The ontogeny of immunity in the honey bee, Apis mellifera L. following an immune challenge

Journal of Insect Physiology

Volumn 57, Issue 7, 2011, Pages 1023-1032

  Laughton, Alice M ^a,b   Boots, Michael ^a   Siva Jothy, Michael T ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b EMORY UNIVERSITY   (United States)

Author keywords

Honey bee; Immunity; Ontogeny; Phenoloxidase; Sex biased immunity; Temporal polyethism

Indexed keywords

ANTIMICROBIAL CATIONIC PEPTIDE; INSECT PROTEIN; LIPOPOLYSACCHARIDE; MONOPHENOL MONOOXYGENASE;

CASTE; DEVELOPMENTAL STAGE; ENZYME ACTIVITY; EUSOCIALITY; HEALTH RISK; HONEYBEE; IMMUNE RESPONSE; IMMUNITY; LIFE HISTORY; ONTOGENY; PARENTAL INVESTMENT; POLYETHISM; REPRODUCTIVE STRATEGY; SENESCENCE; SEX-RELATED DIFFERENCE;

AGING; ANIMAL; ARTICLE; BEE; ESCHERICHIA COLI; FEMALE; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INNATE IMMUNITY; INSECT; LARVA; MALE; METABOLISM; MICROBIOLOGY; UNITED KINGDOM;

AGING; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BEES; ENGLAND; ESCHERICHIA COLI; FEMALE; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; INSECT PROTEINS; LARVA; LIPOPOLYSACCHARIDES; MALE; MONOPHENOL MONOOXYGENASE; PUPA;

APIS MELLIFERA; APOIDEA;

EID: 79959909039     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2011.04.020     Document Type: Article

References (76)

