Trans-generational immune priming in honeybees

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1785, 2014, Pages

  López, Javier Hernández ^a   Schuehly, Wolfgang ^a   Crailsheim, Karl ^a   Riessberger Gallé, Ulrike ^a  

^a UNIVERSITY OF GRAZ   (Austria)

Author keywords

Artificial rearing; Haemocytes; Honeybees; Immune priming; Paenibacillus larvae

Indexed keywords

BACTERIUM; COLONY STRUCTURE; CORRELATION; HONEYBEE; IMMUNE SYSTEM; IMMUNITY; MOLECULAR ANALYSIS;

ANIMAL; ANIMAL FOOD; DIET; EQUIDAE; FEEDING BEHAVIOR; FEMALE; LION; MALE; PHYSIOLOGY; PREDATION; ZIMBABWE;

ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; DIET; EQUIDAE; FEEDING BEHAVIOR; FEMALE; LIONS; MALE; PHYSIOLOGY; PREDATORY BEHAVIOR; ZIMBABWE;

EID: 84899691286     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.0454     Document Type: Article

References (44)

1. Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA. 1996 The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86, 973-983. (doi:10.1016/S0092-8674(00)80172-5)
2. Elrod-Erickson M, Mishra S, Schneider D. 2000 Interactions between the cellular and humoral immune responses in Drosophila. Curr. Biol. 10, 781-784. (doi:10.1016/S0960-9822(00)00569-8)
3. Moret Y, Schmid-Hempel P. 2000 Survival for immunity: the price of immune system activation for bumblebee workers. Science 290, 1166-1168. (doi:10.1126/science.290.5494.1166)
4. Little TJ, Hultmark D, Read AF. 2005 Invertebrate immunity and the limits of mechanistic immunology. Nat. Immunol. 6, 651-654. (doi:10.1038/ni1219)
5. Schmid-Hempel P. 2005 Evolutionary ecology of insect immune defenses. Annu. Rev. Entomol. 50, 529-551. (doi:10.1146/annurev.ento.50. 071803.130420)
6. Evans JD et al. 2006 Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol. 15, 645-656. (doi:10.1111/j.1365-2583. 2006.00682.x)
7. Sadd BM, Schmid-Hempel P. 2009 A distinct infection cost associated with trans-generational priming of antibacterial immunity in bumble-bees. Biol. Lett. 5, 798-801. (doi:10.1098/rsbl.2009.0458)
8. Hoffmann JA, Reichhart JM. 2006 Drosophila innate immunity: an evolutionary perspective. Nat. Immunol. 3, 121-126. (doi:10.1038/ni0202-121)
9. Neves G, Zucker J, Daly M, Chess A. 2004 Stochastic yet biased expression of multiple Dscam splice variants by individual cells. Nat. Genet. 36, 240-246. (doi:10.1038/ng1299)
10. Schmid-Hempel P. 2005 Natural insect host-parasite systems show immune priming and specificity: puzzles to be solved. BioEssays 27, 1026-1034. (doi:10.1002/bies.20282)
11. Kurtz J. 2006 Specific memory within innate immune systems. Trends Immunol. 26, 186-192. (doi:10.1016/j.it.2005.02.001)
12. Watson FL, Püttmann-Holgado R, Thomas F, Lamar DL, Hughes M, Kondo M, Rebel VI, Schmucker D. 2005 Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309, 1874-1878. (doi:10.1126/science.1116887)
13. Sadd BM, Schmid-Hempel P. 2006 Insect immunity shows specificity in protection upon secondary pathogen exposure. Curr. Biol. 16, R1206-R1210. (doi:10.1016/j.cub.2006.04.047)
14. Roth O, Kurtz J. 2009 Strain-specific priming of resistance in the red flour beetle, Tribolium castaneum. Proc. R. Soc. B 276, 145-151. (doi:10. 1098/rspb.2008.1157)
15. Pham LN, Dionne MS, Shirasu-Hiza M, Schneider DS. 2007 A specific primed immune response in Drosophila is dependent on phagocytes. PLOS Pathogens 3, e26. (doi:10.1371/journal.ppat. 0030026)
16. Roth O, Kurtz J. 2009 Phagocytosis mediates specificity in the immune defence of an invertebrate, the woodlouse Porcellio scaber (Crustacea: Isopoda). Dev. Comp. Immunol. 11, 1151-1155. (doi:10.1016/j.dci.2009.04.005)
17. Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C. 2010 Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 329, 1353-1355. (doi:10. 1126/science.1190689)
18. Pope EC, Powell A, Roberts EC, Shields RJ, Wardle R, Rowley AF. 2011 Enhanced cellular Immunity in shrimp (Litopenaeus vannamei) after vaccination. PLoS ONE 6, e20960. (doi:10.1371/journal.pone. 0020960)
19. Bernardo J. 1996 Maternal effects in animal ecology. Am. Zool. 36, 83-105.
20. Grindstaff JL, Brodie III ED, Ketterson ED. 2003 Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proc. R. Soc. B 270, 2309-2319. (doi:10.1098/rspb.2003.2485)
21. 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. (doi:10. 1016/S0960-9822(03)00163-5)
22. Sadd BM, Kleinlogel I, Schmid-Hempel R, Schmid-Hempel P. 2005 Trans-generational immune priming in a social insect. Biol. Lett. 1, 386-388. (doi:10.1098/rsbl.2005.0369)
