Immune responses of bumblebee workers as a function of individual and colony age: Senescence versus plastic adjustment of the immune function

Oikos

Volumn 118, Issue 3, 2009, Pages 371-378

  Moret, Yannick ^a,b   Schmid Hempel, Paul ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITÉ DE BOURGOGNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AGE-RELATED DIFFERENCE; BEE; ENZYME ACTIVITY; FITNESS; IMMUNE RESPONSE; LIFE HISTORY TRAIT; PARASITISM; PHYSIOLOGICAL RESPONSE; REPRODUCTIVE POTENTIAL; REPRODUCTIVE SUCCESS; SENESCENCE; SURVIVAL; WORKER CASTE;

BOMBUS TERRESTRIS; HEXAPODA;

EID: 61849168846     PISSN: 00301299     EISSN: 16000706     Source Type: Journal    
DOI: 10.1111/j.1600-0706.2008.17187.x     Document Type: Article

References (56)

1. Adamo, S. O. et al. 2001. Changes in lifetime immunocompetence in male and female Gryllus texensis (formerly G. integer): tradeoffs between immunity and reproduction Anim. Behav. 62 : 417 425.
2. Amdam, G. V. et al. 2005. Social reversal of immunosenescence in honey bee workers Exp. Gerontol. 40 : 939 947.
3. Aspinall, R. et al. 2003. My T's gone cold, I'm wondering why Nat. Immunol. 4 : 203 205.
4. Barnes, A. I. Siva-Jothy, M. T. 2000. Density-dependent prophylaxis in the mealworm beetle Tenebrio molitor L. (Coleoptera: Tenebrionidae): cuticular melanization is an indicator of investment in immunity Proc. R. Soc. Lond. B 267 : 177 182.
5. Behrends, A. et al. 2007. Cognitive aging is linked to social role in honey bees (Apis mellifera) Exp. Gerontol. 42 : 1146 1153.
6. Bourke, A. F. G. Franks, N. R. 1995. Social evolution in ants. Princeton Univ. Press.
7. David, J et al. 1975. Physiologie de l'inanition et utilisation des réserves chez les adultes de Drosophila melanogaster Arch. Zool. Exp. Gen. 116 : 579 590.
8. Doums, C Schmid-Hempel, P. 2000. Immunocompetence in workers of a social insect, Bombus terrestris L., in relation to foraging activity and parasitic infection Can. J. Zool. 8 : 1060 1066.
9. Doums, C. et al. 2002. Senescence of immune defence in Bombus workers Ecol. Entomol. 27 : 138 144.
10. Ellers, J. 1996. Fat and eggs: an alternative methodto measure the tradeoff between survival and reproduction in insect parasitoids Neth. J. Zool. 46 : 227 235.
11. Finch, C. E. 1990. Longevity, senescence and the genome. Chicago Univ. Press.
12. Franceschi, C. et al. 2000. Human immunoscenescence: the prevailing of innate immunity, the failing of clonotypic immunity, and the filling of immunological space Vaccine 18 : 1717 1720.
13. Gillespie, J. et al. 1997. Biological mediators of insect immunity Annu. Rev. Entomol. 42 : 611 643.
14. Goulson, D. 2003. Bumblebees - their behaviour and ecology. Oxford Univ. Press.
15. Haussmann, M. F. et al. 2005. Cell-mediated immunosenescence in birds Oecologia 145 : 270 275.
16. Hoffmann, J. A. et al. 1996. Innate immunity in higher insects Curr. Opin. Immunol. 8 : 8 13.
17. Hultmark, D. 1993. Immune reactions in Drosophila and other insects: a model for innate immunity Trends Genet. 9 : 178 183.
18. Johansson, M. W. Söderhäll, K. 1985. Exocytosis of the prophenoloxidase activating system from crayfish haemocytes J. Comp. Physiol. B 1556 : 175 181.
19. Kirkwood, T. B. L. Rose, M. R. 1991. Evolution of senescence - late survival sacrificed for reproduction Philos. Trans. R. Soc. B 332 : 15 24.
20. König, C. Schmid-Hempel, P. 1995. Foraging activity and immunocompetence in workers of the bumble bee, Bombus terrestris L Proc. R. Soc. Lond. B 260 : 225 227.
21. Korner, P. Schmid-Hempel, P. 2004. In vivo dynamics of an immune response in the bumble bee Bombus terrestris J. Invert. Pathol. 87 : 59 66.
22. Lavoie, E. T. et al. 2007. Immunosenescence and age-related susceptibility to influenza virus in Japanese quail Dev. Comp. Immunol. 31 : 407 414.
23. Malaguarnera, L. et al. 2001. Immunosenescence: a review Arch. Gerontol. Geriat. 32 : 1 14.
24. Moret, Y. 2003. Explaining variable costs of the immune response: selection for specific versus non-specific immunity and facultative life history change Oikos 102 : 213 216.
25. Moret, Y. Schmid-Hempel, P. 2001. Immune defence in bumble-bee offspring Nature 414 : 506.
