Diet quality determines interspecific parasite interactions in host populations

Ecology and Evolution

Volumn 4, Issue 15, 2014, Pages 3093-3102

  Lange, Benjamin ^a   Reuter, Max ^b   Ebert, Dieter ^c   Muylaert, Koenraad ^a   Decaestecker, Ellen ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Daphnia magna; Disease dynamics; Food quality; Host population demography; Interspecific parasite competition; Multispecies infections; Parasite ecology; Unicellular gut parasite; White bacterial disease

Indexed keywords

BACTERIA (MICROORGANISMS); CRUSTACEA; DAPHNIA; DAPHNIA MAGNA; MICROSPORIDIUM;

EID: 84925834333     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.1167     Document Type: Article

References (97)

1. Aalto, S. L., T. Ketola, and K. Pulkkinen. 2014. No uniform associations between parasite prevalence and environmental nutrients. Ecology (http://www.esajournals.org/doi/abs/10.1890/13-2007.1).
2. Alizon, S., J. C. de Roode, and Y. Michalakis. 2013. Multiple infections and the evolution of virulence. Ecol. Lett. 16:556-567.
3. Anderson, T. R., M. Boersma, and D. Raubenheimer. 2004. Stoichiometry: linking elements to biochemicals. Ecology 85:1193-1202.
4. Arendt, K., S. Jónasdóttir, P. Hansen, and S. Gärtner. 2005. Effects of dietary fatty acids on the reproductive success of the calanoid copepod Temora longicornis. Mar. Biol. 146:513-530.
5. Balmer, O., S. C. Stearns, A. Schotzau, and R. Brun. 2009. Intraspecific competition between co-infecting parasite strains enhances host survival in African trypanosomes. Ecology 90:3367-3378.
6. Basen, T., D. Martin-Creuzburg, and K.-O. Rothhaupt. 2011. Role of essential lipids in determining food quality for the invasive freshwater clam Corbicula fluminea. J. North. Am. Benthol. Soc. 30:653-664.
7. Bell, A. S., J. C. De Roode, D. Sim, and A. F. Read. 2006. Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution 60:1358-1371.
8. Bird, M. I., C. M. Wurster, P. H. de Paula Silva, A. M. Bass, and R. de Nys. 2011. Algal biochar - production and properties. Bioresour. Technol. 102:1886-1891.
9. Bukovinszky, T., E. H. Poelman, R. Gols, G. Prekatsakis, L. E. M. Vet, J. A. Harvey, et al. 2009. Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism. Oecologia 160:299-308.
10. Burdon, J. J., and P. H. Thrall. 2009. Co-evolution of plants and their pathogens in natural habitats. Science 324:755-756.
11. Bush, S. E., and J. R. Malenke. 2008. Host defence mediates interspecific competition in ectoparasites. J. Anim. Ecol. 77:558-564.
12. Chadwick, W., and T. J. Little. 2005. A parasite-mediated life-history shift in Daphnia magna. Proc. Biol. Sci. 272:505-509.
13. Choisy, M., and J. C. de Roode. 2010. Mixed infections and the evolution of virulence: effects of resource competition, parasite plasticity, and impaired host immunity. Am. Nat. 175:E105-E118.
14. Civitello, D. J., R. M. Penczykowski, J. L. Hite, M. A. Duffy, and S. R. Hall. 2013. Potassium stimulates fungal epidemics in Daphnia by increasing host and parasite reproduction. Ecology 94:380-388.
15. Coopman, M., K. Muylaert, B. Lange, L. Reyserhove, and E. Decaestecker. 2014. Context dependency of infectious disease: the cyanobacterium Microcystis aeruginosa decreases white bacterial disease in Daphnia magna. Freshw. Biol. 59:714-723.
16. Dallas, T., and J. M. Drake. 2014. Nitrate enrichment alters a Daphnia-microparasite interaction through multiple pathways. Ecol. Evol. 4:243-250.
