Abstract
Parasites can inflict indirect fitness costs to their hosts by eliciting costly immune responses. These costs depend on the type and amount of immunostimulants presented to the host immune system but also on the amount of resources available to fuel host immune responses. Here, we investigated how the relative costs of two different types of immune challenge are modulated by variation in food availability. We injected nestling tawny owls (Strix aluco) with either 10 μg of phytohaemagglutinin (PHA) or 20 μg of lipopolysaccharide (LPS), and subsequently raised them under two different food regimes (food-restricted vs. ad libitum). After controlling for food consumption, we found that LPS-injected nestlings lost more body mass than PHA-injected ones only when food-restricted. We also found that body mass gain of owlets fed ad libitum decreased with the intensity of the skin swelling response against LPS, but not PHA. These experimental and correlative results suggest that nestling tawny owls suffered greater immune costs when treated with LPS than PHA, and that variation in the costs of two different types of immune challenge can be exacerbated under conditions of low food availability. Our study highlights the importance of taking into consideration the interplay between host immunity and nutrition in the study of indirect costs of parasitism.
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Amat, J. A., Aguilera, E., & Visser, G. H. (2007). Energetic and developmental costs of mounting an immune response in greenfinches (Carduelis chloris). Ecological Research, 22, 282–287.
Bertrand, S., Criscuolo, F., Faivre, B., & Sorci, G. (2006). Immune activation increases susceptibility to oxidative tissue damage in zebra finches. Functional Ecology, 20, 1022–1027.
Bize, P., Jeanneret, C., Klopfenstein, A., & Roulin, A. (2008). What makes a host profitable? Experimental evidence that parasites balance host nutritive resource against immunity. American Naturalist, 171, 107–118.
Bonneaud, C., Mazuc, J., Gonzalez, G., Haussy, C., Chastel, O., Faivre, B., et al. (2003). Assessing the cost of mounting an immune response. American Naturalist, 161, 367–379.
Brzek, P., & Konarzewski, M. (2007). Relationship between avian growth rate and immune response depends on food availability. Journal of Experimental Biology, 210, 2361–2367.
Chandra, R. K. (1996). Nutrition, immunity and infection: From basic knowledge of dietary manipulation to practical application of ameliorating suffering and improving survival. Proceedings of the National Academy of Sciences of the United States of America, 93, 14304–14307.
Cheng, H. W., Freire, R., & Pajor, E. A. (2004). Endotoxin stress responses in chickens from different genetic lines. 1. Sickness, behavioral, and physical responses. Poultry Science, 83, 707–715.
Dantzer, R., Bluthe, R. M., Gheusi, G., Cremona, S., Laye, S., Parnet, P., et al. (1998). Molecular basis of sickness behavior. Annals of the New York Academy of Sciences, 856, 132–138.
Day, T., Graham, A. L., & Read, A. F. (2007). Evolution of parasite virulence when host responses cause disease. Proceedings of the Royal Society of London Series B: Biological Sciences, 274, 2685–2692.
Fair, J. M., Hansen, E. S., & Ricklefs, R. E. (1999). Growth, developmental stability and immune response in juvenile Japanese quails (Coturnix coturnix japonica). Proceedings of the Royal Society of London Series B: Biological Sciences, 266, 1735–1742.
Frank, S. A. (1996). Models of parasite virulence. The Quarterly Review of Biology, 71, 37–78.
Galeotti, P. (2001). Tawny owl Strix aluco. Birds of the Western Palaearctic Update, 3, 43–77.
Gasparini, J., Piault, R., Bize, P., & Roulin, A. (2009). Synergetic and antagonistic interaction between different branches of the immune system is related to melanin-based coloration in nestling tawny owls. Journal of Evolutionary Biology, 22, 2348–2353.
Graham, A. L., Allen, J. E., & Read, A. F. (2005). Evolutionary causes and consequences of immunopathology. Annual Review of Ecology, Evolution, and Systematics, 36, 373–397.
Jacot, A., Scheuber, H., & Brinkhof, M. W. G. (2004). Costs of an induced immune response on sexual display and longevity in field crickets. Evolution; International Journal of Organic Evolution, 58, 2280–2286.
Kaushal, D., Schroeder, B. G., Tyagi, S., Yoshimatsu, T., Scott, C., Ko, C., et al. (2002). Reduced immunopathology and mortality despite tissue persistence in a Mycobacterium tuberculosis mutant lacking alternative sigma factor, SigH. Proceedings of the National Academy of Sciences of the United States of America, 99, 8330–8335.
Kelly, C., & Price, T. D. (2005). Correcting for regression to the mean in behaviour and ecology. American Naturalist, 166, 700–707.
Klasing, K. C. (1988). Nutritional aspects of leukocytic cytokines. Journal of Nutrition, 118, 1436–1446.
Klasing, K. C., Laurin, D. E., Peng, R. K., & Fry, D. M. (1987). Immunologically mediated growth depression in chicks—influence of feed-intake, corticosterone and interleukin-1. Journal of Nutrition, 117, 1629–1637.
Kobasa, D., Jones, S. M., Shinya, K., Kash, J. C., Copps, J., Ebihara, H., et al. (2007). Aberrant innate immune responses in lethal infection of macaques with the 1918 influenza virus. Nature, 445, 319–323.
Long, G. H., Chan, B. H. K., Allen, J. E., Read, A. F., & Graham, A. L. (2008). Experimental manipulation of immune-mediated disease and its fitness costs for rodent malaria parasites. BMC Evolutionary Biology, 8, 128.