23. Moret Y. 2006 'Trans-generational immune priming': specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor. Proc. R. Soc. B 273, 1399-1405. (doi:10.1098/rspb. 2006.3465)
24. Tidbury HJ, Pedersen AB, Boots M. 2011 Within and trans-generational immune priming in an insect to a DNA virus. Proc. R. Soc. B 278, 871-876. (doi:10. 1098/rspb.2010.1517)
25. Freitak D, Heckel DG, Vogel H. 2009 Dietarydependent trans-generational immune priming in an insect herbivore. Proc. R. Soc. B 276, 2617-2624. (doi:10.1098/rspb.2009.0323)
26. Roth O, Joop G, Eggert H, Hilbert J, Daniel J, Schmid-Hempel P, Kurtz J. 2010 Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum. J. Anim. Ecol. 79, 403-413. (doi:10.1111/j.1365-2656.2009.01617.x)
27. Zanchi C, Troussard JP, Martinaud G, Moreau J, Moret Y. 2011 Differential expression and costs between maternally and paternally derived immune priming for offspring in an insect. J. Anim. Ecol. 80, 1174-1183. (doi:10.1111/j.1365-2656.2011. 01872.x)
28. Comman RS, Tarpy DR, Chen Y, Jeffreys L, Lopez D. 2012 Pathogen webs in collapsing honey bee colonies. PLoS ONE 7, e43562. (doi:10.1371/journal. pone.0043562)
29. Genersch E. 2010 American foulbrood in honeybees and its causative agent, Paenibacillus larvae. J. Invertebr. Pathol. 103, 10-19. (doi:10.1016/j.jip. 2009.06.015)
30. Fries I, Lindström A, Korpela S. 2006 Vertical transmission of American foulbrood (Paenibacillus larvae) in honey bees (Apis mellifera). Vet. Microbiol. 114, 269-274. (doi:10.1016/j.vetmic. 2005.11.068)
31. Forsgren E, Olofsson TC, Vásquez A, Fries I. 2010 Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 41, 99-108. (doi:10.1051/apido/2009065)
32. Genersch E, Forsgren E, Pentikäinen J, Ashiralieva A, Rauch S, Kilwinski J, Fries I. 2006 Reclassification of Paenibacillus larvae subsp. pulvifaciens and Paenibacillus larvae subsp. larvae as Paenibacillus larvae without subspecies differentiation. Int. J. Syst. Evol. Microbiol. 56, 501-511. (doi:10.1099/ijs.0. 63928-0)
33. Ashiralieva A, Genersch E. 2006 Reclassification, genotypes and virulence of Paenibacillus larvae, the etiological agent of American foulbrood in honeybees: a review. Apidologie 37, 411-420. (doi:10.1051/apido:2006028)
34. Fünfhaus A, Poppinga L, Genersch E. 2013 Identification and characterization of two novel toxins expressed by the lethal honey bee pathogen Paenibacillus larvae, the causative agent of American foulbrood. Environ. Microbiol. 15, 2951-2965. (doi:10.1111/ 1462-2920.12229)
35. Aupinel P, Fortini D, Dufour H, Tasei JN, Michaud B, Odoux JF, Pham-Delegue M-H. 2005 Improvement of artificial feeding in a standard in vitro method for rearing Apis mellifera larvae. Bull. Insectol. 58, 107-111.
36. Crailsheim K, Brodschneider R, Aupinel P, Behrens D, Genersch E, Vollmann J, Riessberger-Gallé U. 2013 Standard methods for artificial rearing of Apis mellifera larvae. J. Apicult. Res. 52, 1-14. (doi:10. 3896/IBRA.1.52.1.05)
37. Wang Z et al. 2011 A systematic study on hemocyte identification and plasma prophenoloxidase from Culex pipiens quinquefasciatus at different developmental stages. Exp. Parasitol. 127, 135-141. (doi:10.1016/j.exppara.2010.07.005)
38. Ribeiro C, Brehélin M. 2006 Insect haemocytes: what type of cell is that? J. Insect Physiol. 52, 417-429. (doi:10.1016/j.jinsphys.2006. 01.005)
39. Triggs AM, Knell RJ. 2012 Parental diet has strong transgenerational effects on offspring immunity. Func. Ecol. 26, 1409-1417. (doi:10.1111/j.1365-2435.2012.02051.x)
40. Sadd BM, Schmid-Hempel P. 2007 Facultative but persistent transgenerational immunity via the mother's eggs in bumblebees. Curr. Biol. 17, R1046-R1047. (doi:10.1016/j.cub.2007. 11.007)
41. Zanchi C, Troussard JP, Moreau J, Moret Y. 2012 Relationship between maternal transfer of immunity and mother fecundity in an insect. Proc. R. Soc. B 279, 3223-3230. (doi:10.1098/rspb. 2012.0493)
42. Moreau J, Martinaud G, Troussard JP, Zanchi C, Moret Y. 2012 Trans-generational immune priming is constrained by the maternal immune response in an insect. Oikos 121, 1828-1832. (doi:10.1111/j. 1600-0706.2011.19933.x)
43. Cremer S, Armitage SAO, Schmid-Hempel P. 2007 Social immunity. Curr. Biol. 17, R693-R701. (doi:10.1016/j.cub.2007.06.008)
44. Lavine MD, Strand MR. 2002 Insect hemocytes and their role in immunity. Ins. Biochem. Mol. Biol. 32, 1295-1309. (doi:10.1016/S0965-1748(02)00092-9)