17. Decaestecker, E., A. Vergote, D. Ebert, and L. De Meester. 2003. Evidence for strong host clone-parasite species interactions in the Daphnia microparasite system. Evolution 57:784-792.
18. Decaestecker, E., S. Declerck, L. De Meester, and D. Ebert. 2005. Ecological implications of parasites in natural Daphnia populations. Oecologia 144:382-390.
19. Dieckmann, U. 2002. Adaptive dynamics of pathogen-host interactions. Adaptive dynamics of infectious diseases. Pp. 39-59 in U. Dieckmann, J. A. J. Metz, M. W. Sabelis and K. Sigmund, eds. Pursuit of virulence management, 1st ed. Cambridge Univ. Press, Cambridge, U.K.
20. Dobson, A. P. 1985. The population dynamics of competition between parasites. Parasitology 91:317-347.
21. Dobson, A., K. D. Lafferty, A. M. Kuris, R. F. Hechinger, and W. Jetz. 2008. Homage to Linnaeus: how many parasites? How many hosts? Proc. Natl Acad. Sci. 105:11482-11489.
22. Duffy, M. A., C. E. Cáceres, S. R. Hall, A. J. Tessier, and A. R. Ives. 2010. Temporal, spatial, and between-host comparisons of patterns of parasitism in lake zooplankton. Ecology 91:3322-3331.
23. Dunn, R. R. 2005. Modern insect extinctions, the neglected majority. Conserv. Biol. 19:1030-1036.
24. Dunn, A. M., M. E. Torchin, M. J. Hatcher, P. M. Kotanen, D. M. Blumenthal, J. E. Byers, et al. 2012. Indirect effects of parasites in invasions. Funct. Ecol. 26:1262-1274.
25. Ebert, D. 1998. Experimental evolution of parasites. Science 282:1432-1435.
26. Ebert, D. 2005. Ecology, epidemiology, and evolution of parasitism in Daphnia [Internet]. National Library of Medicine (US), National Center for Biotechnology Information, Bethesda, MD. See http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=Books.
27. Ebert, D., M. Lipsitch, and K. L. Mangin. 2000. The effect of parasites on host population density and extinction: experimental epidemiology with Daphnia and six microparasites. Am. Nat. 156:459-477.
28. Elser, J. J., R. W. Sterner, E. Gorokhova, W. F. Fagan, T. A. Markow, J. B. Cotner, et al. 2000. Biological stoichiometry from genes to ecosystems. Ecol. Lett. 3:540-550.
29. Fellous, S., and J. C. Koella. 2009. Infectious dose affects the outcome of the within-host competition between parasites. Am. Nat. 173:E177-E184.
30. Forde, S. E., J. N. Thompson, and B. J. M. Bohannan. 2004. Adaptation varies through space and time in a coevolving host-parasitoid interaction. Nature 431:841-844.
31. Frost, P. C., D. Ebert, and V. H. Smith. 2008. Responses of a bacterial pathogen to phosphorus limitation of its aquatic invertebrate host. Ecology 89:313-318.
32. Garbutt, J. S., J. A. Scholefied, P. F. Vale, and T. J. Little. 2014. Funct. Ecol. 28:424-431.
33. Gower, C. M., and J. P. Webster. 2005. Intraspecific competition and the evolution of virulence in a parasitic trematode. Evolution 59:544-553.
34. Graham, A. L. 2008. Ecological rules governing helminth-microparasite coinfection. Proc. Natl Acad. Sci. USA 105:566-570.
35. Griffiths, E. C., A. B. Pedersen, A. Fenton, and O. L. Petchey. 2014. Analysis of a summary network of co-infection in humans reveals that parasites interact most via shared resources. Proc. Biol. Sci. 281:20132286.
36. Guillard, R. R. L. 1975. Culture of marine invertebrate animals. Plenum Press, New York, NY.
37. Hall, S. R., C. J. Knight, C. R. Becker, M. A. Duffy, A. J. Tessier, and C. E. Cáceres. 2009. Quality matters: resource quality for hosts and the timing of epidemics. Ecol. Lett. 12:118-128.
