Impact of host nutritional status on infection dynamics and parasite virulence in a bird-malaria system

Journal of Animal Ecology

Volumn 83, Issue 1, 2014, Pages 256-265

  Cornet, Stéphane ^a,b   Bichet, Coraline ^c   Larcombe, Stephen ^d   Faivre, Bruno ^c   Sorci, Gabriele ^c  

^a University de Montpellier   (France)

^b CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^c UNIVERSITÉ DE BOURGOGNE   (France)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Avian malaria; Environmental variation; Host parasite interaction; Nutrition; Pathogen; Plasmodium relictum; Virulence

Indexed keywords

AVIAN INFLUENZA; BIRD; ENVIRONMENTAL CHANGE; FOOD SUPPLEMENTATION; HOST-PARASITE INTERACTION; INFECTIOUS DISEASE; MALARIA; NUTRITIONAL STATUS; VIRULENCE;

AVES; PLASMODIUM PARASITES; PLASMODIUM RELICTUM;

ANIMAL; ANIMAL DISEASE; ANIMAL FOOD; ARTICLE; AVIAN MALARIA; CANARY; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DIET; ENVIRONMENTAL VARIATION; HOST-PARASITE INTERACTION; MALARIA; NUTRITION; NUTRITIONAL STATUS; PARASITEMIA; PARASITOLOGY; PATHOGENESIS; PATHOGENICITY; PHYSIOLOGY; PLASMODIUM; PLASMODIUM RELICTUM; RANDOMIZED CONTROLLED TRIAL; VIRULENCE;

AVIAN MALARIA; ENVIRONMENTAL VARIATION; HOST-PARASITE INTERACTION; NUTRITION; PATHOGEN; PLASMODIUM RELICTUM; VIRULENCE;

ANIMAL FEED; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; CANARIES; DIET; MALARIA; NUTRITIONAL STATUS; PARASITEMIA; PLASMODIUM; VIRULENCE;

EID: 84890796706     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/1365-2656.12113     Document Type: Article

References (79)

