Living fast and dying of infection: Host life history drives interspecific variation in infection and disease risk

Ecology Letters

Volumn 15, Issue 3, 2012, Pages 235-242

  Johnson, Pieter T J ^a   Rohr, Jason R ^b   Hoverman, Jason T ^a   Kellermanns, Esra ^a   Bowerman, Jay ^c   Lunde, Kevin B ^d  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c Sunriver Nature Center   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amphibian decline; Conservation; Dilution effect; Emerging disease; Immunoecology; Phylogenetic comparative methods; Ribeiroia ondatrae; Trematode

Indexed keywords

AMPHIBIA; RIBEIROIA ONDATRAE; TREMATODA;

EID: 84931748965     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/j.1461-0248.2011.01730.x     Document Type: Article

References (50)

1. Arriero, E. & Moller, A.P. (2008). Host ecology and life-history traits associated with blood parasite species richness in birds. J. Evol. Biol., 21, 1504-1513.
2. Blackwell, A.D., Snodgrass, J.J., Madimenos, F.C. & Sugiyama, L.S. (2010). Life history, immune function, and intestinal helminths: trade-offs among immunoglobulin e, c-reactive protein, and growth in an amazonian population. Am. J. Hum. Biol., 22, 836-848.
3. Borer, E.T., Mitchell, C.E., Power, A.G. & Seabloom, E.W. (2009). Consumers indirectly increase infection risk in grassland food webs. Proc. Natl Acad. Sci. USA, 106, 503-506.
4. Burnham, K.P. & Anderson, D.R. (2002). Model Selection and Multimodel Inference. Springer-Verlag, New York, NY.
5. Craft, M.E., Hawthorne, P.L., Packer, C. & Dobson, A.P. (2008). Dynamics of a multihost pathogen in a carnivore community. J. Anim. Ecol., 77, 1257-1264.
6. Cronin, J.P., Welsh, M.E., Dekkers, M.G., Abercrombie, S.T. & Mitchell, C.E. (2010). Host physiological phenotype explains pathogen reservoir potential. Ecol. Lett., 13, 1221-1232.
7. Daszak, P., Cunningham, A.A. & Hyatt, A.D. (2000). Wildlife ecology - emerging infectious diseases of wildlife: threats to biodiversity and human health. Science, 287, 443-449.
8. Frost, D.R., Grant, T., Faivovich, J., Bain, R.H., Haas, A., Haddad, C.F.B. et al. (2006). The amphibian tree of life. Bull. Am. Mus. Nat. Hist., 297, 8-370.
9. Gilbert, G.S. & Webb, C.O. (2007). Phylogenetic signal in plant pathogen-host range. Proc. Natl Acad. Sci. USA, 104, 4979-4983.
10. Hart, B.L. (1994). Behavioral defense against parasites - interaction with parasite invasiveness. Parasitology, 109, S139-S151.
11. Hasselquist, D. (2007). Comparative immunoecology in birds: hypotheses and tests. J. Ornithol., 148, S571-S582.
12. Hawley, D.M. & Altizer, S.M. (2010). Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Funct. Ecol., 25, 48-60.
13. Haydon, D.T., Cleaveland, S., Taylor, L.H. & Laurenson, M.K. (2002). Identifying reservoirs of infection: a conceptual and practical challenge. Emerg. Infect. Dis., 8, 1468-1473.
14. Johnson, P.T.J. & Hartson, R.B. (2009). All hosts are not equal: explaining differential patterns of malformations in an amphibian community. J. Anim. Ecol., 78, 191-201.
15. Johnson, P.T.J., Lunde, K.B., Ritchie, E.G. & Launer, A.E. (1999). The effect of trematode infection on amphibian limb development and survivorship. Science, 284, 802-804.
16. Johnson, P.T.J., Lunde, K.B., Ritchie, E.G., Reaser, J.K. & Launer, A.E. (2001). Morphological abnormality patterns in a California amphibian community. Herpetologica, 57, 336-352.
17. Johnson, P.T.J., Kellermanns, E. & Bowerman, J. (2011). Critical windows of disease risk: amphibian pathology driven by developmental changes in host resistance and tolerance. Funct. Ecol., 25, 726-734.
18. Jones, K.E., Patel, N.G., Levy, M.A., Storeygard, A., Balk, D., Gittleman, J.L. et al. (2008). Global trends in emerging infectious diseases. Nature, 451, 990-994.
19. Keesing, F., Holt, R.D. & Ostfeld, R.S. (2006). Effects of species diversity on disease risk. Ecol. Lett., 9, 485-498.
20. Kilpatrick, A.M., Daszak, P., Jones, M.J., Marra, P.P. & Kramer, L.D. (2006). Host heterogeneity dominates West Nile virus transmission. Proc. R. Soc. Lond. [Biol.], 273, 2327-2333.
21. Knowles, S.C.L., Nakagawa, S. & Sheldon, B.C. (2009). Elevated reproductive effort increases blood parasitaemia and decreases immune function in birds: a meta-regression approach. Funct. Ecol., 23, 405-415.
