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Evolutionary Ecology

, Volume 26, Issue 1, pp 95–107 | Cite as

The impact of infection on host competition and its relationship to parasite persistence in a Daphnia microparasite system

  • Dominik Refardt
  • Dieter Ebert
Original Paper

Abstract

Evolutionary studies often estimate fitness components with the aim to make predictions about the outcome of selection. Depending on the system and the question, different fitness components are used, but their usefulness for predicting the outcome of selection is rarely tested. Here we estimate host fitness components in different ways with the aim to test how well they agree with each other and how well they predict host fitness at the population level in the presence of the parasite. We use a Daphnia magna-microparasite system to study the competitive ability of host clones in the absence and presence of the parasite, the infection intensity of the parasite in individuals of twelve host clones (an estimate of both host resistance and parasite reproductive success), and parasite persistence in small host populations (an estimate of R 0 of the parasite). Analysis of host competitive ability and parasite persistence reveals strong host genotype effects, while none are found for infection intensity. Host competitive ability further shows a genotype-specific change upon infection, which is correlated with the relative persistence of the parasite in the competing hosts. Hosts in which the parasite persists better suffer a competitive disadvantage in the parasite’s presence. This suggests that in this system, parasite-mediated selection can be predicted by parasite persistence, but not by parasite infection intensity.

Keywords

Competition Fitness components Red Queen Resistance Virulence 

Notes

Acknowledgments

We thank N. Basieux, J. Hottinger, S. Lass and L. Sygnarski for technical assistance, M. Kölliker for statistical advice, and H. K. Alexander for polishing the language. The manuscript benefitted from comments by J. Bull, J. Jokela, C. Kost, S. Lass, M. Zbinden, two anonymous reviewers, and the handling editor. The authors were supported by the Swiss National Science Foundation.

