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Investment in immune defense is linked to pace of life in house sparrows

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Abstract

The evidence for a relationship between life history and immune defense is equivocal, although the basic premise is intuitively appealing: animals that live short lives and reproduce early and rapidly should not waste resources on defenses they might never use. One possible reason for a lack of strong support for this hypothesis could be the inherent complexity of the vertebrate immune system. Indeed, different components of the vertebrate immune system vary in their relative costs and benefits, and therefore only some defenses may complement variation in species’ life history. To address this hypothesis, we compared multiple types of immune activity between two populations of house sparrows (Passer domesticus) with distinct life histories, one from Colon, Panama, which lay small clutches over an extended breeding season (i.e., slow-living) and the other from Princeton, New Jersey, which lay larger clutches in a smaller window of time (i.e., fast-living). We expected (a) that more costly types of immune defenses would be stronger in the slow-living sparrows and (2) that the slow-living sparrows would show a greater increase in whole-body energy expenditure after immune challenge compared to their fast-living counterparts. We found that secondary antibody response to a novel antigen was more rapid and energetic investment in immune activity was greater in slow-living sparrows. However, cell-mediated immune activity was more robust in fast-living sparrows, and other measures of defense were not different between populations. These results provide partial support for a relationship between life history and immune defense in this species, but they also indicate that this relationship is not clear-cut. Further study is necessary to identify the influence of other factors, particular pathogen environment during development, on the architecture of the immune system of wild animals.

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References

  • Adamo S (2004) How should behavioral ecologists interpret measures of immunity. Anim Behav 68:1443–1449

    Article  Google Scholar 

  • Aschoff J, Pohl H (1970) Der Ruheumsatz von Vögeln als Funktion der Tageszeit und der Körpergrösse. Journal für Ornithology 111:38–47

    Article  Google Scholar 

  • Bonneaud C, Mazuc J, Gonzalez G, Haussy C, Chastel O, Faivre B, Sorci G. (2003) Assessing the cost of mounting an immune response. Am Nat 161:367–379

    Article  PubMed  Google Scholar 

  • Cohn M, Langman R (1990) The protection: the unit of humoral immunity selected by evolution. Immunol Rev 115:7–147

    Article  Google Scholar 

  • Demas G (2004) The energetics of immunity: a neuroendocrine link between energy balance and immune function. Horm Behav 45:173–180

    Article  PubMed  CAS  Google Scholar 

  • Elgert K (1996) Immunology. Wiley-Liss, New York

    Google Scholar 

  • Folstad I, Karter A (1992) Parasites, bright males, and the immunocompetence handicap hypothesis. Am Nat 139:603–622

    Article  Google Scholar 

  • Garland T, Adolph SC (1994) Why not to do 2-species comparative studies: limitations on inferring adaptation. Physiol Zool 67:797–828

    Google Scholar 

  • Ghalambor C, Martin T (2000) Parental investment strategies in two species of nuthatch vary with stage-specific predation risk and reproductive effort. Anim Behav 60:263–267

    Article  PubMed  Google Scholar 

  • Graham A (2002) When T-helper cells don’t help: immunopathology during concomitant infection. Q Rev Biol 77:409–434

    Article  PubMed  Google Scholar 

  • Greenman C, Martin LB, Hau M (2005) Reproductive state, but not testosterone, reduces immune function in male house sparrows (Passer domesticus). Physiol Biochem Zool 78:60–68

    Article  PubMed  CAS  Google Scholar 

  • Grossman C (1985) Interactions between gonadal steroids and the immune system. Science 227:257–261

    Article  PubMed  CAS  Google Scholar 

  • Hanssen S, Hasselquist D, Folstad I, Erikstad K (2004) Severe cost of acquired immune defence in a vertebrate: humoral immune responsiveness reduces survival in elders. Proc R Soc Lond B 271:925–930

    Article  Google Scholar 

  • Harris J, Markl J (1999) Keyhole limpet hemocyanin (KLH): a biomedical approach. Micron 30:597–623

    Article  PubMed  CAS  Google Scholar 

  • Hasselquist D, Marsh J, Sherman P, Wingfield J (1999) Is avian humoral immunocompetence suppressed by testosterone? Behav Ecol Sociobiol 45:167–175

    Article  Google Scholar 

  • Ilmonen P, Taarna T, Hasselquist D (2000) Experimentally activated immune defence in female pied flycatchers results in reduced breeding success. Proc R Soc Lond B Biol Sci 267:665–670

    Article  CAS  Google Scholar 

  • Kaufmann S, Sher A, Ahmed R (2002) Immunology of infectious diseases. ASM Press, Washington

    Google Scholar 

  • Kendeigh C (1976) Latitudinal trends in the metabolic adjustments of the house sparrow. Ecology 57:509–519

    Article  Google Scholar 

  • Kendeigh C, Blem CB (1974) Metabolic adaptation to local climate in birds. Comp Biochem Physiol 48A:175–187

    Article  Google Scholar 

  • Klasing KC, Leshchinsky T (1999) Functions, costs, and benefits of the immune system during development and growth. Pages 2817 –2835 In: Adams N, Slotow R, (eds) Proceedings of the 22nd International Ornithological Congress. Durban University of Natal Press, Durban, South Africa

