Effects of immunostimulation on social behavior, chemical communication and genome-wide gene expression in honey bee workers (Apis mellifera)

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Richard, Freddie Jeanne ^a,c   Holt, Holly L ^b   Grozinger, Christina M ^b,c  

^a UNIVERSITÉ DE POITIERS   (France)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Chemical ecology; Cuticular hydrocarbons; Genomics; Honey bees; Immunity; Nestmate recognition; Social behavior; Social immunity

Indexed keywords

HYDROCARBON; SEPHADEX; SODIUM CHLORIDE;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL COMMUNICATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; APIS MELLIFERA; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; ESCHERICHIA COLI; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; IMMUNE RESPONSE; IMMUNOSTIMULATION; INSECT GENOME; INSECT SOCIETY; NONHUMAN; NUCLEOTIDE SEQUENCE; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SOCIAL BEHAVIOR; SOCIAL INTERACTION; WORKER (INSECT);

ANIMALS; BEES; BEHAVIOR, ANIMAL; FEMALE; GENE EXPRESSION; GENES, INSECT; HYDROCARBONS; IMMUNITY; IMMUNIZATION; METABOLIC NETWORKS AND PATHWAYS; SOCIAL BEHAVIOR;

APIS MELLIFERA; APOIDEA; HEXAPODA; NEGIBACTERIA;

EID: 84867422557     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-558     Document Type: Article

References (76)

