Nutrition, immunity and viral infections in honey bees

Current Opinion in Insect Science

Volumn 10, Issue , 2015, Pages 170-176

  DeGrandi Hoffman, Gloria ^a   Chen, Yanping ^b  

^a CARL HAYDEN BEE RESEARCH CENTER   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACARI; APIS MELLIFERA; HEXAPODA; VARROA;

EID: 84931271053     PISSN: 22145745     EISSN: 22145753     Source Type: Journal    
DOI: 10.1016/j.cois.2015.05.007     Document Type: Review

References (80)

1. A.D. Kay, A.J. Bruning, A. van Alst, T.T. Abrahamson, W.O. Hughes, and M. Kaspari A carbohydrate-rich diet increases social immunity in ants Proc Biol Sci 281 2014 20132374
2. S. Cremer, S.A. Armitage, and P. Schmid-Hempel Social immunity Curr Biol 17 2007 R693 R702
3. J.D. Evans, and M. Spivak Socialized medicine: individual and communal disease barriers in honey bees J Invertebr Pathol 103 Suppl. 1 2010 S62 S72
4. N.W. Calderone Insect pollinated crops, insect pollinators and US agriculture: trend analysis of aggregate data for the period 1992-2009 PLoS One 7 2012 e37235
5. E. Genersch, W. von der Ohe, H. Kaatz, A. Schroeder, C. Otten, R. Büchler, S. Berg, W. Ritter, W. Mülen, and S. Gisder The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies Apidologie 41 2010 332 352
6. R.M. Francis, S.L. Nielsen, and P. Kryger Varroa-virus interaction in collapsing honey bee colonies PLoS One 8 2013 e57540
7. C. Alaux, C. Dantec, H. Parrinello, and Y. Le Conte Nutrigenomics in honey bees: digital gene expression analysis of pollen's nutritive effects on healthy and varroa-parasitized bees BMC Genomics 12 2011 496
8. L.M. Brutscher, and D.K.M.L. Flenniken Antiviral defense mechanisms in honey bees Curr Opin Insect Sci 2015 (this issue)
9. J.R. de Miranda, G.L. Ribière, and M.Y.P. Chen Honey bee viruses and their effects on bee and colony health D. Sammataro, J.A. Yoder, Honey Bee Colony Health: Challenges and Sustainable Solution" 2011 CRC Press Taylor & Francis Group 71 102
10. Y.P. Chen, J.S. Pettis, M. Corona, W.P. Chen, C.J. Li, M. Spivak, P.K. Visscher, G. DeGrandi-Hoffman, H. Boncristiani, and Y. Zhao Israeli acute paralysis virus: epidemiology, pathogenesis and implications for honey bee health PLoS Pathog 10 2014 e1004261
11. J.R. de Miranda, G. Cordoni, and G. Budge The Acute bee paralysis virus-Kashmir bee virus-Israeli acute paralysis virus complex J Invertebr Pathol 103 Suppl. 1 2010 S30 S47
12. Y.P. Chen, and R. Siede Honey bee viruses Adv Virus Res 70 2007 33 80
13. S.J. Martin The role of Varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach J Appl Ecol 38 2001 1082 1093
14. G.C.R. DeGrandi-Hoffman A mathematical model of Varroa mite (Varroa destructor Anderson and Trueman) and honeybee (Apis mellifera L.) population dynamics Int J Acarol 30 2004 259 274
15. Doke M, Frazier M, Grozinger CM: Overwintering honey bees: biology and management. Curr Opin Insect Sci (this issue).
16. Y.P. Chen, P.J. Evans, J.D. Kramer, and M.M.F. Feldlaufer Transmission of Kashmir bee virus by the ectoparasitic mite Varroa destructor Apidologie 35 2004 441 448
17. Y.P. Chen, J.A. Higgins, and M.F. Feldlaufer Quantitative real-time reverse transcription-PCR analysis of deformed wing virus infection in the honeybee (Apis mellifera L.) Appl Environ Microbiol 71 2005 436 441
18. G. Di Prisco, F. Pennacchio, E. Caprio, H.F. Boncristiani Jr., J.D. Evans, and Y. Chen Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera J Gen Virol 92 2011 151 155