1. Adamo S.A., Jensen M., Younger M. Changes in lifetime immunocompetence in male and female Gryllus texensis (formerly G. integer)*: trade-offs between immunity and reproduction. Animal Behaviour 2001, 62:417-425.
2. Allen M., Ball B. The incidence and world distribution of honey bee viruses. Bee World 1996, 77:141-162.
3. Amdam G.V., Aase A.L.T.O., Seehuus S., Fondrk M.K., Norberg K., Hartfelder K. Social reversal of immunosenescence in honey bee workers. Experimental Gerontology 2005, 40:939-947.
4. Amdam G.V., Hartfelder K., Norberg K., Hagen A., Omholt S.W. Altered physiology in worker honey bees (Hymenoptera: Apidae) infested with the mite Varroa destructor (Acari: Varroidae): a factor in colony loss during overwintering?. Journal of Economic Entomology 2004, 97:741-747.
5. Baer B., Schmid-Hempel P. Phenotypic variation in male and worker encapsulation response in the bumblebee Bombus terrestris. Ecological Entomology 2006, 31:591-596.
6. Baer B., Krug A., Boomsma J.J., Hughes W.O.H. Examination of the immune responses of males and workers of the leaf-cutting ant Acromyrmex echinatior and the effect of infection. Insectes Sociaux 2005, 52:298-303.
7. Bailey L. Honey bee pathology. Annual Review of Entomology 1968, 13:191-212.
8. Bailey L., Ball B.V. Honey Bee Pathology 1991, Academic Press Limited, London.
9. Barnes A.I., Siva-Jothy M.T. Density-dependent prophylaxis in the mealworm beetle Tenebrio molitor L. (Coleoptera: Tenebrionidae): cuticular melanization is an indicator of investment in immunity. Proceedings of the Royal Society of London, Series B 2000, 267:177-182.
10. Bedick J.C., Tunaz H., Nor Aliza A.R., Putnam S.M., Ellis M.D., Stanley D.W. Eicosanoids act in nodulation reactions to bacterial infections in newly emerged adult honey bees Apis mellifera, but not in older foragers. Comparative Biochemistry and Physiology Part C 2001, 130:107-117.
11. Bocher A., Tirard C., Doums C. Phenotypic plasticity of immune defence linked with foraging activity in the ant Cataglyphis velox. Journal of Evolutionary Biology 2007, 20:2228-2234.
12. Boman H.G., Hultmark D. Cell-free immunity in insects. Annual Review of Microbiology 1987, 41:103-126.
13. Boomsma J.J., Schmid-Hempel P., Hughes W.O.H. Life histories and parasite pressure across the major groups of social insects. Insect Evolutionary Ecology 2005, 139-175. CABI Publishing, Oxford. M.D.E. Fellowes, G.J. Holloway, J. Rolff (Eds.).
14. Boulanger N., Brun R., Ehret-Sabatier L., Kunz C., Bulet P. Immunopeptides in the defense reactions of Glossina morsitans to bacterial and Trypanosoma brucei brucei infections. Insect Biochemistry and Molecular Biology 2002, 32:369-375.
15. Boulanger N., Ehret-Sabatier L., Brun R., Zachary D., Bulet P., Imler J. Immune response of Drosophila melanogaster to infection with the flagellate parasite Crithidia spp. Insect Biochemistry and Molecular Biology 2001, 31:129-137.
16. Cerenius L., Lee B.L., Söderhäll K. The proPO-system: pros and cons for its role in invertebrate immunity. Trends in Immunology 2008, 29:263-271.
17. Chan Q.W.T., Melathopoulos A.P., Pernal S.F., Foster L.J. The innate immune and systemic response in honey bees to a bacterial pathogen, Paenibacillus larvae. BMC Genomics 2009, 10:387.
18. Chan Q.W.T., Howes C.G., Foster L.J. Quantitative comparison of caste differences in honeybee hemolymph. Molecular and Cellular Proteomics 2006, 5:2252-2262.
19. Chmurzynska W., Wojtczak L. Effect of thiourea on moulting and pupation of the silkworm Bombyx mori L. Biological Bulletin 1963, 125:61-68.
20. Chung K.T., Ourth D.D. Viresin. A novel antibacterial protein from immune hemolymph of Heliothis virescens pupae. European Journal of Biochemistry 2000, 267:677-683.
21. Cremer S., Armitage S.A., Schmid-Hempel O.P. Social immunity. Current Biology 2007, 17:R693-R702.
22. DeVeale B., Brummel T., Seroude L. Immunity and aging: the enemy within?. Aging Cell 2004, 3:195-208.
23. Doums C., Moret Y., Benelli E., Schmid-Hempel P. Senescence of immune defence in Bombus workers. Ecological Entomology 2002, 27:138-144.
24. Doums C., Schmid-Hempel P. Immunocompetence in workers of a social insect Bombus terrestris L., in relation to foraging activity and parasitic infection. Canadian Journal of Zoology 2000, 78:1060-1066.