1. Vanengelsdorp D, Meixner MD. A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. J Invertebr Pathol 2010, 103(Suppl 1):S80-S95.
2. Winston ML. The Biology of the Honey Bee 1987, Cambridge: Harvard University Press.
3. Brown P. Cinderella goes to the ball. Nature 2001, 410(6832):1018-1020. 10.1038/35074279, 11323633.
4. Bonasio R, Zhang G, Ye C, Mutti NS, Fang X, Qin N, Donahue G, Yang P, Li Q, Li C, et al. Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 2010, 329(5995):1068-1071. 10.1126/science.1192428, 20798317.
5. Gerardo NM, Altincicek B, Anselme C, Atamian H, Barribeau SM, de Vos M, Duncan EJ, Evans JD, Gabaldon T, Ghanim M, et al. Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol 2010, 11(2):R21. 10.1186/gb-2010-11-2-r21, 2872881, 20178569.
6. Smith CD, Zimin A, Holt C, Abouheif E, Benton R, Cash E, Croset V, Currie CR, Elhaik E, Elsik CG, et al. Draft genome of the globally widespread and invasive Argentine ant (Linepithema humile). Proc Natl Acad Sci USA 2011, 108(14):5673-5678. 10.1073/pnas.1008617108, 3078359, 21282631.
7. Smith CR, Smith CD, Robertson HM, Helmkampf M, Zimin A, Yandell M, Holt C, Hu H, Abouheif E, Benton R, et al. Draft genome of the red harvester ant Pogonomyrmex barbatus. Proc Natl Acad Sci USA 2011, 108(14):5667-5672. 10.1073/pnas.1007901108, 3078412, 21282651.
8. Werren JH, Richards S, Desjardins CA, Niehuis O, Gadau J, Colbourne JK, Beukeboom LW, Desplan C, Elsik CG, Grimmelikhuijzen CJ, et al. Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 2010, 327(5963):343-348. 10.1126/science.1178028, 2849982, 20075255.
9. Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL, Jiang H, Kanost M, Thompson GJ, Zou Z, Hultmark D. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol 2006, 15(5):645-656. 10.1111/j.1365-2583.2006.00682.x, 1847501, 17069638.
10. Lemaitre B, Hoffmann J. The host defense of Drosophila melanogaster. Annu Rev Immunol 2007, 25:697-743. 10.1146/annurev.immunol.25.022106.141615, 17201680.
11. Wilson-Rich N, Spivak M, Fefferman NH, Starks PT. Genetic, individual, and group facilitation of disease resistance in insect societies. Annu Rev Entomol 2009, 54:405-423. 10.1146/annurev.ento.53.103106.093301, 18793100.
12. Chen YP, Siede R. Honey Bee Viruses. Advances in Virus Research 2007, 34-80. San Diego, California: Elsevier Academic Press, Maramorosh K, Shatkin AJ, Murphy FA.
13. Maori E, Lavi S, Mozes-Koch R, Gantman Y, Peretz Y, Edelbaum O, Tanne E, Sela I. Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honeybees in Israel: evidence for diversity due to intra- and inter-species recombination. J Gen Virol 2007, 88(Pt 12):3428-3438.
14. Runckel C, Flenniken ML, Engel JC, Ruby JG, Ganem D, Andino R, DeRisi JL. Temporal Analysis of the Honey Bee Microbiome Reveals Four Novel Viruses and Seasonal Prevalence of Known Viruses, Nosema, and Crithidia. PLoS One 2011, 6(6):e20656. 10.1371/journal.pone.0020656, 3110205, 21687739.
15. Aronstein KA, Murray KD. Chalkbrood disease in honey bees. J Invertebr Pathol 2010, 103(Suppl 1):S20-S29.
16. Forsgren E. European foulbrood in honey bees. J Invertebr Pathol 2010, 103(Suppl 1):S5-S9.
17. Genersch E. Paenibacillus larvae and American Foulbrood - long since known and still surprising. Journal fur Verbrauchershutz und Lebensmittelsicherheit 2008, 3:429-434.
18. Chen YP, Huang ZY. Nosema ceranae, a newly identified pathogen of Apis mellifera in the USA and Asia. Apidologie 2010, 41(3):364-374.
19. Sammataro D, Gerson U, Needham G. Parasitic mites of honey bees: life history, implications, and impact. Annu Rev Entomol 2000, 45:519-548. 10.1146/annurev.ento.45.1.519, 10761588.