22. Komar, N., Langevin, S., Hinten, S., Nemeth, N., Edwards, E., Hettler, D. et al. (2003). Experimental infection of North American birds with the New York 1999 strain of West Nile virus. Emerg. Infect. Dis., 9, 311-322.
23. LaDeau, S.L., Kilpatrick, A.M. & Marra, P.P. (2007). West Nile virus emergence and large-scale declines of North American bird populations. Nature, 447, 710-714.
24. Lee, K.A. (2006). Linking immune defences and life history at the levels of the individual and the species. Integr. Comp. Biol., 46, 1000-1015.
25. Lee, K.A., Wikelski, M., Robinson, W.D., Robinson, T.R. & Klasing, K.C. (2008). Constitutive immune defences correlate with life-history variables in tropical birds. J. Anim. Ecol., 77, 356-363.
26. Lochmiller, R.L. & Deerenberg, C. (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos, 88, 87-98.
27. LoGiudice, K., Ostfeld, R.S., Schmidt, K.A. & Keesing, F. (2003). The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proc. Natl Acad. Sci. USA, 100, 567-571.
28. Martin, L.B., Hasselquist, D. & Wikelski, M. (2006a). Investment in immune defense is linked to pace of life in house sparrows. Oecologia, 147, 565-575.
29. Martin, L.B., Weil, Z.M. & Nelson, R.J. (2006b). Refining approaches and diversifying directions in ecoimmunology. Integr. Comp. Biol., 46, 1030-1039.
30. Martin, L.B., Weil, Z.M. & Nelson, R.J. (2007). Immune defense and reproductive pace of life in Peromyscus mice. Ecology, 88, 2516-2528.
31. Martins, E.P. & Hansen, T.F. (1997). Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am. Nat., 149, 646-667.
32. McGarigal, K., Cushman, S. & Stafford, S.G. (2000). Multivariate Statistics for Wildlife and Ecology Research. Springer, New York.
33. Miller, M.R., White, A. & Boots, M. (2007). Host life span and the evolution of resistance characteristics. Evolution, 61, 2-14.
34. Ostfeld, R. & Keesing, F. (2000). The function of biodiversity in the ecology of vector-borne zoonotic diseases. Can. J. Zool., 78, 2061-2078.
35. Paradis, E., Bolker, B., Claude, J., Cuong, H.S., Desper, R., Durand, B. et al. (2011). Package 'ape', version 2.8. Analyses of phylogenetics and evolution. .
36. Poulin, R. & Morand, S. (2004). Parasite Biodiversity. Smithsonian Books, Washington D.C.
37. Promislow, D.E.L. & Harvey, P.H. (1990). Living fast and dying young - a comparative analysis of life history variation among mammals. J. Zool., 220, 417-437.
38. Purvis, A., Gittleman, J.L., Cowlishaw, G. & Mace, G.M. (2000). Predicting extinction risk in declining species. Proc. R. Soc. Lond. [Biol.], 267, 1947-1952.
39. R Development Core Team (2008). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL .
40. Råberg, L., Graham, A.L. & Read, A.F. (2009). Decomposing health: tolerance and resistance to parasites in animals. Philos. Trans. R. Soc. Lond. [Biol.], 364, 37-49.
41. Ricklefs, R.E. & Wikelski, M. (2002). The physiology/life-history nexus. Trends Ecol. Evol., 17, 462-468.
42. Rohr, J.R., Raffel, T.R. & Hall, C.A. (2010). Developmental variation in resistance and tolerance in a multi-host-parasite system. Funct. Ecol., 24, 1110-1121.
43. Rosseel, Y., Oberski, D. & Byrnes, J. (2011). Latent variable analysis v. 0.4-10. .
44. Schmid-Hempel, P. & Ebert, D. (2003). On the evolutionary ecology of specific immune defence. Trends Ecol. Evol., 18, 27-32.
45. Sparkman, A.M. & Palacios, M.G. (2009). A test of life-history theories of immune defence in two ecotypes of the garter snake, Thamnophis elegans. J. Anim. Ecol., 78, 1242-1248.
46. Stearns, S.C. (1992). The Evolution of Life Histories. Oxford University Press, New York.
47. Tieleman, B.I., Williams, J.B., Ricklefs, R.E. & Klasing, K.C. (2005). Constitutive innate immunity is a component of the pace-of-life syndrome in tropical birds. Proc. R. Soc. Lond. [Biol.], 272, 1715-1720.
48. Todd, B.D. (2007). Parasites lost? An overlooked hypothesis for the evolution of alternative reproductive strategies in amphibians. Am. Nat., 170, 793-799.
49. Viney, M.E., Riley, E.M. & Buchanan, K.L. (2005). Optimal immune responses: immunocompetence revisited. Trends Ecol. Evol., 20, 665-669.
50. Zuk, M. & Stoehr, A.M. (2002). Immune defense and host life history. Am. Nat., 160, S9-S22.