26. Moret, Y. Siva-Jothy, M. T. 2003. Adaptive innate immunity? Responsive-mode prophylaxis in the mealworm beetle, Tenebrio molitor Proc. R. Soc. Lond. B 270 : 2475 2480.
27. Moret, Y. Schmid-Hempel, P. 2004. Social life-history response to individual immune challenge of workers of Bombus terrestris L.: a possible new cooperative phenomenon Ecol. Lett. 7 : 146 152.
28. Nappi, A. J. Ottaviani, E. 2000. Cytotoxicity and cytotoxic molecules in invertebrates BioEssays 22 : 469 480.
29. Quinn, G. P. Keough, M. J. 2002. Experimental design and data analysis for biologists. Cambridge Univ. Press.
30. Rees, J. A. et al. 1996. Novel antibacterial peptides isolated from a European bumblebee, Bombus pascusrum (Hymenoptera, Apoidea) Insect Biochem. Mol. Biol. 27 : 413 422.
31. Rolff, J. 2001. Effects of age and gender on immune function of dragonflies (Odonata, Lestidae) from a wild population Can. J. Zool. 79 : 2176 2180.
32. Rose, M. R. 1991. Evolutionary biology of ageing. Oxford Univ. Press.
33. Rutrecht, S. T. Brown, M. J. F. 2008. The life history impact and implications of multiple parasites for bumble bee queens Int. J. Parasitol. 38 : 799 808.
34. Råberg, L. et al. 2002. Basal metabolic rate and the evolution of the adaptive immune system Proc. R. Soc. Lond. B 269 : 817 821.
35. Sadd, B. M. Siva-Jothy, M. T. 2006. Self-harm caused by an insect's innate immunity Proc. R. Soc. Lond. B 273 : 2571 2574.
36. Sadd, B. M. Schmid-Hempel, P. 2006. Insect immunity shows specificity in protection upon secondary pathogen exposure Curr. Biol. 16 : 1206 1210.
37. Saad, B. M. et al. 2005. Trans-generational immune priming in a social insect Biol. Lett. 1 : 386 388.
38. Schmid-Hempel, P. 1998. Parasites in social insects, monograph in behavior and ecology. Princeton Univ. Press.
39. Schmid-Hempel, R. Schmid-Hempel, P. 1998. Colony performance and immunocompetence of a social insect, Bombus terrestris, in a poor and variable environments Ecol. 12 : 22 30.
40. Schmid-Hempel, P. Schmid-Hempel, R. 2000. Female mating frequency in Bombus spp. from central Europe Insect. Soc. 47 : 36 41.
41. Seeley, T. D. 1985. Honeybee ecology. Princeton Univ. Press.
42. Shykoff, J. A. Schmid-Hempel, P. 1991. Incidence and effects of four parasites in natural populations in bumble bees in Switzerland Apidologie 22 : 117 126.
43. Sheldon, B.C. Verhulst, S. 1996. Ecological immunology: costly parasite defences and tradeoffs in evolutionary ecology Trends Ecol. Evol. 11 : 317 321.
44. Siva-Jothy, M. T. et al. 2005. Insect immunity: an evolutionary ecology perspective Adv. Insect Physiol. 32 : 1 48.
45. Söderhäll, K. Cerenius, L. 1998. Role of the prophenoloxidase-activating system in invertebrate immunity Curr. Opin. Immunol. 10 : 23 28.
46. Stearns, S.C. 1992. Life history evolution. Oxford Univ. Press.
47. Steinhaus, E. A. 1958. Crowding as a possible stress factor in insect disease Ecology 39 : 503 514.
48. Stoehr, A. M. 2007. Inter-and intra-sexual variation in immune defence in the cabbage white butterfly, Pieris rapae L. (Lepidoptera: Pieridae) Ecol. Entomol. 32 : 188 193.
49. Sugumaran, M. et al. 2000. A new mechanism for the control of phenoloxidase activity: inhibition and complex formation with quinone isomerase Arch. Biochem. Biophys. 379 : 252 260.
50. Wille, H. Rutz, W. 1975. Beziehungen zwischen Juvenilhormontiter und Hamozyten erwachsener Sommerbienen (Apis mellifera L.) Schweiz Landwirtschaft. Forsch. 14 : 339 353.
51. Williams, G. C. 1957. Pleiotropy, natural selection, and the evolution of senescence Evolution 11 : 398 411.
52. Wilson, K. 2002. Coping with crowds: density-dependent disease resistance in desert locusts Proc. Natl Acad. Sci. USA 99 : 5471 5475.
53. Wilson, K. Reeson, A. F. 1998. Density-dependent prophylaxis: evidence from Lepidoptera-baculovirus interactions? Ecol. Entomol. 23 : 100 101.
54. Wilson, K. et al. 2001. Melanism and disease resistance in insects Ecol. Lett. 4 : 637 649.
55. Wilson, K. et al. 2003. Group living and investment in immune defence: an interspecific analysis J. Anim. Ecol. 72 : 133 143.
56. Zachary, D. Hoffmann, D. 1984. Lysozyme is stored in the granule of certain haemocyte types in Locusta J. Insect Physiol. 30 : 405 411.