38. Hall, M. D., A. Vettiger, and D. Ebert. 2013. Interactions between environmental stressors: the influence of salinity on host-parasite interactions between Daphnia magna and Pasteuria ramosa. Oecologia 171:789-796.
39. Harrison, F., J. Paul, R. C. Massey, and A. Buckling. 2008. Interspecific competition and siderophore-mediated cooperation in Pseudomonas aeruginosa. ISME J. 2:49-55.
40. Hibbing, M. E., C. Fuqua, M. R. Parsek, and S. B. Peterson. 2010. Bacterial competition: surviving and thriving in the microbial jungle. Nat. Rev. Microbiol. 8:15-25.
41. Holdo, R. M., A. R. E. Sinclair, A. P. Dobson, K. L. Metzger, B. M. Bolker, M. E. Ritchie, et al. 2009. A Disease-mediated trophic cascade in the serengeti and its implications for ecosystem C. PLoS Biol. 7:e1000210.
42. Hoverman, J. T., B. J. Hoye, and P. T. J. Johnson. 2013. Does timing matter? How priority effects influence the outcome of parasite interactions within hosts. Oecologia 4:1471-1480.
43. Hudson, P. J., A. P. Dobson, and K. D. Lafferty. 2006. Is a healthy ecosystem one that is rich in parasites? Trends Ecol. Evol. 21:381-385.
44. Hughes, W. O. H., and J. J. Boomsma. 2004. Let your enemy do the work: within-host interactions between two fungal parasites of leaf-cutting ants. Proc. Biol. Sci. 271:S104-S106.
45. Jansen, M., R. Stoks, E. Decaestecker, A. Coors, F. Van De Meutter, and L. De Meester. 2010. Local exposure shapes spatial patterns in infectivity and community structure of Daphnia parasites. J. Anim. Ecol. 79:1023-1033.
46. Johnson, P. T. J., and I. D. Buller. 2011. Parasite competition hidden by correlated coinfection: using surveys and experiments to understand parasite interactions. Ecology 92:535-541.
47. Johnson, P. T. J., and D. W. Thieltges. 2010. Diversity, decoys and the dilution effect: how ecological communities affect disease risk. J. Exp. Biol. 213:961-970.
48. Karvonen, A., P. Rintamäki, J. Jokela, and E. T. Valtonen. 2010. Increasing water temperature and disease risks in aquatic systems: climate change increases the risk of some, but not all, diseases. Int. J. Parasitol. 40:1483-1488.
49. Klüttgen, B., U. Dülmer, M. Engels, and H. T. Ratte. 1994. ADaM, an artificial freshwater for the culture of zooplankton. Water Res. 28:743-746.
50. Lafferty, K. D., A. P. Dobson, and A. M. Kuris. 2006. Parasites dominate food web links. Proc. Natl Acad. Sci. USA 103:11211-11216.
51. Laine, A.-L., and A. Tellier. 2008. Heterogeneous selection promotes maintenance of polymorphism in host-parasite interactions. Oikos 117:1281-1288.
52. Lello, J., B. Boag, A. Fenton, I. R. Stevenson, and P. J. Hudson. 2004. Competition and mutualism among the gut helminths of a mammalian host. Nature 428:840-844.
53. Lochmiller, R. L., and C. Deerenberg. 2000. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87-98.
54. Lohr, J. N., M. Yin, and J. Wolinska. 2010. Prior residency does not always pay off co-infections in Daphnia. Parasitology 137:1493-1500.
55. Malenke, J. R., N. Newbold, and D. H. Clayton. 2011. Condition-specific competition governs the geographic distribution and diversity of ectoparasites. Am. Nat. 177:522-534.
56. Martin-Creuzburg, D., and E. Von Elert. 2009. Good food versus bad food: the role of sterols and polyunsaturated fatty acids in determining growth and reproduction of Daphnia magna. Aquat. Ecol. 43:943-950.
57. McKenzie, V. J., and A. R. Townsend. 2007. Parasitic and infectious disease responses to changing global nutrient cycles. EcoHealth 4:384-396.