19. S.J. Martin, A.C. Highfield, L. Brettell, E.M. Villalobos, G.E. Budge, M. Powell, S. Nikaido, and D.C. Schroeder Global honey bee viral landscape altered by a parasitic mite Science 336 2012 1304 1306
20. B.J. Fischman, S.H. Woodard, and G.E. Robinson Molecular evolutionary analyses of insect societies Proc Natl Acad Sci USA 108 Suppl. 2 2011 10847 10854
21. E.V. Ryabov, G.R. Wood, J.M. Fannon, J.D. Moore, J.C. Bull, D. Chandler, A. Mead, N. Burroughs, and D.J. Evans A virulent strain of deformed wing virus (DWV) of honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission PLoS Pathog 10 2014 e100430
22. F. Nazzi, S.P. Brown, D. Annoscia, F. Del Piccolo, G. Di Prisco, P. Varricchio, G. Della Vedova, F. Cattonaro, E. Caprio, and F. Pennacchio Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies PLoS Pathog 8 2012 e1002735
23. K. Khongphinitbunjong, L.I. de Guzman, M.R. Tarver, T.E. Rinderer, Y. Chen, and P. Chantawannakul Differential viral levels and immune gene expression in three stocks of Apis mellifera induced by different numbers of Varroa destructor J Insect Physiol 72 2015 28 34
24. J. Li, W. Peng, J. Wu, J.P. Strange, H. Boncristiani, and Y. Chen Cross-species infection of deformed wing virus poses a new threat to pollinator conservation J Econ Entomol 104 2011 732 739
25. W.J. Peng, L.J. Boncristiani, H. Strange, J.P. Hamilton, and M.Y.P. Chen Host range expansion of honey bee black queen cell virus in the bumble bee, Bombus huntii Apidologie 42 2011 650 658
26. M.A. Furst, D.P. McMahon, J.L. Osborne, R.J. Paxton, and M.J. Brown Disease associations between honeybees and bumblebees as a threat to wild pollinators Nature 506 2014 364 366
27. M. Simone-Finstrom, F.B. Tarpy, and D.R.P.T. Starks Impact of food availability, pathogen exposure, and genetic diversity on thermoregulation in honey bees (Apis mellifera) J Ins behav 27 2014 527 539
28. M.D.S.M. Simone-Finstrom Propolis and bee health: the natural history and significance of resin use by honey bees Apidologie 41 2010 295 311
29. M. Simone, J.D. Evans, and M. Spivak Resin collection and social immunity in honey bees Evolution 63 2009 3016 3022
30. K. Bilikova, P.M. Trusheva, and B.V. Bankova New anti-Paenibacillus larvae substances purified from propolis Apidologie 44 2013 278 285
31. V. Bankova, M. Popova, S. Bogdanov, and A.G. Sabatini Chemical composition of European propolis: expected and unexpected results Z Naturforsch C 57 2002 530 533
32. M. Popova, M. Reyes, Y. Le Conte, and V. Bankova Propolis chemical composition and honeybee resistance against Varroa destructor Nat Prod Res 28 2014 788 794
33. W. Mao, M.A. Schuler, and M.R. Berenbaum Honey constituents up-regulate detoxification and immunity genes in the western honey bee Apis mellifera Proc Natl Acad Sci USA 110 2013 8842 8846
34. N. Damiani, N.J. Fernandez, L.M. Maldonado, A.R. Alvarez, M.J. Eguaras, and J.A. Marcangeli Bioactivity of propolis from different geographical origins on Varroa destructor (Acari: Varroidae) Parasitol Res 107 2010 31 37
35. N. Wilson-Rich, S.T. Dres, and P.T. Starks The ontogeny of immunity: development of innate immune strength in the honey bee (Apis mellifera) J Insect Physiol 54 2008 1392 1399
36. A.M. Laughton, M. Boots, and M.T. Siva-Jothy The ontogeny of immunity in the honey bee, Apis mellifera L. following an immune challenge J Insect Physiol 57 2011 1023 1032
37. K. Casteels-Josson, W. Zhang, T. Capaci, P. Casteels, and P. Tempst Acute transcriptional response of the honeybee peptide-antibiotics gene repertoire and required post-translational conversion of the precursor structures J Biol Chem 269 1994 28569 28575
