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Apidologie

, Volume 50, Issue 4, pp 463–471 | Cite as

Different activation of immune-related genes in honey bee nurses and foragers (Apis mellifera)

  • Eva Marit Hystad ByhrøEmail author
  • Heli Salmela
  • Ana Vitlic
  • Ying Wang
  • Daniel Münch
  • Gro V. Amdam
Original article
  • 74 Downloads

Abstract

Honey bee workers show very flexible aging patterns. Their typical behavioral progression, from nurse bees to forager bees, is associated with an onset of aging symptoms. Here, we studied how immune-activation can affect nurse and forager bees differently. Nurse and forager bees of identical chronological age were injected with vehicle control or the bacterial cell wall components lipopolysaccharide (LPS) or peptidoglycan (PGN). Next, we monitored survival and tested the expression of three immune-related genes. We confirm that forager bees die sooner than same-aged nurse bees, independent of the type of immune challenge. The relative gene expression patterns of two immune-related genes differed between the nurse and forager honey bees as well as between the treatment groups. Our findings support that nurse and forager honey bees can respond differently to immune challenge, despite a lack of detectable differences in mortality between treatments. This response was specifically associated with the workers’ behavioral caste, as the chronological age was similar among all tested animals.

Keywords

honeybee aging immune activation vitellogenin defensin-2 

Notes

Acknowledgments

We thank Nick Baker for managing the colonies. We thank Claus Kreibich for valuable input. We thank Jane Ludvigsen for reading and commenting on the text.

Author contributions

EMHB, HS, GVA: designed the study, analyzed the data; EMHB, HS, AV, YW: performed research; EMHB, DM, GVA drafted the paper. All authors provided text, read, and approved the final manuscript.

Compliance with ethical standards

Conflict of interests

The authors declare that they have no potential conflict of interest in relation to the study in this paper.