1. Adamo, S.A. (2004) How should behavioural ecologists interpret measurements of immunity? Animal Behaviour, 68, 1443-1449.
2. Atkinson, C.T., Woods, K.L., Dusek, R.J., Sileo, L.S. & Iko, W.M. (1995) Wildlife disease and conservation in Hawaii: pathogenicity of avian malaria (Plasmodium relictum) in experimentally infected Iiwi (Vestiaria coccinea). Parasitology, 111, S59-S69.
3. Atkinson, C.T., Dusek, R.J., Woods, K.L. & Iko, W.M. (2000) Pathogenicity of avian malaria in experimentally-infected Hawaii Amakihi. Journal of Wildlife Diseases, 36, 197-204.
4. Ayres, J.S. & Schneider, D.S. (2012) Tolerance of infections. Annual Review of Immunology, 30, 271-294.
5. Beck, M.A., Handy, J. & Levander, O.A. (2004) Host nutritional status: the neglected virulence factor. Trends in Microbiology, 12, 417-423.
6. Bedhomme, S., Agnew, P., Sidobre, C. & Michalakis, Y. (2004) Virulence reaction norms across a food gradient. Proceedings of the Royal Society of London. Series B, Biological Sciences, 271, 739-744.
7. Bendich, A. (2001) Micronutrients in women's health and immune function. Nutrition, 17, 858-867.
8. Bichet, C., Cornet, S., Larcombe, S. & Sorci, G. (2012) Experimental inhibition of nitric oxide increases Plasmodium relictum (lineage SGS1) parasitemia. Experimental Parasitology, 132, 417-423.
9. Bize, P., Jeanneret, C., Klopfenstein, A. & Roulin, A. (2008) What makes a host profitable? Parasites balance host nutritive resources against immunity. The American Naturalist, 171, 107-118.
10. Brown, M.J.F., Loosli, R. & Schmid-Hempel, P. (2000) Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos, 91, 421-427.
11. Buckling, A. & Read, A.F. (2001) The effect of partial host immunity on the transmission of malaria parasites. Proceedings of the Royal Society of London. Series B, Biological Sciences, 268, 2325-2330.
12. Cahill, A.E., Aiello-Lammens, M.E., Fisher-Reid, M.C., Hua, X., Karanewsky, C.J., Yeong Ryu, H. et al. (2013) How does climate change cause extinction? Proceedings of the Royal Society. B, Biological Sciences, 280, 20121890.
13. Cellier-Holzem, E., Esparza-Salas, R., Garnier, S. & Sorci, G. (2010) Effect of repeated exposure to Plasmodium relictum (lineage SGS1) on infection dynamics in domestic canaries. International Journal for Parasitology, 40, 1447-1453.
14. Cha, H.R., Chang, S.Y., Chang, J.H., Kim, J.O., Yang, J.Y., Kim, C.H. et al. (2010) Downregulation of Th17 cells in the small intestine by disruption of gut flora in the absence of retinoic acid. Journal of Immunology, 184, 6799-6806.
15. Chandra, R.K. (1996) Nutrition, immunity and infection: from basic knowledge of dietary manipulation of immune responses 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.
16. Cornet, S., Nicot, A., Rivero, A. & Gandon, S. (2013) Malaria infection increases bird attractiveness to uninfected mosquitoes. Ecology Letters, 16, 323-329.
17. Cosgrove, C.L., Wood, M.J., Day, K.P. & Sheldon, B.C. (2008) Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. Journal of Animal Ecology, 77, 540-548.
18. 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.
19. Day, T., Graham, A.L. & Read, A.F. (2007) Evolution of parasite virulence when host responses cause disease. Proceedings of the Royal Society. B, Biological Sciences, 274, 2685-2692.
20. Ebert, D. (1998) Experimental evolution of parasites. Science, 282, 1432-1436.
21. Garamszegi, L.Z. (2011) Climate change increases the risk of malaria in birds. Global Change Biology, 17, 1751-1759.
22. Glaizot, O., Fumagalli, L., Iritano, K., Lalubin, F., Van Rooyen, J. & Christe, P. (2012) High prevalence and lineage diversity of avian malaria in wild populations of Great Tits (Parus major) and mosquitoes (Culex pipiens). PLoS ONE, 7, e34964.
23. Gonzalez, G., Sorci, G., Møller, A.P., Ninni, P., Haussy, C. & De Lope, F. (1999) Immunocompetence and condition-dependent sexual advertisement in male house sparrows (Passer domesticus). Journal of Animal Ecology, 68, 1225-1234.
24. Graham, A.L., Allen, J.E. & Read, A.F. (2005a) Evolutionary causes and consequences of immunopathology. Annual Review of Ecology, Evolution and Systematics, 36, 373-397.
25. Graham, A.L., Lamb, T.J., Read, A.F. & Allen, J.E. (2005b) Malaria-filaria coinfection in mice makes malarial disease more severe unless filarial infection achieves patency. Journal of Infectious Diseases, 191, 410-421.
26. Grau, G.E.R. & Craig, A.G. (2012) Cerebral malaria pathogenesis: revisiting parasite and host contributions. Future Microbiology, 7, 291-302.
27. Hall, S.R., Knight, C.J., Becker, C.R., Duffy, M.A., Tessier, A.J. & Caceres, C.E. (2009) Quality matters: resource quality for hosts and the timing of epidemics. Ecology Letters, 12, 118-128.