38. J.D. Evans, K. Aronstein, Y.P. Chen, C. Hetru, J.L. Imler, H. Jiang, M. Kanost, G.J. Thompson, Z. Zou, and D. Hultmark Immune pathways and defence mechanisms in honey bees Apis mellifera Insect Mol Biol 15 2006 645 656
39. J.D. Evans Transcriptional immune responses by honey bee larvae during invasion by the bacterial pathogen, Paenibacillus larvae J Invertebr Pathol 85 2004 105 111
40. J. Vizioli, and M. Salzet Antimicrobial peptides from animals: focus on invertebrates Trends Pharmacol Sci 23 2002 494 496
41. L.M. Hedges, and K.N. Johnson Induction of host defence responses by Drosophila C virus J Gen Virol 89 2008 1497 1501
42. S. Govind Innate immunity in Drosophila: pathogens and pathways Insect Sci 15 2008 29 43
43. R.A. Zambon, M. Nandakumar, V.N. Vakharia, and L.P. Wu The Toll pathway is important for an antiviral response in Drosophila Proc Natl Acad Sci USA 102 2005 7257 7262
44. K. Azzami, W. Ritter, J. Tautz, and H. Beier Infection of honey bees with acute bee paralysis virus does not trigger humoral or cellular immune responses Arch Virol 157 2012 689 702
45. S.W. Ding RNA-based antiviral immunity Nat Rev Immunol 10 2010 632 644
46. M.L. Flenniken, K.M. Tassetto, and M.R. Andino Insect Virology - The Antiviral Role of RNA Interference 2010 Caister Academic Press. 367 388
47. S.W. Ding, and O. Voinnet Antiviral immunity directed by small RNAs Cell 130 2007 413 426
48. X.H. Wang, R. Aliyari, W.X. Li, H.W. Li, K. Kim, R. Carthew, P. Atkinson, and S.W. Ding RNA interference directs innate immunity against viruses in adult Drosophila Science 312 2006 452 454
49. R.A. Zambon, V.N. Vakharia, and L.P. Wu RNAi is an antiviral immune response against a dsRNA virus in Drosophila melanogaster Cell Microbiol 8 2006 880 889
50. Honeybee Genome Sequencing C Insights into social insects from the genome of the honeybee Apis mellifera Nature 443 2006 931 949
51. K. Aronstein, T. Pankew, and E. Saldivar SID-1 is implicated in systemic gene silencing in the honey bee J Api Res 45 2006 20 24
52. D.L. Cox-Foster, S. Conlan, E.C. Holmes, G. Palacios, J.D. Evans, N.A. Moran, P.L. Quan, T. Briese, M. Hornig, and D.M. Geiser A metagenomic survey of microbes in honey bee colony collapse disorder Science 318 2007 283 287
53. N. Chejanovsky, R. Ophir, M.S. Schwager, Y. Slabezki, S. Grossman, and D. Cox-Foster Characterization of viral siRNA populations in honey bee colony collapse disorder Virology 454-455 2014 176 183
54. E. Maori, N. Paldi, S. Shafir, H. Kalev, E. Tsur, E. Glick, and I. Sela IAPV, a bee-affecting virus associated with Colony Collapse Disorder can be silenced by dsRNA ingestion Insect Mol Biol 18 2009 55 60
55. W. Hunter, J. Ellis, D. Vanengelsdorp, J. Hayes, D. Westervelt, E. Glick, M. Williams, I. Sela, E. Maori, and J. Pettis Large-scale field application of RNAi technology reducing Israeli acute paralysis virus disease in honey bees (Apis mellifera, Hymenoptera: Apidae) PLoS Pathog 6 2010 e1001160
56. Y.P.E.J. Chen RNAi in treating honey bee diseases Bee Culture 140 2012 27 29
57. S.D. Desai, Y.J. Eu, S. Whyard, and R.W. Currie Reduction in deformed wing virus infection in larval and adult honey bees (Apis mellifera L.) by double-stranded RNA ingestion Insect Mol Biol 21 2012 446 455
58. M.L. Flenniken, and R. Andino Non-specific dsRNA-mediated antiviral response in the honey bee PLoS One 8 2013 e77263
59. D.A. Galbraith, X. Yang, E.L. Nino, S. Yi, and C. Grozinger Parallel epigenomic and transcriptomic responses to viral infection in honey bees (Apis mellifera) PLoS Pathog 11 2015 e1004713
