagocytic ability of granular cells. Journal of Insect Physiology, 81, 60–68.
133. Wu, G., Yi, Y., Sun, J., Li, M. & Qiu, L. (2015b) No evidence for priming response in Galleria mellonella larvae exposed to toxin protein PirA 2 B 2 from Photorhabdus luminescens TT01: an association with the inhibition of the host cellular immunity. Vaccine, 33, 6307–6313.
134. Wu, G., Yi, Y., Lv, Y., Li, M., Wang, J. & Qiu, L. (2015c) The lipopolysaccharide (LPS) of Photorhabdus luminescens TT01 can elicit dose-and time-dependent immune priming in Galleria mellonella larvae. Journal of Invertebrate Pathology, 127, 63–72.
135. Yue, F., Zhou, Z., Wang, L., Ma, Z., Wang, J., Wang, M. et al. (2013) Maternal transfer of immunity in scallop Chlamys farreri and its trans-generational immune protection to offspring against bacterial challenge. Developmental & Comparative Immunology, 41, 569–577.
136. Zanchi, C., Troussard, J.-P., Martinaud, G., Moreau, J. & Moret, Y. (2011) Differential expression and costs between maternally and paternally derived immune priming for offspring in an insect. Journal of Animal Ecology, 80, 1174–1183.
137. Zhang, T., Qiu, L., Sun, Z., Wang, L., Zhou, Z., Liu, R. et al. (2014) The specifically enhanced cellular immune responses in Pacific oyster (Crassostrea gigas) against secondary challenge with Vibrio splendus. Developmental and Comparative Immunology, 45, 141–150.
138. Zhao, Z., Wu, G., Wang, J., Liu, C. & Qiu, L. (2013) Next-generation sequencing-based transcriptome analysis of Helicoverpa armigera larvae immune-primed with Photorhabdus luminescens TT01. PLoS ONE, 8, e80146.