20. Broderick NA, Welchman DP, Lemaitre B. Recognition and response to microbial infection in Drosophila. Insect Infection and Immunity: Evolution, Ecology and Mechanisms 2009, 13-33. Oxford: Oxford University Press, Rolff J, Reynolds S.
21. Rolff J, Reynolds SE. Introducing insect infection and immunity. Insect Infection and Immunity: Evolution, Ecology and Mechanisms 2009, 1-12. Oxford:Oxford University Press, Rolff J, Reynolds S.
22. Schmid-Hempel P. Evolutionary ecology of insect immune defenses. Annu Rev Entomol 2005, 50:529-551. 10.1146/annurev.ento.50.071803.130420, 15471530.
23. Ganesan S, Aggarwal K, Paquette N, Silverman N. NF-kappa B/Rel Proteins and the Humoral Immune Responses of Drosophila melanogaster. Nf-Kb in Health and Disease 2011, 349:25-60.
24. Martin P, Parkhurst SM. Parallels between tissue repair and embryo morphogenesis. Development 2004, 131:3021-3034. 10.1242/dev.01253, 15197160.
25. Dionne MS, Schneider DS. Models of infectious diseases in the fruit fly Drosophila melanogaster. Dis Model Mech 2008, 1(1):43-49. 10.1242/dmm.000307, 2561979, 19048052.
26. Cremer S, Armitage SA, Schmid-Hempel P. Social immunity. Curr Biol 2007, 17(16):R693-R702. 10.1016/j.cub.2007.06.008, 17714663.
27. Simone M, Evans JD, Spivak M. Resin collection and social immunity in honey bees. Evolution 2009, 63(11):3016-3022. 10.1111/j.1558-5646.2009.00772.x, 19619221.
28. Rueppell O, Hayworth MK, Ross NP. Altruistic self-removal of health-compromised honey bee workers from their hive. J Evol Biol 2010, 23(7):1538-1546. 10.1111/j.1420-9101.2010.02022.x, 20500363.
29. Hassanein MH. The Influence of Infection with Nosema-Apis on the Activities and Longevity of the Worker Honeybee. Ann Appl Biol 1953, 40(2):418-423.
30. Traniello JF, Rosengaus RB, Savoie K. The development of immunity in a social insect: evidence for the group facilitation of disease resistance. Proc Natl Acad Sci USA 2002, 99(10):6838-6842. 10.1073/pnas.102176599, 124490, 12011442.
31. Richard FJ, Aubert A, Grozinger CM. Modulation of social interactions by immune stimulation in honey bee, Apis mellifera, workers. BMC Biol 2008, 6:50. 10.1186/1741-7007-6-50, 2596086, 19014614.
32. Fan Y, Zurek L, Dykstra MJ, Schal C. Hydrocarbon synthesis by enzymatically dissociated oenocytes of the abdominal integument of the German Cockroach, Blattella germanica. Naturwissenschaften 2003, 90(3):121-126.
33. Howard RW, Blomquist GJ. Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 2005, 50:371-393. 10.1146/annurev.ento.50.071803.130359, 15355247.
34. Blomquist GJ, Bagneres AG. Insect hydrocarbons: biology, biochemistry and chemical ecology 2010, Cambridge: Cambridge University Press.
35. Fan YL, Richard FJ, Rouf N, Grozinger CM. Effects of queen mandibular pheromone on nestmate recognition in worker honeybees, Apis mellifera. Anim Behav 2010, 79(3):649-656.
36. Salvy M, Martin C, Bagneres AG, Provost E, Roux M, Le Conte Y, Clement JL. Modifications of the cuticular hydrocarbon profile of Apis mellifera worker bees in the presence of the ectoparasitic mite Varroa jacobsoni in brood cells. Parasitology 2001, 122(Pt 2):145-159.
37. Kulincevic JM, Stairs GR, Rothenbuhler WC. A disease of the honey bee causing behavioral changes and mortality. J Invertebr Pathol 1969, 14(1):13-17. 10.1016/0022-2011(69)90004-4, 5816958.
38. Alaux C, Dantec C, Parrinello H, Le Conte Y. Nutrigenomics in honey bees: digital gene expression analysis of pollen's nutritive effects on healthy and varroa-parasitized bees. BMC Genomics 2011, 12:496. 10.1186/1471-2164-12-496, 3209670, 21985689.
39. De Gregorio E, Spellman PT, Rubin GM, Lemaitre B. Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc Natl Acad Sci USA 2001, 98(22):12590-12595. 10.1073/pnas.221458698, 60098, 11606746.