Supplementary material

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References

  1. Alaux, C., N. Kemper, A. Kretzschmar and Y. Le Conte (2012). Brain, physiological and behavioral modulation induced by immune stimulation in honeybees (Apis mellifera): A potential mediator of social immunity? Brain Behavior and Immunity 26(7): 1057–1060.CrossRefGoogle Scholar
  2. Amdam, G. V., A. Aase, S. C. Seehuus, M. K. Fondrk, K. Norberg and K. Hartfelder (2005). Social reversal of immunosenescence in honey bee workers. Experimental Gerontology 40(12): 939–947.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Behrends, A., R. Scheiner, N. Baker and G. V. Amdam (2007). Cognitive aging is linked to social role in honey bees (Apis mellifera). Experimental Gerontology 42(12): 1146–1153.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bordier, C., S. Suchail, M. Pioz, J. M. Devaud, C. Collet, M. Charreton, Y. Le Conte and C. Alaux (2017). Stress response in honeybees is associated with changes in task-related physiology and energetic metabolism. J Insect Physiol 98: 47–54.CrossRefPubMedGoogle Scholar
  5. Evans, J. D., K. Aronstein, Y. P. Chen, C. Hetru, J. L. Imler, H. Jiang, M. Kanost, G. J. Thompson, Z. Zou and D. Hultmark (2006). Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Molecular Biology 15(5): 645–656.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Fluri, P., H. Wille, L. Gerig and M. Lüscher (1977). Juvenile hormone, vitellogenin and haemocyte composition in winter worker honeybees (Apis mellifera). Experientia 33(9): 1240–1241.CrossRefGoogle Scholar
  7. Guzmán-Novoa, E., R. E. Page and N. E. Gary (1994). Behavioral and life-history components of division of labor in honey bees (Apis mellifera L.). Behavioral Ecology and Sociobiology 34(6): 117–409.CrossRefGoogle Scholar
  8. Hillyer, J. F. (2016). Insect immunology and hematopoiesis. Dev Comp Immunol 58: 102–118.CrossRefPubMedGoogle Scholar
  9. Huang, Z. Y. and G. E. Robinson (1992). Honeybee colony integration: worker-worker interactions mediate hormonally regulated plasticity in division of labor. Proc Natl Acad Sci U S A 89(24): 11726–11729.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Ihle, K. E., O. Rueppell, Z. Y. Huang, Y. Wang, M. K. Fondrk, R. E. Page, Jr. and G. V. Amdam (2015). Genetic architecture of a hormonal response to gene knockdown in honey bees. J Hered 106(2): 155–165.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Kazlauskas, N., M. Klappenbach, A. M. Depino and F. F. Locatelli (2016). Sickness Behavior in Honey Bees. Frontiers in Physiology 7: 10.CrossRefGoogle Scholar
  12. Kohler, A., C. W. W. Pirk and S. W. Nicolson (2012). Simultaneous stressors: Interactive effects of an immune challenge and dietary toxin can be detrimental to honeybees. Journal of Insect Physiology 58(7): 918–923.CrossRefPubMedGoogle Scholar
  13. Laughton, A. M., M. Boots and M. T. Siva-Jothy (2011). The ontogeny of immunity in the honey bee, Apis mellifera L. following an immune challenge. Journal of Insect Physiology 57(7): 1023–1032.CrossRefPubMedGoogle Scholar
  14. Li, W., Y. Chen and S. C. Cook (2018). Chronic Nosema ceranae infection inflicts comprehensive and persistent immunosuppression and accelerated lipid loss in host Apis mellifera honey bees. Int J Parasitol 48(6): 433–444.CrossRefPubMedGoogle Scholar
  15. Lourenco, A. P., K. R. Guidugli-Lazzarini, F. C. P. Freitas, M. M. G. Bitondi and Z. L. P. Simoes (2013). Bacterial infection activates the immune system response and dysregulates microRNA expression in honey bees. Insect Biochemistry and Molecular Biology 43(5): 474–482.CrossRefPubMedGoogle Scholar
  16. Lourenco, A. P., A. Mackert, A. D. Cristino and Z. L. P. Simoes (2008). Validation of reference genes for gene expression studies in the honey bee, Apis mellifera, by quantitative real-time RT-PCR. Apidologie 39(3): 372-U333.CrossRefGoogle Scholar
  17. Lourenco, A. P., J. R. Martins, F. A. S. Torres, A. Mackert, L. R. Aguiar, K. Hartfelder, M. M. G. Bitondi and Z. L. P. Simoes (2019). Immunosenescence in honey bees (Apis mellifera L.) is caused by intrinsic senescence and behavioral physiology. Exp Gerontol 119: 174–183.CrossRefPubMedGoogle Scholar
  18. Munch, D., N. Baker, E. M. K. Rasmussen, A. K. Shah, C. D. Kreibich, L. E. Heidem and G. V. Amdam (2013). Obtaining Specimens with Slowed, Accelerated and Reversed Aging in the Honey Bee Model. Jove-Journal of Visualized Experiments(78).Google Scholar
  19. Münch, D. and G. V. Amdam (2013). Brain Aging and Performance Plasticity in Honeybees. Handbook of Behavioral Neuroscience 22: 487–500.CrossRefGoogle Scholar
  20. Nelson, C. M., K. E. Ihle, M. K. Fondrk, R. E. Page and G. V. Amdam (2007). The gene vitellogenin has multiple coordinating effects on social organization. PLoS Biol 5(3): e62.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Richard, F. J., A. Aubert and C. M. Grozinger (2008). Modulation of social interactions by immune stimulation in honey bee, Apis mellifera, workers. Bmc Biology 6.Google Scholar
  22. Rueppell, O., C. Bachelier, M. K. Fondrk and R. E. Page (2007). Regulation of life history determines lifespan of worker honey bees (Apis mellifera L.). Experimental Gerontology 42(10): 1020–1032.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Rueppell, O., B. Yousefi, J. Collazo and D. Smith (2017). Early life stress affects mortality rate more than social behavior, gene expression or oxidative damage in honey bee workers. Exp Gerontol 90: 19–25.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Salmela, H., G. V. Amdam and D. Freitak (2015). Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin. Plos Pathogens 11(7): 12.CrossRefGoogle Scholar
  25. Scharlaken, B., D. C. de Graaf, K. Goossens, M. Brunain, L. J. Peelman and F. J. Jacobs (2008). Reference gene selection for insect expression studies using quantitative real-time PCR: The head of the honeybee, Apis mellifera, after a bacterial challenge. Journal of Insect Science 8.Google Scholar
  26. Schmid, M. R., A. Brockmann, C. W. W. Pirk, D. W. Stanley and J. Tautz (2008). Adult honeybees (Apis mellifera L.) abandon hemocytic, but not phenoloxidase-based immunity. Journal of Insect Physiology 54(2): 439–444.CrossRefPubMedGoogle Scholar
  27. Seehuus, S. C., K. Norberg, U. Gimsa, T. Krekling and G. V. Amdam (2006). Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proc Natl Acad Sci U S A 103(4): 962–967.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Seeley, T. D. (1995). The wisdom of the hive : the social physiology of honey bee colonies. Cambridge, Mass., Harvard University Press.Google Scholar
  29. Speth, M. T., C. D. Kreibich, G. V. Amdam and D. Munch (2015). Aging- and task-related resilience decline is linked to food responsiveness in highly social honey bees. Exp Gerontol 65: 46–52.CrossRefPubMedGoogle Scholar
  30. Wang, Y., C. S. Brent, E. Fennern and G. V. Amdam (2012). Gustatory perception and fat body energy metabolism are jointly affected by vitellogenin and juvenile hormone in honey bees. PLoS Genet 8(6): e1002779.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Wilson-Rich, N., S. T. Dres and P. T. Starks (2008). The ontogeny of immunity: Development of innate immune strength in the honey bee (Apis mellifera). Journal of Insect Physiology 54(10–11): 1392–1399.CrossRefPubMedGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Faculty of Chemistry, Biotechnology and Food ScienceNorwegian University of Life SciencesÅsNorway
  2. 2.Department of Biosciences, Centre of Excellence in Biological InteractionsUniversity of HelsinkiHelsinkiFinland
  3. 3.School of Sport, Exercise and Rehabilitation SciencesUniversity of BirminghamBirminghamUK
  4. 4.MRC-Arthritis Research UK Centre for Musculoskeletal Ageing ResearchUniversity of BirminghamBirminghamUK
  5. 5.School of Applied SciencesUniversity of HuddersfieldHuddersfieldUK
  6. 6.School of Life SciencesArizona State UniversityTempeUSA
  7. 7.Faculty of Ecology and Natural Resource ManagementNorwegian University of Life SciencesÅsNorway

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