60. G. Di Pasquale, M. Salignon, Y. Le Conte, L.P. Belzunces, A. Decourtye, A. Kretzschmar, S. Suchail, J.L. Brunet, and C. Alaux Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter? PLoS One 8 2013 e72016
61. A.D. Vaudo, T.J. Grozinger, and C.M.H.M. Patch Bee nutrition and floral resource restoration Curr Opin Insect Sci 2015 (this issue)
62. S.C. Cotter, S.S. Raubenheimer, and D.K. Wilson Macronutrient balance mediates trade-offs between immune function and life history traits Func Ecol 25 2011 186 198
63. T.G.D. França, I.L. Zorzella-Pezavento, S.F.G. Chiuso-Minicucci, F. daCunha, and M.L.R.S.A. Sartori Impact of malnutrition on immunity and infection J Venm Anim Toxins 15 2009 374 390
64. R.F. Grimble Nutritional modulation of immune function Proc Nutr Soc 60 2001 389 397
65. P. Schmid-Hempel Evolutionary ecology of insect immune defenses Annu Rev Entomol 50 2005 529 551
66. H.Y. Yi, M. Chowdhury, Y.D. Huang, and X.Q. Yu Insect antimicrobial peptides and their applications Appl Microbiol Biotechnol 98 2014 5807 5822
67. S. Erler, A. Denner, O. Bobis, E. Forsgren, and R.F. Moritz Diversity of honey stores and their impact on pathogenic bacteria of the honeybee, Apis mellifera Ecol Evol 4 2014 3960 3967
68. C. van Dooremalen, E. Stam, L. Gerritsen, B. Cornelissen, J. van der Steen, F. van Langevelde, and T. Blacquiere Interactive effect of reduced pollen availability and Varroa destructor infestation limits growth and protein content of young honey bees J Insect Physiol 59 2013 487 493
69. K.A. Aronstein, S.E. Vega, R. Westmiller, and S.A.E. Douglas How Varroa parasitism affects the immunological and nutritional staus of the honey bee, Apis mellifera Insects 3 2012 601 615
70. M.M. Wheeler, and G.E. Robinson Diet-dependent gene expression in honey bees: honey vs. sucrose or high fructose corn syrup Sci Rep 4 2014 5726
71. D.R. Schmehl, P.E. Teal, J.L. Frazier, and C.M. Grozinger Genomic analysis of the interaction between pesticide exposure and nutrition in honey bees (Apis mellifera) J Insect Physiol 71 2014 177 190
72. P.J. Turnbaugh, V.K. Ridaura, J.J. Faith, F.E. Rey, R. Knight, and J.I. Gordon The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice Sci Transl Med 1 2009 6ra14
73. M.A. Hildebrandt, C. Hoffmann, S.A. Sherrill-Mix, S.A. Keilbaugh, M. Hamady, Y.Y. Chen, R. Knight, R.S. Ahima, F. Bushman, and G.D. Wu High-fat diet determines the composition of the murine gut microbiome independently of obesity Gastroenterology 137 2009 1716-1724 e1711-1712
74. F. Ponton, K. Wilson, A.J. Holmes, S.C. Cotter, D. Raubenheimer, and S.J. Simpson Integrating nutrition and immunology: a new frontier J Insect Physiol 59 2013 130 137
75. F.J. Reynaldi, M.R. De Giusti, and A.M. Alippi Inhibition of the growth of Ascosphaera apis by Bacillus and Paenibacillus strains isolated from honey Rev Argent Microbiol 36 2004 52 55
76. J.D. Evans, and T.N. Armstrong Antagonistic interactions between honey bee bacterial symbionts and implications for disease BMC Ecol 6 2006 4
77. J.D.A.T. Evans Inhibition of the American foulbrood bacterium, Paenibacillus larvae, by bacteria isolated from honey bees J Api Res 44 2005 168 171
78. D.C. Sabate, L. Carrillo, and M.C. Audisio Inhibition of Paenibacillus larvae and Ascosphaera apis by Bacillus subtilis isolated from honeybee gut and honey samples Res Microbiol 160 2009 193 199
79. N.A. Moran Genomics of the honey bee microbiome Curr Opin Insect Sci 2015 (this issue)
80. A. Barron Death of the bee hive: understanding the failure of an insect society Curr Opin Insect Sci 2015 (this issue)