25. Dubovskiy I.M., Krukova N.A., Glupov V.V. Phagocytic activity and encapsulation rate of Galleria mellonella larval haemocytes during bacterial infection by Bacillus thuringiensis. Journal of Invertebrate Pathology 2008, 98:360-362.
26. Eleftherianos I., Baldwin H., ffrench-Constant R.H., Reynolds S.E. Developmental modulation of immunity: changes within the feeding period of the fifth larval stage in the defence reactions of Manduca sexta to infection by Photorhabdus. Journal of Insect Physiology 2008, 54:309-318.
27. Evans J.D. Transcriptional immune responses by honey bee larvae during invasion by the bacterial pathogen, Paenibacillus larvae. Journal of Invertebrate Pathology 2004, 85:105-111.
28. Evans J.D., Lopez D.L. Bacterial probiotics induce an immune response in the honey bee (Hymenoptera: Apidae). Journal of Economical Entomology 2004, 97:752-756.
29. Evans J.D., Spivak M. Socialized medicine: individual and communal disease barriers in honey bees. Journal of Invertebrate Pathology 2009, 103:S62-S72.
30. Falchuk K.H. The molecular basis for the role of zinc in developmental biology. Molecular and Cellular Biochemistry 1998, 188:41-48.
31. Freitak D., Wheat C., Heckel C., Vogel H. Immune system responses and fitness costs associated with consumption of bacteria in larvae of Trichoplusia ni. BMC Biology 2007, 5:56.
32. Gerloff C.U., Ottmer B.K., Schmid-Hempel P. Effects of inbreeding on immune response and body size in a social insect, Bombus terrestris. Functional Ecology 2003, 17:582-589.
33. Gillespie J.P., Kanost M.R., Trenczek T. Biological mediators of insect immunity. Annual Review Entomology 1997, 42:611-643.
34. Haine E.R., Pollitt L.C., Moret Y., Siva-Jothy M., Rolff T.J. Temporal patterns in immune responses to a range of microbial insults (Tenebrio molitor). Journal of Insect Physiology 2008, 54:1090-1097.
35. Hillyer J.F., Schmidt S.L., Fuchs J.F., Boyle J.P., Christensen B.M. Age-associated mortality in immune challenged mosquitoes (Aedes aegypti) correlates with a decrease in haemocyte numbers. Cellular Microbiology 2005, 7:39-51.
36. Hooper T. Guide to Bees and Honey 1997, Marston House, Yeovil.
37. Hopkins T.L., Kramer K.J. Insect cuticle sclerotization. Annual Reviews in Entomology 1992, 37:273-302.
38. Horowitz N.H., Shen S. Neurospora tyrosinase. Journal of Biological Chemistry 1952, 197:513-520.
39. Hultmark D. Insect lysozymes. Lysozymes: Model Enzymes in Biochemistry and Biology 1996, 87-102. Birkhäuser Verlag, Basel, Switzerland. P. Jollès (Ed.).
40. Kaaya G.P., Darji N. The humoral defense system in tsetse: differences in response due to age, sex and antigen types. Developmental & Comparative Immunology 1988, 12:255-268.
41. König C., Schmid-Hempel P. Foraging activity and immunocompetence in workers of the bumble bee, Bombus terrestris L. Proceedings of the Royal Society of London, Series B 1995, 260:225-227.
42. Kopacek P., Weise C., Gotz P. The prophenoloxidase from the wax moth Galleria mellonella: purification and characterization of the proenzyme. Insect Biochemistry and Molecular Biology 1995, 25:1081-1091.
43. Laughton A.M., Siva-Jothy M.T. A standardised protocol for measuring phenoloxidase and prophenoloxidase in the honey bee Apis mellifera. Apidologie 2010, 10.1051/apido/2010046.
44. Lavine M.D., Strand M.R. Insect hemocytes and their role in immunity. Insect Biochemistry and Molecular Biology 2002, 32:1295-1309.
45. Lehrer R.I., Ganz T. Antimicrobial peptides in mammalian and insect host defence. Current Opinion in Immunology 1999, 11:23-27.
46. Lourenço A.P., Zufelato M.S., Bitondi M.M.G., Simöes Z.L.P. Molecular characterization of a cDNA encoding prophenoloxidase and its expression in Apis mellifera. Insect Biochemistry and Molecular Biology 2005, 35:541-552.
47. Mason H.S. Comparative biochemistry of the phenolase complex. Advances in Enzymology 1955, 16:105-184.
48. Meylaers K., Freitak D., Schoofs L. Immunocompetence of Galleria. mellonella: sex- and stage-specific differences and the physiological cost of mounting an immune response during metamorphosis. Journal of Insect Physiology 2007, 53:146-156.