28. Humphrey, J.H. (2009) Child undernutrition, tropical enteropathy, toilets, and handwashing. Lancet, 374, 1032-1035.
29. 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, 990-993.
30. Kau, A.L., Ahern, P.P., Griffin, N.W., Goodman, A.L. & Gordon, J.I. (2011) Human nutrition, the gut microbiome and the immune system. Nature, 474, 327-336.
31. Knowles, S.C.L., Palinauskas, V. & Sheldon, B.C. (2009) Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from a wild bird population. Journal of Evolutionary Biology, 23, 557-569.
32. Krasnov, B.R., Khokhlova, I.S., Arakelyan, M.S. & Degen, A.A. (2005) Is a starving host tastier? Reproduction in fleas parasitizing food-limited rodents. Functional Ecology, 19, 625-631.
33. Kubinak, J.L., Ruff, J.S., Hyzer, C.W., Slev, P.R. & Potts, W.K. (2012) Experimental viral evolution to specific host MHC genotypes reveals fitness and virulence trade-offs in alternative MHC types. Proceedings of the National Academy of Sciences, 109, 3422-3427.
34. Lachish, S., Knowles, S.C.L., Alves, R., Wood, M.J. & Sheldon, B.C. (2011) Fitness effects of endemic malaria infections in a wild bird population: the importance of ecological structure. Journal of Animal Ecology, 80, 1196-1206.
35. Lamikanra, A.A., Brown, D., Potocnik, A., Casals-Pascual, C., Langhorne, J. & Roberts, D.J. (2007) Malarial anemia: of mice and men. Blood, 110, 18-28.
36. Lazzaro, B.P. & Little, T.J. (2009) Immunity in a variable world. Philosophical Transactions of the Royal Society. B, Biological Sciences, 364, 15-26.
37. Little, T., Birch, J., Vale, P. & Tseng, M. (2007) Parasite transgenerational effects on infection. Evolutionary Ecology Research, 9, 459-469.
38. Loiseau, C., Zoorob, R., Garnier, S., Birard, J., Federici, P., Julliard, R. et al. (2008) Antagonistic effects of a Mhc class I allele on malaria-infected house sparrows. Ecology Letters, 11, 258-265.
39. Loiseau, C., Zoorob, R., Robert, A., Chastel, O., Julliard, R. & Sorci, G. (2011) Plasmodium relictum infection and MHC diversity in the house sparrow (Passer domesticus). Proceedings of the Royal Society. B, Biological Sciences, 278, 1264-1272.
40. Loiseau, C., Harrigan, R.J., Bichet, C., Julliard, R., Garnier, S., Lendvai, A.Z. et al. (2013) Predictions of avian Plasmodium expansion under climate change. Scientific Reports, 3, 1126.
41. Long, G.H. & Graham, A.L. (2011) Consequences of immunopathology for pathogen virulence evolution and public health: malaria as a case study. Evolutionary Applications, 4, 278-291.
42. Mackinnon, M.J. & Read, A.F. (2003) The effects of host immunity on virulence-transmissibility relationships in the rodent malaria parasite Plasmodium chabaudi. Parasitology, 126, 103-112.
43. McGraw, K.J. & Ardia, D.R. (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. The American Naturalist, 162, 704-712.
44. Medzhitov, R., Schneider, D.S. & Soares, M.P. (2012) Disease tolerance as a defense strategy. Science, 335, 936-941.
45. Metcalf, C.J.E., Graham, A.L., Huijben, S., Barclay, V.C., Long, G.H., Grenfell, B.T. et al. (2011) Partitioning regulatory mechanisms of within-host malaria dynamics using the effective propagation number. Science, 333, 984-988.
46. Miller, M.R., White, A. & Boots, M. (2006) The evolution of parasites in response to tolerance in their hosts: the good, the bad, and apparent commensalism. Evolution, 60, 945-956.
47. Mora, J.R., Iwata, M. & von Andrian, U.H. (2008) Vitamin effects on the immune system: vitamins A and D take centre stage. Nature Reviews Immunology, 8, 685-698.
48. Mostowy, R. & Engelstadter, J. (2011) The impact of environmental change on host-parasite coevolutionary dynamics. Proceedings of the Royal Society. B, Biological Sciences, 278, 2283-2292.
49. Paaijmans, K.P., Blanford, S., Bell, A.S., Blanford, J.I., Read, A.F. & Thomas, M.B. (2010) Influence of climate on malaria transmission depends on daily temperature variation. Proceedings of the National Academy of Sciences, USA, 107, 15135-15139.
50. Palinauskas, V., Valkiunas, G.N., Bolshakov, C.V. & Bensch, S. (2008) Plasmodium relictum (lineage P-SGS1): effects on experimentally infected passerine birds. Experimental Parasitology, 120, 372-380.
51. Pamplona, A., Ferreira, A., Balla, J., Jeney, V., Balla, G., Epiphanio, S. et al. (2007) Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nature Medicine, 13, 703-710.
52. Percario, S., Moreira, D.R., Gomes, B.A.Q., Ferreira, M.E.S., Gonçalves, A.C.M., Laurindo, P.S.O.C. et al. (2012) Oxidative stress in malaria. International Journal of Molecular Sciences, 13, 16346-16372.
53. Pollitt, L.C., Reece, S.E., Mideo, N., Nussey, D.H. & Colegrave, N. (2012) The problem of auto-correlation in parasitology. PLoS Pathogens, 8, e1002590.