40. Navajas M, Migeon A, Alaux C, Martin-Magniette M, Robinson G, Evans J, Cros-Arteil S, Crauser D, Le Conte Y. Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection. BMC Genomics 2008, 9:301. 10.1186/1471-2164-9-301, 2447852, 18578863.
41. Roxstrom-Lindquist K, Terenius O, Faye I. Parasite-specific immune response in adult Drosophila melanogaster: a genomic study. EMBO Rep 2004, 5(2):207-212. 10.1038/sj.embor.7400073, 1298984, 14749722.
42. Decanini LI, Collins AM, Evans JD. Variation and heritability in immune gene expression by diseased honeybees. J Hered 2007, 98(3):195-201. 10.1093/jhered/esm008, 17404328.
43. Evans JD. Transcriptional immune responses by honey bee larvae during invasion by the bacterial pathogen, Paenibacillus larvae. J Invertebr Pathol 2004, 85(2):105-111. 10.1016/j.jip.2004.02.004, 15050840.
44. Wittkopp PJ, Beldade P. Development and evolution of insect pigmentation: genetic mechanisms and the potential consequences of pleiotropy. Semin Cell Dev Biol 2009, 20(1):65-71. 10.1016/j.semcdb.2008.10.002, 18977308.
45. Munoz-Descalzo S, Terol J, Paricio N. Cabut, aC(2)H(2) zinc finger transcription factor, is required during Drosophila dorsal closure downstream of JNK signaling. Dev Biol 2005, 287(1):168-179. 10.1016/j.ydbio.2005.08.048, 16198331.
46. Kambris Z, Brun S, Jang IH, Nam HJ, Romeo Y, Takahashi K, Lee WJ, Ueda R, Lemaitre B. Drosophila immunity: a large-scale in vivo RNAi screen identifies five serine proteases required for Toll activation. Curr Biol 2006, 16(8):808-813. 10.1016/j.cub.2006.03.020, 16631589.
47. Blomquist GJ. Biosynthesis of cuticular hydrocarbons. Insect hydrocarbons: biology, biochemistry and chemical ecology 2010, 35-52. Cambridge: Cambridge University Press, Blomquist GJ, Bagneres AG.
48. Min KT, Benzer S. Preventing neurodegeneration in the Drosophila mutant bubblegum. Science 1999, 284(5422):1985-1988. 10.1126/science.284.5422.1985, 10373116.
49. Teixeira L, Rabouille C, Rorth P, Ephrussi A, Vanzo NF. Drosophila perilipin/ADRP homologue Lsd2 regulates lipid metabolism. Mech Dev 2003, 120(9):1071-1081. 10.1016/S0925-4773(03)00158-8, 14550535.
50. Beller M, Riedel D, Jansch L, Dieterich G, Wehland J, Jackle H, Kuhnlein RP. Characterization of the Drosophila lipid droplet subproteome. Mol Cell Proteomics 2006, 5(6):1082-1094. 10.1074/mcp.M600011-MCP200, 16543254.
51. Ayres JS, Schneider DS. The Role of Anorexia in Resistance and Tolerance to Infections in Drosophila. PLoS Biol 2009, 7(7):e1000150. 10.1371/journal.pbio.1000150, 2701602, 19597539.
52. Luque T, Hjelmqvist L, Marfany G, Danielsson O, El-Ahmad M, Persson B, Jornvall H, Gonzalez-Duarte R. Sorbitol dehydrogenase of Drosophila - Gene, protein, and expression data show a two-gene system. J Biol Chem 1998, 273(51):34293-34301. 10.1074/jbc.273.51.34293, 9852094.
53. Chen QF, Haddad GG. Role of trehalose phosphate synthase and trehalose during hypoxia: from flies to mammals. J Exp Biol 2004, 207(18):3125-3129. 10.1242/jeb.01133, 15299033.
54. Scherfer C, Tang H, Kambris Z, Lhocine N, Hashimoto C, Lemaitre B. Drosophila Serpin-28D regulates hemolymph phenoloxidase activity and adult pigmentation. Dev Biol 2008, 323(2):189-196. 10.1016/j.ydbio.2008.08.030, 18801354.
55. Dani FR, Jones GR, Corsi S, Beard R, Pradella D, Turillazzi S. Nestmate recognition cues in the honey bee: differential importance of cuticular alkanes and alkenes. Chem Senses 2005, 30(6):477-489. 10.1093/chemse/bji040, 15917370.
56. Hamilton C, Lejeune BT, Rosengaus RB. Trophallaxis and prophylaxis: social immunity in the carpenter ant Camponotus pennsylvanicus. Biol Lett 2011, 7(1):89-92. 10.1098/rsbl.2010.0466, 3030872, 20591850.