49. Michelette E.R., Soares A.E.E. Characterization of preimaginal development stages in Africanized honeybee workers (Apis mellifera L.). Apidologie 1993, 24:431-440.
50. Moret Y., Schmid-Hempel P. Immune responses of bumblebee workers as a function of individual and colony age: senescence versus plastic adjustment of the immune function. Oikos 2009, 118:371-378.
51. Moret Y., Schmid-Hempel P. Survival for immunity: the price of immune system activation for bumblebee workers. Science 2000, 290:1166-1168.
52. Natori S., Shiraishi H., Hori S., Kobayashi A. The roles of Sarcophaga defense molecules in immunity and metamorphosis. Developmental and Comparative Immunology 1999, 23:317-328.
53. Navajas M., Migeon A., Alaux C., Martin-Magniette M.L., Robinson G.E., Evans J.D., 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.
54. Oldroyd B.P. What's killing American honey bees?. PLoS Biology 2007, 5:e168.
55. Omholt S.W., Amdam G.V. Epigenetic regulation of aging in honeybee workers. Science of Aging Knowledge Environment 2004, 2004:28.
56. Page R.E., Peng C.Y.S. Aging and development in social insects with emphasis on the honey bee, Apis mellifera L. Experimental Gerontology 2001, 36:695-711.
57. Ratcliffe N.A., Leonard C., Rowley A.F. Prophenoloxidase activation: nonself recognition and cell cooperation in insect immunity. Science 1984, 226:55-559.
58. Robinson G.E. Regulation of division of labor in insect societies. Annual Review Entomology 1992, 37:637-665.
59. Robinson G.E. Regulation of honey bee age polyethism by juvenile hormone. Behavioural Ecology and Sociobiology 1987, 20:329-338.
60. Rolff J. Bateman's principle and immunity. Proceedings of the Royal Society of London, Series B 2002, 269:867-872.
61. Rueppell O., Fondrk M.K., Page R.E. Biodemographic analysis of male honey bee mortality. Aging Cell 2004, 4:13-19.
62. Ruiz-González M.X., Brown M.J.F. Males vs workers: testing the assumptions of the haploid susceptibility hypothesis in bumblebees. Behavioural Ecology and Sociobiology 2006, 60:501-509.
63. Saul S.J., Sugumaran M. Prophenoloxidase activation in the hemolymph of Sarcophaga bullata larvae. Archives of Insect Biochemistry and Physiology 1988, 7:91-103.
64. Schmid M.R., Brockmann A., Pirk C.W.W., Stanley D.W., Tautz J. Adult honeybees (Apis mellifera L.) abandon hemocytic but not phenoloxidase-based immunity. Journal of Insect Physiology 2008, 54:439-444.
65. Schmid-Hempel P. Evolutionary ecology of insect immune defenses. Annual Review of Entomology 2005, 50:529-551.
66. Schmid-Hempel P. Parasites in Social Insects 1998, Princeton University Press, Chichester, West Sussex.
67. Simmons L.W., Roberts B. Bacterial immunity traded for sperm viability in male crickets. Science 2005, 309:2031.
68. Siva-Jothy M.T., Moret Y., Rolff J. Insect immunity: an evolutionary ecology perspective. Advances in Insect Physiology 2005, 32:1-48.
69. Thompson J.J.W. Aspects of Melanin Production and Immunity in the Mealworm Beetle Tenebrio molitor 2002, MPhil., Department of Animal and Plant Sciences, University of Sheffield.
70. Tzou P., Ohresser S., Ferrandon D., Capovilla M., Reichhart J., Lemaitre B., Hoffman J., Imler J. Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia. Immunity 2000, 13:737-748.
71. Vainio L., Hakkarainen H., Rantala M.J., Sorvari J. Individual variation in immune function in the ant Formica exsecta; effects of the nest, body size and sex. Evolutionary Ecology 2004, 18:75-84.
72. Wilson E.O. The Insect Societies 1971, Oxford University Press, London.
73. Wilson-Rich N., Dres S.T., Starks P.T. The ontogeny of immunity: development of innate immune strength in the honey bee (Apis mellifera). Journal of Insect Physiology 2008, 54:1392-1399.
74. Zerofsky M., Harel E., Silverman N., Tatar M. Aging of the innate immune response in Drosophila melanogaster. Aging Cell 2005, 4:103-108.
75. Zufelato M.S., Lourenço A.P., Simoes Z.L.P., Jorge J.A., Bitondi M.M.G. Phenoloxidase activity in Apis mellifera honey bee pupae, and ecdysteroid-dependent expression of the prophenoloxidase mRNA. Insect Biochemistry and Molecular Biology 2004, 34:1257-1268.
76. Zuk M. The sicker sex. PLoS Pathogens 2009, 5:e1000267.