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Starvation Reveals Maintenance Cost of Humoral Immunity

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Abstract

Susceptibility to pathogens and genetic variation in disease resistance is assumed to persist in nature because of the high costs of immunity. Within immunity there are different kinds of costs. Costs of immunological deployment, the costs of mounting an immune response, are measured as a change in fitness following immunological challenge. Maintenance costs of immunity are associated with investments of resources into the infrastructure of an immune system and keeping the system at a given level of readiness in the absence of infection. To demonstrate the costs of immunological maintenance in the absence of infection is considered more difficult. In the present study we examined the maintenance costs of the immune system in lines of Drosophila melanogaster that differed in their antibacterial innate immune response under starved and non-starved conditions. Immunodeficient mutant flies that have to invest less in the immunological maintenance were found to live longer under starvation than wild type flies, whereas the opposite was found when food was provided ad libitum. Our study provides evidence for the physiological cost of immunological maintenance and highlights the importance of environmental variation in the study of evolutionary trade-offs.

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References

  • Dushay, M. S., Asling, B., & Hultmark, D. (1996). Origins of immunity: Relish, a compound Rel-like gene in the antibacterial defense of Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 93(19), 10343–10347.

    Article  CAS  PubMed  Google Scholar 

  • Fellowes, M. D. E., Kraaijeveld, A. R., & Godfray, H. C. J. (1998). Trade-off associated with selection for increased ability to resist parasitoid attack in Drosophila melanogaster. Proceedings of the Royal Society B, 265(1405), 1553–1558.

    Article  CAS  PubMed  Google Scholar 

  • Haine, E. R., Moret, Y., Siva-Jothy, M. T., & Rolff, J. (2008). Antibacterial defense and persistent infection in insects. Science, 322, 1257–1259.

    Article  CAS  PubMed  Google Scholar 

  • Harbison, S. T., Yamamoto, A. H., Fanara, J. J., Norga, K. K., & Mackay, T. F. C. (2004). Quantitative trait loci affecting starvation resistance in Drosophila melanogaster. Genetics, 166(4), 1807–1823.

    Article  CAS  PubMed  Google Scholar 

  • Hedengren, M., Åsling, B., Dushay, M. S., Ando, I., Ekengren, S., Wihlborg, M., et al. (1999). Relish, a central factor in the control of humoral but not cellular immunity in Drosophila. Molecular Cell, 4(5), 827–837.

    Article  CAS  PubMed  Google Scholar 

  • Hoang, A. (2001). Immune response to parasitism reduces resistance of Drosophila melanogaster to desiccation and starvation. Evolution, 55(11), 2353–2358.

    CAS  PubMed  Google Scholar 

  • Hoffmann, J. A. (1995). Innate immunity of insects. Current Opinion in Immunology, 7, 4–10.

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann, A. A., Hallas, R., Sinclair, C., & Mitrovski, P. (2001). Levels of variation in stress resistance in Drosophila among strains, local populations, and geographic regions; patterns for desiccasion, starvation, cold resistance, and associated traits. Evolution, 55(8), 1621–1630.

    CAS  PubMed  Google Scholar 

  • Hoffmann, A. A., & Harshman, L. G. (1999). Desiccation and starvation resistance in Drosophila: Patterns of variation at the species, population and intrapopulation levels. Heredity, 83, 637–643.

    Article  PubMed  Google Scholar 

  • Hoffmann, A. A., & Parsons, P. A. (1989). An integrated approach to environmental stress tolerance and life-history variation: Desiccation tolerance in Drosophila. Biological Journal of the Linnean Society, 37(1–2), 117–136.

    Article  Google Scholar 

  • Hoffmann, A. A., & Parsons, P. A. (1993). Direct and correlated responses to selection for desiccation resistance: A comparison of Drosophila melanogaster and D. simulans. Journal of Evolutionary Biology, 6(5), 643–657.

    Article  Google Scholar 

  • Kraaijeveld, A. R., & Godfray, H. C. J. (1997). Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature, 389, 278–280.

    Article  CAS  PubMed  Google Scholar 

  • Kraaijeveld, A. R., Limentani, E. C., & Godfray, H. C. J. (2001). Basis of the trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Proceedings of the Royal Society B, 268, 259–261.

    Article  CAS  PubMed  Google Scholar 

  • Leclerc, V., & Reichhart, J. M. (2004). The immune response of Drosophila melanogaster. Immunological Reviews, 198(1), 59–71.

    Article  CAS  PubMed  Google Scholar 

  • Lemaitre, B., Kromer-Metzger, E., Michaut, L., Nicolas, E., Meister, M., Georgel, P., et al. (1995). A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defense. Proceedings of the National Academy of Sciences of the United States of America, 92(21), 9465–9469.

    Article  CAS  PubMed  Google Scholar 

  • Libert, S., Yufang, C., Xiaowen, C., & Pletcher, S. D. (2006). Trade-offs between longevity and pathogen resistance in Drosophila melanogaster are mediated by NFκB signaling. Aging Cell, 5, 533–543.

    Article  CAS  PubMed  Google Scholar 

  • Lochmiller, R. L., & Deerenberg, C. (2000). Trade-offs in evolutionary immunology: Just what is the cost of immunity? Oikos, 88, 87–98.