54. Pulkkinen, K. & Ebert, D. (2004) Host starvation decreases parasite load and mean host size in experimental populations. Ecology, 85, 823-833.
55. Råberg, L., Graham, A.L. & Read, A.F. (2009) Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society. B, Biological Sciences, 364, 37-49.
56. Råberg, L., Sim, D. & Read, A.F. (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science, 318, 812-814.
57. Read, A.F., Graham, A.L. & Råberg, L. (2008) Animal defenses against infectious agents: is damage control more important than pathogen control? Plos Biology, 6, e1000004.
58. Scrimshaw, N.S., Taylor, C.E. & Gordon, J.E. (1959) Interactions of nutrition and infection. American Journal of the Medical Sciences, 237, 367-403.
59. Sears, B.F., Rohr, J.R., Allen, J.E. & Martin, L.B. (2011) The economy of inflammation: when is less more? Trends in Parasitology, 27, 382-387.
60. Seixas, E., Gozzelino, R., Chora, A., Ferreira, A., Silva, G., Larsen, R. et al. (2009) Heme oxygenase-1 affords protection against noncerebral forms of severe malaria. Proceedings of the National Academy of Sciences of the United States of America, 106, 15837-15842.
61. Seppälä, O., Liljeroos, K., Karvonen, A. & Jokela, J. (2008) Host condition as a constraint for parasite reproduction. Oikos, 117, 749-753.
62. Sergent, E. & Sergent, E. (1952) Recherches expérimentales sur l'infection latente et prémunition dans le paludisme. Archives de l'Institut Pasteur d'Algérie Institut Pasteur d'Algérie, 30, 203-239.
63. Siva-Jothy, M.T. & Thompson, J.J.W. (2002) Short-term nutrient deprivation affects immune function. Physiological Entomology, 27, 206-212.
64. Smith, H.G., Råberg, L., Ohlsson, T., Granbom, M. & Hasselquist, D. (2007) Carotenoid and protein supplementation have differential effects on pheasant ornamentation and immunity. Journal of Evolutionary Biology, 20, 310-319.
65. Sorci, G., Cornet, S. & Faivre, B. (2013) Immunity and the emergence of virulent pathogens. Infection, Genetics and Evolution, 16, 441-446.
66. Sorci, G. & Faivre, B. (2009) Inflammation and oxidative stress in vertebrate host-parasite systems. Philosophical Transactions of the Royal Society. B, Biological Sciences, 364, 71-83.
67. Szöllösi, E., Cichon, M., Eens, M., Hasselquist, D., Kempenaers, B., Merino, S. et al. (2011) Determinants of distribution and prevalence of avian malaria in blue tit populations across Europe: separating host and parasite effects. Journal of Evolutionary Biology, 24, 2014-2024.
68. Tschirren, B., Bischoff, L.L., Saladin, V. & Richner, H. (2007) Host condition and host immunity affect parasite fitness in a bird-ectoparasite system. Functional Ecology, 21, 372-378.
69. Tseng, M. (2006) Interactions between the parasite's previous and current environment mediate the outcome of parasite infection. The American Naturalist, 168, 565-571.
70. Vale, P.F., Wilson, A.J., Best, A., Boots, M. & Little, T.J. (2011) Epidemiological, evolutionary, and coevolutionary implications of context-dependent parasitism. The American Naturalist, 177, 510-521.
71. Van Riper, C. III, Van Riper, S.G., Goff, M.L. & Laird, M. (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs, 56, 327-344.
72. Waldenström, J., Bensch, S., Hasselquist, D. & Ostman, O. (2004) A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Journal of Parasitology, 90, 191-194.
73. Westerdahl, H., Waldenström, J., Hansson, B., Hasselquist, D., von Schantz, T. & Bensch, S. (2005) Associations between malaria and MHC genes in a migratory songbird. Proceedings of the Royal Society. B, Biological Sciences, 272, 1511-1518.
74. Williams, R.B. (2005) Avian malaria: clinical and chemical pathology of Plasmodium gallinaceum in the domesticated fowl Gallus gallus. Avian Pathology, 34, 29-47.
75. Williams, P.D. & Day, T. (2001) Interactions between sources of mortality and the evolution of parasite virulence. Proceedings of the Royal Society of London. Series B, Biological Sciences, 268, 2331-2337.
76. Wolinska, J. & King, K.C. (2009) Environment can alter selection in host-parasite interactions. Trends in Parasitology, 25, 236-244.
77. Wood, M.J., Cosgrove, C.L., Wilkin, T.A., Knowles, S.C.L., Day, K.P. & Sheldon, B.C. (2007) Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Molecular Ecology, 16, 3263-3273.
78. Yourth, C.P. & Schmid-Hempel, P. (2006) Serial passage of the parasite Crithidia bombi within a colony of its host, Bombus terrestris, reduces success in unrelated hosts. Proceedings of the Royal Society. B, Biological Sciences, 273, 655-659.
79. Zehtindjiev, P., Ilieva, M., Westerdahl, H., Hansson, B., Valkiunas, G. & Bensch, S. (2008) Dynamics of parasitaemia of malaria parasites in a naturally and experimentally infected migratory songbirds, the great reed warbler Acrocephalus arundinaceus. Experimental Parasitology, 119, 99-110.