  • Klasing KC (2002) The avian immune system: nutritional costs of ownership and use. Proceedings of the 23rd International Ornithological Congress, p 6–7

  • Klein S, Gamble H, Nelson RJ (1999) Role of steroid hormones in Trichnella spiralis infections among voles. Am J Physiol: Regul Integr Comp Physiol 277:R1362–R1367

    CAS  Google Scholar 

  • Kreukniet M, Gianotten N, Nieuwland M, Parmentier H (1994) In vitro T cell activity in two chicken lines divergently selected for antibody response to sheep erythrocytes. Poult Sci 73:336–340

    PubMed  CAS  Google Scholar 

  • Lee KA, Martin LB, Wikelski M. 2005. Responding to inflammatory challenges is less costly for a successful avian invader, the house sparrow (Passer domesticus), than its less invasive congener. Oecologia 145:244–251

    Article  PubMed  Google Scholar 

  • Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98

    Article  Google Scholar 

  • Martin LB, Scheuerlein A, Wikelski M (2003) Immune activity elevates energy expenditure of House Sparrows: a link between direct and indirect costs. Proc R Soc Lond B Biol Sci 270:153–158

    Article  Google Scholar 

  • Martin LB, Pless M, Svoboda J, Wikelski M (2004) Immune function in tropical and temperate house sparrows: a common garden experiment. Ecology 85:2323–2331

    Article  Google Scholar 

  • Martin LB (2005) Trade-offs between molt and immune activity in two populations of house sparrows (Passer domesticus). Can J Zool 83:780–787

    Article  Google Scholar 

  • Martin LB, Gilliam J, Han P, Lee K, Wikelski M (2005) Corticosterone suppresses immune function in temperate but not tropical house sparrows (Passer domesticus). Gen Comp Endocrinol 140:126–135

    Article  CAS  Google Scholar 

  • Martin LB, Fitzgerald L (2005) A taste for novelty in invading house sparrows. Behav Ecol 16:702–707

    Article  Google Scholar 

  • Martin TE, Møller AP, Merino S, Clobert J (2001) Does clutch size evolve in response to parasites and immunocompetence? Proc Natl Acad Sci 98:2071–2076

    Article  PubMed  CAS  Google Scholar 

  • Matson K, Ricklefs RE, Klasing KC (2005) A hemolysis–hemagglutination assay for characterizing constitutive innate humoral immunity in wild and domestic birds. Dev Comp Immunol 29:275–286

    Article  PubMed  CAS  Google Scholar 

  • Matson K, Scheuerlein A, Ricklefs RE (2002). Comparative immunology of tropical and temperate birds. Proceedings of the 23rd International Ornithological Congress, pp 199

  • Nelson RJ (2004) Seasonal immune function and disease responses. Trends Immunol 24:187–192

    Article  Google Scholar 

  • Nelson RJ, Demas GE (1996) Seasonal changes in immune function. Q Rev Biol 71:511–548

    Article  PubMed  CAS  Google Scholar 

  • Norris K, Evans M (2000) Ecological immunology: life history trade-offs and immune defense in birds. Behav Ecol 11:19–26

    Article  Google Scholar 

  • North C (1973) Population dynamics of the House Sparrow Passer domesticus (L.) in Wisconsin, USA. In: Kendeigh SC, Pinowska J (eds) Productivity, population dynamics, and systematics of granivorous birds. Institute of Ecology, Dziekanow, Poland, pp 195–210

    Google Scholar 

  • Nunn C (2002) A comparative study of leukocyte counts and disease risk in primates. Evolution 56:177–190

    PubMed  Google Scholar 

  • Owen-Ashley N, Hasselquist D, Wingfield J (2004) Androgens and the immunocompetence handicap hypothesis: unraveling direct and indirect pathways of immunosuppression in song sparrows. Am Nat 490–505

  • Owens I, Wilson K (1999) Immunocompetence: a neglected life history trait or conspicuous red herring? Trends Ecol Evol 14:170–172

    Article  Google Scholar 

  • Parmentier H, Nieuwland M, Rijke E, De Vries Reilingh G, Schrama J (1996) Divergent antibody responses to vaccines and divergent body weights of chickens selected for high and low humoral responsiveness to sheep red blood cells. Avian Dis 40:634–644

    Article  PubMed  CAS  Google Scholar 

  • Parmentier H, Lammers A, Hoekman J, De Vries Reilingh G, Zaanen I, Savelkoul H (2004) Different levels of natural antibodies in chickens divergently selected for specific antibody responses. Dev Comp Immunol 28:39–49

    Article  PubMed  CAS  Google Scholar 

  • Piersma T (1997) Do global patterns of habitat use and migration strategies co-evolve with relative investments in immunocompetence due to spatial variation in parasite pressure? Oikos 80:623–631

    Article  Google Scholar 

  • Råberg L, Grahn M, Hasselquist D, Svensson E (1998) On the adaptive significance of stress-induced immunosuppression. Proc R Soc Lond B 265:1637–1641