Martin, L. B., I. I., Han, P., Lewittes, J., Kuhlman, J. R., Klasing, K. C., & Wikelski, M. (2006). Phytohemagglutinin-induced skin swelling in birds: Histological support for a classic immunoecological technique. Functional Ecology, 20, 290–299.
Martin, L. B., I. I., Scheuerlein, A., & Wikelski, M. (2003). Immune activity elevates energy expenditure of house sparrows: A link between direct and indirect costs? Proceedings of the Royal Society of London Series B: Biological Sciences, 270, 153–158.
Mayringer, I., Reindl, M., & Berger, T. (2000). A critical comparison of frequently used methods for the analysis of tumor necrosis factor-alpha expression by human immune cells. Journal of Immunological Methods, 235, 33–40.
Merino, S., Martinez, J., Moller, A. P., Sanabria, L., De Lope, F., Perez, J., et al. (1999). Phytohaemagglutinin injection assay and physiological stress in nestling house martins. Animal Behaviour, 58, 219–222.
Mire-Sluis, A. R., Wickremasinghe, R. G., Hoffbrand, A. V., Timms, A. M., & Francis, G. E. (1987). Human T lymphocytes stimulated by phytohaemagglutinin undergo a single round of cell division without a requirement for interleukin-2 or accessory cells. Immunology, 60, 7–12.
Moret, Y., & Schmid-Hempel, P. (2000). Survival for immunity: The price of immune system activation for bumblebee workers. Science, 290, 1166–1168.
Munford, R. S. (2006). Severe sepsis and septic shock: The role of gram-negative bacteremia. Annual Review of Pathology: Mechanisms of Disease, 1, 467–496.
Nossal, G. J. (1983). Cellular mechanisms of immunologic tolerance. Annual Review of Immunology, 1, 33–62.
Overskaug, K., Bolstad, J. P., Sunde, P., & Oien, I. J. (1999). Fledgling behavior and survival in northern tawny owls. Condor, 101, 169–174.
Parmentier, H. K., De Vries Reilingh, G., & Nieuwland, M. G. (1998). Kinetic and immunohistochemical characteristics of mitogen-induced cutaneous hypersensitivity in chickens selected for antibody responsiveness. Veterinary Immunology and Immunopathology, 66, 367–376.
Piault, R., Gasparini, J., Bize, P., Jenni-Eiermann, S., & Roulin, A. (2009). Phaeomelanin-based coloration and the ability to cope with variation in food supply and parasitism. American Naturalist, 174, 548–556.
Roulin, A., Ducret, B., Bize, P., Piault, R., & Ravussin, P.-A. (2008). Régime alimentaire de la Chouette hulotte Strix aluco en Suisse romande de 1986 à 2007. Nos Oiseaux, 55, 149–156.
Saladin, V., Ritschard, M., Roulin, A., Bize, P., & Richner, H. (2007). Analysis of genetic parentage in the tawny owl (Strix aluco) reveals extra-pair paternity is low. Journal of Ornithology, 148, 113–116.
Schmid-Hempel, P. (2003). Variation in immune defence as a question of evolutionary ecology. Proceedings of the Royal Society of London Series B: Biological Sciences, 270, 357–366.
Sheldon, B. C., & Verhulst, S. (1996). Ecological immunology: Costly parasite defences and trade-offs in evolutionary biology. Trends in Ecology & Evolution, 11, 317–321.
Skidmore, B. J., Chiller, J. M., Morrison, D. C., & Weigle, W. O. (1975). Immunological properties of bacterial lipopolysaccharide (Lps): Correlation between mitogenic, adjuvant, and immunogenic activities. Journal of Immunology, 114, 770–775.
Smits, J. E., Bortolotti, G. R., & Tella, J. L. (1999). Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Functional Ecology, 13, 567–572.
Stjernman, M., Raberg, L., & Nilsson, J.-A. (2008). Maximum host survival at intermediate parasite infection intensities. PLoS ONE, 3, e3463.
Tella, J. L., Lemus, J. A., Carrete, M., & Blanco, G. (2009). The PHA test reflects acquired T-cell mediated immunocompetence in birds. PLoS ONE, 3, e3295.
Yachnin, S., & Svenson, R. H. (1972). Immunological and physicochemical properties of mitogenic proteins derived from Phaseolus vulgaris. Immunology, 22, 871–883.
Zaccone, P., Burton, O. T., & Cooke, A. (2008). Interplay of parasite-driven immune responses and autoimmunity. Trends in Parasitology, 24, 35–42.
Zuk, M., & Stoehr, A. M. (2002). Immune defense and host life history. American Naturalist, 160, S9–S22.
Acknowledgments
This study was supported by the Swiss National Science Foundation (grant no. PPOOA-102913 and 31003A-120517 to AR, PPOOA-109009 to PB and PBLAP3-124279 to RP) and the Roche Research Foundation (grant no. Mkl/stm 14-2008 to RP). The experiment was approved by the veterinary services of Canton de Vaud (licence no. 1508) and birds were ringed under the legal authorization of the Swiss Agency for the Environment, Forests and Landscape.
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Pierre Bize and Romain Piault contributed equally.
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Bize, P., Piault, R., Gasparini, J. et al. Indirect Costs of Parasitism are Shaped by Variation in the Type of Immune Challenge and Food Availability. Evol Biol 37, 169–176 (2010). https://doi.org/10.1007/s11692-010-9092-5
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DOI: https://doi.org/10.1007/s11692-010-9092-5