58. McVean, R. I. K., S. M. Sait, D. J. Thompson, and M. Begon. 2002. Effects of resource quality on the population dynamics of the Indian meal moth Plodia interpunctella and its granulovirus. Oecologia 131:71-78.
59. Mercereau-Puijalon, O. 1996. Revisiting host/parasite interactions: molecular analysis of parasites collected during longitudinal and cross-sectional surveys in humans. Parasite Immunol. 18:173-180.
60. Mideo, N. 2009. Parasite adaptations to within-host competition. Trends Parasitol. 25:261-268.
61. Mitchell, S. E., E. S. Rogers, T. J. Little, and A. F. Read. 2005. Host-parasite and genotype-by-environment interactions: temperature modifies potential for selection by a sterilizing pathogen. Evolution 59:70-80.
62. Nunn, C. L., S. M. Altizer, W. Sechrest, and A. A. Cunningham. 2005. Latitudinal gradients of parasite species richness in primates. Divers. Distrib. 11:249-256.
63. Pajk, F., E. Von Elert, and P. Fink. 2012. Interaction of changes in food quality and temperature reveals maternal effects on fitness parameters of a keystone aquatic herbivore. Limnol. Oceanogr. 57:281-292.
64. Parker, B. J., S. M. Barribeau, A. M. Laughton, J. C. de Roode, and N. M. Gerardo. 2011. Non-immunological defense in an evolutionary framework. Trends Ecol. Evol. 26:242-248.
65. Pech, D., M. L. Aguirre-Macedo, J. W. Lewis, and V. M. Vidal-Martínez. 2010. Rainfall induces time-lagged changes in the proportion of tropical aquatic hosts infected with metazoan parasites. Int. J. Parasitol. 40:937-944.
66. Pedersen, A. B., and A. Fenton. 2007. Emphasizing the ecology in parasite community ecology. Trends Ecol. Evol. 22:133-139.
67. Poulin, R. 2007. Evolutionary ecology of parasites, 2nd ed. Princeton Univ. Press, Princeton, NJ.
68. R Development Core Team. 2009. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
69. Ranta, E., J. Bengtsson, and J. McManus. 1993. Growth, size and shape of Daphnia longispina, Daphnia magna and Daphnia pulex. Ann. Zool. Fenn. 30:299-311.
70. Read, A. F., and L. H. Taylor. 2001. The ecology of genetically diverse infections. Science 292:1099-1102.
71. Refardt, D., and D. Ebert. 2007. Inference of parasite local adaptation using two different fitness components. J. Evol. Biol. 20:921-929.
72. Refardt, D., and D. Ebert. 2012. The impact of infection on host competition and its relationship to parasite persistence in a Daphnia microparasite system. Evol. Ecol. 26:95-107.
73. Rigaud, T., M.-J. Perrot-Minnot, and M. J. F. Brown. 2010. Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence. Proc. Biol. Sci. 277:3693-3702.
74. Rohde, K., and M. Heap. 1998. Latitudinal differences in species and community richness and in community structure of metazoan endo- and ectoparasites of marine teleost fish. Int. J. Parasitol. 28:461-474.
75. de Roode, J. C., R. Culleton, S. J. Cheesman, R. Carter, and A. F. Read. 2004. Host heterogeneity is a determinant of competitive exclusion or coexistence in genetically diverse malaria infections. Proc. Biol. Sci. 271:1073-1080.
76. de Roode, J. C., M. E. H. Helinski, M. A. Anwar, and A. F. Read. 2005. Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. Am. Nat. 166:531-542.
77. Sarfraz, M., L. M. Dosdall, and B. A. Keddie. 2009. Host plant nutritional quality affects the performance of the parasitoid Diadegma insulare. Biol. Control 51:34-41.
78. Sato, T., T. Egusa, K. Fukushima, T. Oda, N. Ohte, N. Tokuchi, et al. 2012. Nematomorph parasites indirectly alter the food web and ecosystem function of streams through behavioural manipulation of their cricket hosts. Ecol. Lett. 15:786-793.