    Article  Google Scholar 

  • Råberg L, Nilsson J-Å, Ilmonen P, Stjernman M, Hasselquist D (2000) The cost of an immune response: vaccination reduces parental effort. Ecol Lett 3:382–386

    Article  Google Scholar 

  • Råberg L, Vestberg M, Hasselquist D, Holmdahl R, Svensson E Nilsson J-Å (2002) Energetic benefits of the adaptive immune system. Proc R Soc B 269:817–821

    Article  PubMed  Google Scholar 

  • Ricklefs R (1992) Embryonic development period and the prevalence of avian blood parasites. Proc Natl Acad Sci 89:4722–4725

    Article  PubMed  CAS  Google Scholar 

  • Ricklefs R, Wikelski M (2002) The physiology—life history nexus. Trends Ecol Evol 17:462–468

    Article  Google Scholar 

  • Ridgely R, Gwynne Jr J (1989) A guide to the birds of Panama with Costa Rica, Nicaragua, and Honduras 2nd edn. Princeton University Press, Princeton

    Google Scholar 

  • Sanz JJ, Moreno J, Merino S, Tomas G (2004) A trade-off between two resource-demanding functions: post-nuptial moult and immunity during reproduction in male pied flycatchers. J Anim Ecol 73:441–447

    Article  Google Scholar 

  • Sapolsky R, Romero LM, Munck A (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrinol Rev 21:55–89

    Article  CAS  Google Scholar 

  • Schmid-Hempel P, Ebert D (2003) On the evolutionary ecology of specific immune defence. Trends Ecol Evol 18:27–32

    Article  Google Scholar 

  • Sheldon B, Verhulst S (1996) Ecological immunology: costly parasite defenses and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321

    Article  Google Scholar 

  • Smith A, Vollmer-Conna U, Geczy A, Dunckley H, Bennett B, Hickie I, Lloyd A (2005) Does genotype mask the relationship between psychological factors and immune function? Brain Behav Immun 19:147–152

    Article  PubMed  CAS  Google Scholar 

  • Stadecker M, Lukic M, Dvorak A, Leskowitz S (1977) The cutaneous basophil response to phytohemagglutinin in chickens. J Immunol 118:1564–1568

    PubMed  CAS  Google Scholar 

  • Summers-Smith J (1988) The sparrows: a study of the genus Passer. T & AD Poyser, Staffordshire

    Google Scholar 

  • Tella J, Scheuerlein A, Ricklefs RE (2002) Is cell-mediated immunity related to the evolution of life history strategies of birds? Proc R Soc Lond B 269:1059–1066

    Article  Google Scholar 

  • Turk JL (1967) Delayed hypersensitivity. Wiley, New York

    Google Scholar 

  • Weathers W, Greene E (1998) Thermoregulatory responses of bridled and juniper titmice to high temperature. Condor 100:365–372

    Article  Google Scholar 

  • Wikelski M, Spinney L, Schelsky W, Scheuerlein A, Gwinner E (2003) Slow pace of life in tropical sedentary birds: a common-garden experiment on four stonechat populations from different latitudes. Proc R Soc Lond 270:2383–2388

    Article  Google Scholar 

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Acknowledgements

Many people helped with assays and bird care and capture including Paula Capece, Lisa Fitzgerald, Peggy Han, Kelly Lee, Lars Råberg, and Laura Spinney. We thank the management of the Belle Mead Farmer’s Co-op and the Princeton Shopping Center for allowing us to work on their property in New Jersey, and Jeanne Altmann, Michaela Hau, Henry Horn, Kirk Klasing, Dustin Rubenstein, Alex Scheuerlein and Brian Trainor for comments on earlier drafts. We thank Robert Ricklefs for allowing us to conduct the NAb assay in his lab, and Kevin Matson for assistance in performing the assay. Funding for this work comes from grants to LBM from the American Museum of Natural History, the American Ornithologist’s Union, the Princeton University Program in Latin American Studies, the Pew Charitable Trusts Training Program in Biocomplexity, and the US Environmental Protection Agency STAR Fellowship, to DH from the Swedish Research Council for Environment, Agriculture and Spatial Planning (FORMAS), Crafoord Foundation, and Carl Tryggers Foundation, and to MW from NSF-IRCEB #0212587. All methods used in this study were approved by the Princeton University Institutional Animal Care and Use Committee (protocol number 1492), the National Environmental Authority of Panama (ANAM), and the Smithsonian Tropical Research Institute (STRI).

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, USA

    Lynn B. Martin II & Martin Wikelski

  2. Department of Animal Ecology, Lund University, Lund, Sweden

    Dennis Hasselquist

  3. Departments of Psychology and Neuroscience, The Ohio State University, Townshend Hall, Columbus, OH, 43210, USA

    Lynn B. Martin II

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  1. Lynn B. Martin II
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Correspondence to Lynn B. Martin II.

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Communicated by Carol Vleck

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Martin II, L.B., Hasselquist, D. & Wikelski, M. Investment in immune defense is linked to pace of life in house sparrows. Oecologia 147, 565–575 (2006). https://doi.org/10.1007/s00442-005-0314-y

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