References

  1. Anderson RM, May RM (1981) The population dynamics of microparasites and their invertebrate hosts. Phil Trans R Soc B 291:451–524CrossRefGoogle Scholar
  2. Anderson RM, May RM (1982) Coevolution of hosts and parasites. Parasitology 85:411–426PubMedCrossRefGoogle Scholar
  3. Bull JJ (1994) Virulence. Evolution 48:1423–1437CrossRefGoogle Scholar
  4. Capaul M, Ebert D (2003) Parasite-mediated selection in experimental Daphnia magna populations. Evolution 57:249–260PubMedGoogle Scholar
  5. Carius HJ, Little TJ, Ebert D (2001) Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution 55:1136–1145PubMedGoogle Scholar
  6. Clarke BC (1979) Evolution of genetic diversity. Proc R Soc B 205:453–474CrossRefGoogle Scholar
  7. de Roode JC, Yates AJ, Altizer S (2008) Virulence-transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proc Natl Acad Sci USA 105:7489–7494PubMedCrossRefGoogle Scholar
  8. Decaestecker E, Vergote A, Ebert D, Meester LD (2003) Evidence for strong host clone-parasite species interactions in the Daphnia microparasite system. Evolution 57:784–792PubMedGoogle Scholar
  9. Decaestecker E, Declerck S, Meester LD, Ebert D (2005) Ecological implications of parasites in natural Daphnia populations. Oecologia 144:382–390PubMedCrossRefGoogle Scholar
  10. Dieckmann U (ed) (2002) Adaptive dynamics of infectious disease. Cambridge University Press, CambridgeGoogle Scholar
  11. Duffy MA (2007) Selective predation, parasitism, and trophic cascades in a bluegill–Daphnia–parasite system. Oecologia 153:453–460PubMedCrossRefGoogle Scholar
  12. Duffy MA, Sivars-Becker L (2007) Rapid evolution and ecological host-parasite dynamics. Ecol Lett 10:44–53PubMedCrossRefGoogle Scholar
  13. Duncan AB, Mitchell SE, Little TJ (2006) Parasite-mediated selection and the role of sex and diapause in Daphnia. J Evol Biol 19:1183–1189PubMedCrossRefGoogle Scholar
  14. Ebert D (2005) Ecology, epidemiology, and evolution of parasitism in Daphnia [Internet]. National Library of Medicine (US), National Center for Biotechnology Information, Bethesda, MD. Available from http://www.ncbi.nlm.nih.gov/books/NBK2036. (Accessed Feb 2011)
  15. Ebert D (2008) Host-parasite coevolution: insights from the Daphnia-parasite model system. Curr Opin Microbiol 11:290–301PubMedCrossRefGoogle Scholar
  16. Ebert D, Bull JJ (2003) Challenging the trade-off model for the evolution of virulence: is virulence management feasible? Trends Microbiol 11:15–20PubMedCrossRefGoogle Scholar
  17. Ebert D, Zschokke-Rohringer CD, Carius HJ (1998) Within- and between-population variation for resistance of Daphnia magna to the bacterial endoparasite Pasteuria ramosa. Proc R Soc B 265:2127–2134CrossRefGoogle Scholar
  18. Ebert D, Lipsitch M, Mangin KL (2000) The effect of parasites on host population density and extinction: experimental epidemiology with Daphnia and six microparasites. Am Nat 156:459–477CrossRefGoogle Scholar
  19. Ebert D, Haag C, Kirkpatrick M, Riek M, Hottinger J, Pajunen VI (2002) A selective advantage to immigrant genes in a Daphnia metapopulation. Science 295:485–488PubMedCrossRefGoogle Scholar
  20. Fels D (2005) The effect of food on microparasite transmission in the waterflea Daphnia magna. Oikos 109:360–366CrossRefGoogle Scholar
  21. Fels D, Lee VA, Ebert D (2004) The impact of microparasites on the vertical distribution of Daphnia magna. Arch Hydrobiol 161:65–80CrossRefGoogle Scholar
  22. Frank SA (1996) Models of parasite virulence. Quart Rev Biol 71:37–78PubMedCrossRefGoogle Scholar
  23. Grech K, Watt K, Read AF (2006) Host–parasite interactions for virulence and resistance in a malaria model system. J Evol Biol 19:1620–1630PubMedCrossRefGoogle Scholar
  24. Green J (1974) Parasites and epibionts of Cladocera. Trans Zool Soc Lond 32:417–515CrossRefGoogle Scholar
  25. Haag CR, Ebert D (2004) Parasite-mediated selection in experimental metapopulations of Daphnia magna. Proc R Soc B 271:2149–2155PubMedCrossRefGoogle Scholar
  26. Haag CR, Sakwinska O, Ebert D (2003) Test of synergistic interaction between infection and inbreeding in Daphnia magna. Evolution 57:777–783PubMedGoogle Scholar
  27. Hamilton WD (1980) Sex versus non-sex versus parasite. Oikos 35:282–290CrossRefGoogle Scholar
  28. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387PubMedCrossRefGoogle Scholar
  29. Hartl DL (1987) A primer of population genetics. Sinauer, SunderlandGoogle Scholar
  30. Hochberg ME (1998) Establishing genetic correlations involving parasite virulence. Evolution 52:1865–1868CrossRefGoogle Scholar
  31. Jensen KH, Little TJ, Skorping A, Ebert D (2006) Empirical support for optimal virulence in a castrating parasite. PLoS Biol 4:e197PubMedCrossRefGoogle Scholar
  32. Jungen H, Hartl DL (1979) Average fitness of populations of Drospohila melanogaster as estimated using compound-autosome strains. Evolution 33:359–370CrossRefGoogle Scholar
  33. Larsson JIR, Ebert D, Vávra J, Voronin VN (1996) Redescription of Pleistophora intestinalis Chatton, 1907, a microsporidian parasite of Daphnia magna and Daphnia pulex, with establisment of the new genus Glugoides (Microspora, Glugeidae). Europ J Protistol 32:251–261CrossRefGoogle Scholar
  34. Little TJ, Carius HJ, Sakwinska O, Ebert D (2002) Competitiveness and life-history characteristics of Daphnia with respect to susceptibility to a bacterial pathogen. J Evol Biol 15:796–802CrossRefGoogle Scholar
  35. Mackinnon MJ, Read AF (1999) Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution 53:689–703CrossRefGoogle Scholar
  36. May RM, Anderson RM (1983) Epidemiology and genetics in the coevolution of parasites and hosts. Proc R Soc B 219:281–313CrossRefGoogle Scholar
  37. Mitchell SE, Read AF, Little TJ (2004) The effect of a pathogen epidemic on the genetic structure and reproductive strategy of the crustacean Daphnia magna. Ecol Lett 7:848–858CrossRefGoogle Scholar
  38. Packer C, Holt RD, Hudson PJ, Lafferty KD, Dobson AP (2003) Keeping the herds healthy and alert: Implications of predator control for infectious disease. Ecol Lett 6:797–802CrossRefGoogle Scholar
  39. Refardt D, Ebert D (2006) Quantitative PCR to detect, discriminate and quantify intracellular parasites in their host: an example from three microsporidians in Daphnia. Parasitology 133:11–18PubMedCrossRefGoogle Scholar
  40. Refardt D, Ebert D (2007) Inference of parasite local adaptation using two different fitness components. J Evol Biol 20:921–929PubMedCrossRefGoogle Scholar
  41. Refardt D, Canning EU, Mathis A, Cheney SA, Lafranchi-Tristem NJ, Ebert D (2002) Small subunit ribosomal DNA phylogeny of microsporidia that infect Daphnia (Crustacea: Cladocera). Parasitology 124:381–389PubMedCrossRefGoogle Scholar
  42. Rigby MC, Hechinger RF, Stevens L (2002) Why should parasite resistance be costly? Trends Parasitol 18:116–120PubMedCrossRefGoogle Scholar
  43. Rolff J, Joop G (2002) Estimating condition: pitfalls of using weight as a fitness correlate. Evol Ecol Res 4:931–935Google Scholar
  44. Roy BA, Kirchner JW (2000) Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54:51–63PubMedGoogle Scholar
  45. SAS Institute Inc (1989) JMP, Version 8. SAS Institute Inc., CaryGoogle Scholar
  46. Schmid-Hempel P, Ebert D (2003) On the evolutionary ecology of specific immune defence. Trends Ecol Evol 18:27–32CrossRefGoogle Scholar
  47. Schwarzenbach GA, Ward PI (2006) Responses to selection on phenoloxidase activity in yellow dung flies. Evolution 60:1612–1621PubMedGoogle Scholar
  48. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  49. Stirnadel HA, Ebert D (1997) Prevalence, host specificity and impact on host fecundity of microparasites and epibionts in three sympatric Daphnia species. J Anim Ecol 66:212–222CrossRefGoogle Scholar
  50. Thompson JN (1994) The coevolutionary process. University of Chicago Press, ChicagoGoogle Scholar
  51. Tompkins DM, Begon M (1999) Parasites can regulate wildlife populations. Parasitol Today 15:311–313PubMedCrossRefGoogle Scholar
  52. Vijendravarma RK, Kraaijeveld AR, Godfray HCJ (2009) Experimental evolution shows Drosophila melanogaster resistance to a microsporidian pathogen has fitness costs. Evolution 63:104–114PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Département de Biologie, Unitè Ecologie and EvolutionUniversité de FribourgFribourgSwitzerland
  2. 2.Institut für Integrative BiologieETH ZürichZürichSwitzerland
  3. 3.Zoologisches InstitutUniversität BaselBaselSwitzerland

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