57. Aubert A, Richard FJ. Social management of LPS-induced inflammation in Formica polyctena ants. Brain Behav Immun 2008, 22(6):833-837. 10.1016/j.bbi.2008.01.010, 18331785.
58. Hughes WOH, Eilenberg J, Boomsma JJ. Trade-offs in group living: transmission and disease resistance in leaf-cutting ants. Proc R Soc Lond B 2002, 269:1811-1819.
59. Traniello JFA, Rosengaus RB, Savoie K. The development of immunity in a social evidence for the group facilitation of disease resistance. Proc Natl Acad Sci USA 2002, 99:6838-6842. 10.1073/pnas.102176599, 124490, 12011442.
60. Zecchini V, Brennan K, Martinez-Arias A. An activity of Notch regulates JNK signalling and affects dorsal closure in Drosophila. Curr Biol 1999, 9(9):460-469. 10.1016/S0960-9822(99)80211-5, 10322111.
61. Arrese EL, Soulages JL. Insect Fat Body: Energy, Metabolism, and Regulation. Annu Rev Entomol 2010, 55:207-225. 10.1146/annurev-ento-112408-085356, 3075550, 19725772.
62. Bischoff V, Vignal C, Duvic B, Boneca IG, Hoffmann JA, Royet J. Downregulation of the Drosophila immune response by peptidoglycan-recognition proteins SC1 and SC2. PLoS Pathog 2006, 2(2):e14. 10.1371/journal.ppat.0020014, 1383489, 16518472.
63. Schluns H, Crozier RH. Relish regulates expression of antimicrobial peptide genes in the honeybee, Apis mellifera, shown by RNA interference. Insect Mol Biol 2007, 16(6):753-759. 10.1111/j.1365-2583.2007.00768.x, 18093004.
64. Dade HA. Anatomy and Dissection of the Honeybee 1994, Cardiff: International Bee Research Association.
65. Gutierrez E, Wiggins D, Fielding B, Gould AP. Specialized hepatocyte-like cells regulate Drosophila lipid metabolism. Nature 2007, 445(7125):275-280. 10.1038/nature05382, 17136098.
66. Mashek DG, Li LO, Coleman RA. Long-chain acyl-CoA synthetases and fatty acid channeling. Future Lipidology 2007, 2(4):465-476. 10.2217/17460875.2.4.465, 2846691, 20354580.
67. Pei ZT, Oey NA, Zuidervaart MM, Jia ZZ, Li YY, Steinberg SJ, Smith KD, Watkins PA. The acyl-CoA synthetase "bubblegum" (lipidosin) - Further characterization and role in neuronal fatty acid beta-oxidation. J Biol Chem 2003, 278(47):47070-47078. 10.1074/jbc.M310075200, 12975357.
68. Grozinger CM, Sharabash NM, Whitfield CW, Robinson GE. Pheromone-mediated gene expression in the honey bee brain. Proc Natl Acad Sci USA 2003, 100(Suppl 2):14519-14525. 304112, 14573707.
69. Hoover SE, Keeling CI, Winston ML, Slessor KN. The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften 2003, 90(10):477-480. 10.1007/s00114-003-0462-z, 14564409.
70. Yang X, Cox-Foster DL. Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proc Natl Acad Sci USA 2005, 102(21):7470-7475. 10.1073/pnas.0501860102, 1140434, 15897457.
71. Richard FJ, Poulsen M, Drijfhout F, Jones G, Boomsma JJ. Specificity in chemical profiles of workers, brood and mutualistic fungi in Atta, Acromyrmex, and Sericomyrmex fungus-growing ants. J Chem Ecol 2007, 33(12):2281-2292. 10.1007/s10886-007-9385-z, 18040743.
72. Reyment RA. Compositional data analysis. Terra Nova 1989, 1(1):29-34.
73. Dennis G, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 2003, 4(5):P3. 10.1186/gb-2003-4-5-p3, 12734009.
74. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4(1):44-57.
75. VENNY An interactive tool for comparing lists with Venn Diagrams http://bioinfogp.cnb.csic.es/tools/venny/index.html, VENNY.
76. Fussnecker BL, McKenzie AM, Grozinger CM. cGMP modulates responses to queen mandibular pheromone in worker honey bees. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2011, 197(9):939-948. 10.1007/s00359-011-0654-5, 21626397.