79. Schlotz, N., D. Ebert, and D. Martin-Creuzburg. 2013. Dietary supply with polyunsaturated fatty acids and resulting maternal effects influence host-parasite interactions. BMC Ecol. 13:41.
80. Schmid-Hempel, P. 2011. Evolutionary parasitology: the integrated study of infections, immunology, ecology, and genetics. Oxford Univ. Press, Oxford, U.K.
81. Schmid-Hempel, P., and D. Ebert. 2003. On the evolutionary ecology of specific immune defence. Trends Ecol. Evol. 18:27-32.
82. Seppälä, O., K. Liljeroos, A. Karvonen, and J. Jokela. 2008. Host condition as a constraint for parasite reproduction. Oikos 117:749-753.
83. Smith, T., I. Felger, M. Tanner, and H.-P. Beck. 1999. Premunition in Plasmodium falciparum infection: insights from the epidemiology of multiple infections. Trans. R. Soc. Trop. Med. Hyg. 93:S1/59-S1/64.
84. Taipale, S. J., M. J. Kainz, and M. T. Brett. 2011. Diet-switching experiments show rapid accumulation and preferential retention of highly unsaturated fatty acids in Daphnia. Oikos 120:1674-1682.
85. Telfer, S., R. Birtles, M. Bennett, X. Lambin, S. Paterson, and M. Begon. 2008. Parasite interactions in natural populations: insights from longitudinal data. Parasitology 135:767-781.
86. Telfer, S., X. Lambin, R. Birtles, P. Beldomenico, S. Burthe, S. Paterson, et al. 2010. Species interactions in a parasite community drive infection risk in a wildlife population. Science 330:243-246.
87. Thomas, M. B., E. L. Watson, and P. Valverde-Garcia. 2003. Mixed infections and insect-pathogen interactions. Ecol. Lett. 6:183-188.
88. Thumbi, S. M., B. M. de C Bronsvoort, E. J. Poole, H. Kiara, P. Toye, M. Ndila, et al. 2013. Parasite co-infections show synergistic and antagonistic interactions on growth performance of East African zebu cattle under one year. Parasitology 140:1789-1798.
89. Vale, P. F., A. J. Wilson, A. Best, M. Boots, and T. J. Little. 2011. Epidemiological, evolutionary and co-evolutionary implications of context-dependent parasitism. Am. Nat. 177:510-521.
90. Van De Bund, W. J., and E. Van Donk. 2002. Impact of 'white bacterial disease' on a Daphnia magna population. Verhandlungen der Internationalen Vereinigung Limnologie 28:303-306.
91. Wacker, A., and D. Martin-Creuzburg. 2007. Allocation of essential lipids in Daphnia magna during exposure to poor food quality. Funct. Ecol. 21:738-747.
92. Wargo, A. R., J. C. de Roode, S. Huijben, D. R. Drew, and A. F. Read. 2007. Transmission stage investment of malaria parasites in response to in-host competition. Proc. Biol. Sci. 274:2629-2638.
93. Weers, P. M. M., and R. D. Gulati. 1997. Effect of the addition of polyunsaturated fatty acids to the diet on the growth and fecundity of Daphnia galeata. Freshw. Biol. 38:721-729.
94. Wiehn, J., and E. Korpimäki. 1998. Resource levels, reproduction and resistance to haematozoan infections. Proc. Biol. Sci. 265:1197-1201.
95. Wolinska, J., and K. C. King. 2009. Environment can alter selection in host-parasite interactions. Trends Parasitol. 25:236-244.
96. Wolinska, J., S. Giessler, and H. Koerner. 2009. Molecular identification and hidden diversity of novel Daphnia parasites from European lakes. Appl. Environ. Microbiol. 75:7051-7059.
97. Woolhouse, M. E. J., and S. Gowtage-Sequeria. 2005. Host range and emerging and reemerging pathogens. Emerg. Infect. Dis. 11:1842-1847.