    Article  Google Scholar 

  • Luong, L. T., & Polak, M. (2007). Costs of resistance in the Drosophila–macrocheles system: A negative genetic correlation between ectoparasite resistance and reproduction. Evolution, 61(6), 1391–1402.

    Article  PubMed  Google Scholar 

  • Matova, N., & Anderson, K. V. (2006). Rel/NF-κB double mutants reveal that cellular immunity is central to Drosophila host defense. Proceedings of the National Academy of Sciences of the United States of America, 103(44), 16426–16429.

    Article  Google Scholar 

  • McKean, K. A., Yourth, C. P., Lazzaro, B. P., & Clark, A. G. (2008). The evolutionary costs of immunological maintenance and deployment. BMC Evolutionary Biology, 8, 76.

    Article  PubMed  Google Scholar 

  • Moret, Y., & Schmid-Hempel, P. (2000). Survival for immunity: The price of immune system activation for bumblebee workers. Science, 290(5494), 1166–1168.

    Article  CAS  PubMed  Google Scholar 

  • Park, J. M., Brady, H., Ruocco, M. G., Sun, H., Williams, D. A., Lee, S. J., et al. (2004). Targeting of TAK1 by the NF-κB protein Relish regulates the JNK-mediated immune response in Drosophila. Genes and Development, 18(5), 584–594.

    Article  CAS  PubMed  Google Scholar 

  • Parkash, R., & Munjal, A. K. (1999). Climatic selection of starvation and desiccation resistance in populations of some tropical Drosophilids. Journal of Zoological Systematics and Evolutionary Research, 37(4), 195–202.

    Google Scholar 

  • Price, B. D., & Laughon, A. (1993). The isolation and characterization of a Drosophila gene encoding a putative NAD-dependent methylenetetrahydrofolate dehydrogenase-methenyltetrahydrofolate cyclohydrolase. Biochimica et Biophysica Acta, 1173(1), 94–98.

    CAS  PubMed  Google Scholar 

  • Råberg, L., Vestberg, M., Hasselquist, D., Holmdahl, R., Svensson, E., & Nilsson, J. Å. (2002). Basal metabolic rate and the evolution of the adaptive immune system. Proceedings of the Royal Society B, 269(1493), 817–821.

    Article  PubMed  Google Scholar 

  • Roff, D. A. (2002). Life history evolution. Sunderland, MA: Sinauer Associates.

    Google Scholar 

  • Royet, J., Reichhart, J. M., & Hoffmann, J. A. (2005). Sensing and signaling during infection in Drosophila. Current Opinion in Immunology, 17, 11–17.

    Article  CAS  PubMed  Google Scholar 

  • Schmid-Hempel, P. (2003). Variation in immune defence as a question of evolutionary ecology. Proceedings of the Royal Society B, 270(1513), 357–366.

    Article  PubMed  Google Scholar 

  • Sgrò, C. M., & Hoffmann, A. A. (2004). Genetic correlations, tradeoffs and environmental variation. Heredity, 93, 241–248.

    Article  PubMed  Google Scholar 

  • Sheldon, B. C., & Verhulst, S. (1996). Ecological immunology: Costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology & Evolution, 11(8), 317–321.

    Article  Google Scholar 

  • Siva-Jothy, M. T., Moret, Y., & Rolff, J. (2005). Insect immunity: An evolutionary ecology perspective. Advances in Insect Physiology, 32, 1–48.

    Article  CAS  Google Scholar 

  • Speakman, J. R. (2005). Body size, energy metabolism and lifespan. Journal of Experimental Biology, 208, 1717–1730.

    Article  PubMed  Google Scholar 

  • Via, S., & Lande, R. (1985). Genotype–environment interaction and the evolution of phenotypic plasticity. Evolution, 39(3), 505–522.

    Article  Google Scholar 

  • Ye, Y. H., Chenoweth, S. F., & McGraw, E. A. (2009). Effective but costly, evolved mechanisms of defense against a virulent opportunistic pathogen in Drosophila melanogaster. PloS Pathogens, 5(4), e1000385.

    Article  PubMed  Google Scholar 

  • Zerofsky, M., Harel, E., Silverman, N., & Tatar, M. (2005). Aging of the innate immune response in Drosophila melanogaster. Aging Cell, 4(2), 103–108.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was funded by the Academy of Finland to M.J.R., the Finnish Cultural Foundation’s Varsinais-Suomi Regional Fund to T.M.V., Competitive Research Funding of the Pirkanmaa Hospital District to A.K. and by grants from the Academy of Finland, the Foundation for Pediatric Research, Sigrid Juselius Foundation, Emil Aaltonen Foundation and Competitive Research Funding of the Pirkanmaa Hospital District to M.R.

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Correspondence to Terhi M. Valtonen.

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Valtonen, T.M., Kleino, A., Rämet, M. et al. Starvation Reveals Maintenance Cost of Humoral Immunity. Evol Biol 37, 49–57 (2010). https://doi.org/10.1007/s11692-009-9078-3

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  • DOI: https://doi.org/10.1007/s11692-009-9078-3

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