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Parasite variation and the evolution of virulence in a Daphnia-microparasite system

Published online by Cambridge University Press:  16 November 2007

T. J. LITTLE ,
W. CHADWICK  and
K. WATT
T. J. LITTLE*
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Kings Buildings, West Mains Road, EdinburghEH9 3JT, UK
W. CHADWICK
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Kings Buildings, West Mains Road, EdinburghEH9 3JT, UK
K. WATT
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Kings Buildings, West Mains Road, EdinburghEH9 3JT, UK
*
*Corresponding author. Tel: +0131 650 7781. Fax: +0131 650 6564. E-mail: [email protected]
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Summary

Understanding genetic relationships amongst the life-history traits of parasites is crucial for testing hypotheses on the evolution of virulence. This study therefore examined variation between parasite isolates (the bacterium Pasteuria ramosa) from the crustacean Daphnia magna. From a single wild-caught infected host we obtained 2 P. ramosa isolates that differed substantially in the mortality they caused. Surprisingly, the isolate causing higher early mortality was, on average, less successful at establishing infections and had a slower growth rate within hosts. The observation that within-host replication rate was negatively correlated with mortality could violate a central assumption of the trade-off hypothesis for the evolution of virulence, but we discuss a number of caveats which caution against premature rejection of the trade-off hypothesis. We sought to test if the characteristics of these parasite isolates were constant across host genotypes in a second experiment that included 2 Daphnia host clones. The relative growth rates of the two parasite isolates did indeed depend on the host genotype (although the rank order did not change). We suggest that testing evolutionary hypotheses for virulence may require substantial sampling of both host and parasite genetic variation, and discuss how selection for virulence may change with the epidemiological state of natural populations and how this can promote genetic variation for virulence.

Keywords

natural selectionco-evolutiontrade-offgenetic variationpathogenparasitespecificityPasteuria
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 3 , March 2008 , pp. 303 - 308
Copyright
Copyright © Cambridge University Press 2007

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References

Almogy, G., Cohen, N., Stocker, S. and Stone, L. (2002). Immune response and virus population composition: HIV as a case study. Proceedings of the Royal Society of London, B 269, 809–815.CrossRefGoogle ScholarPubMed
Andre, J. B., Ferdy, J. B. and Godelle, B. (2003). Within-host parasite dynamics, emerging trade-off, and evolution of virulence with immune system. Evolution 57, 1489–1497.Google ScholarPubMed
Bremermann, H. J. and Pickering, J. (1983). A game-theoretical model of parasite virulence. Journal of Theoretical Biology 100, 411–426.CrossRefGoogle ScholarPubMed
Bull, J. J. (1994). Virulence. Evolution 48, 1423–1437.Google ScholarPubMed
Carius, H.-J., Little, T. J. and Ebert, D. (2001). Genetic variation in a host–parasite association: Potential for coevolution and frequency dependent selection. Evolution 55, 1136–1145.Google Scholar
Choo, K., Williams, P. D. and Day, T. (2003). Host mortality, predation and the evolution of parasite virulence. Ecology Letters 6, 310–315.CrossRefGoogle Scholar
Day, T. and Proulx, S. R. (2004). A general theory for the evolutionary dynamics of virulence. American Naturalist 163, E40–.E63CrossRefGoogle ScholarPubMed
De Roode, J. C., Pansini, R., Cheesman, S. J., Helinski, M. E. H., Huijben, S., Wargo, A. R., Bell, A. S., Chan, B. H. K., Walliker, D. and Read, A. F. (2005). Virulence and competitive ability in genetically diverse malaria infections. Proceedings of the National Academy of Sciences, USA 102, 7624–7628.CrossRefGoogle ScholarPubMed
Duncan, A., Mitchell, S. E. and Little, T. J. (2006). Parasite-mediated selection in Daphnia: the role of sex and diapause. The Journal of Evolutionary Biology 19, 1183–1189.CrossRefGoogle ScholarPubMed
Duncan, A. B. and Little, T. J. (2007). Parasite-driven genetic change in a natural population of Daphnia magna. Evolution 64, 796–803.CrossRefGoogle Scholar
Dye, C. and Davies, C. R. (1990). Glasnost and the great gerbil: virulence polymorphisms in the epidemiology of leishmaniasis. Trends in Ecology and Evolution 5, 237–238.CrossRefGoogle Scholar
Ebert, D. (1998). Experimental evolution of parasites. Science 282, 1432–1435.CrossRefGoogle ScholarPubMed
Ebert, D., Carius, H.-J., Little, T. J. and Decaestecker, E. (2004). The evolution of virulence when parasites cause host castration and gigantism. American Naturalist 164, s19–s32.CrossRefGoogle ScholarPubMed
Ebert, D., Rainey, P., Embley, T. M. and Scholz, D. (1996). Development, life cycle, ultrastructure and phylogenetic position of Pasteuria ramosa Metchnikoff 1888: rediscovery of an obligate endoparasite of Daphnia magna Straus. Philosophical Transactions of the Royal Society of London, B 351, 1689–1701.Google Scholar
Escriu, F., Fraile, A. and García-Arenal, F. (2003). The evolution of virulence in a plant virus. Evolution 57, 755–765.Google Scholar
Frank, S. A. (1996). Models of parasite virulence. Quarterly Review of Biology 71, 37–78.CrossRefGoogle ScholarPubMed
Gandon, S., Mackinnon, M. J., Nee, S. and Read, A. F. (2001). Imperfect vaccines and the evolution of pathogen virulence. Nature, London 414, 751–755.CrossRefGoogle ScholarPubMed
Grech, K., Watt, K. and Read, A. F. (2006). Host-parasite interactions for virulence and resistance in a malaria model system. Journal of Evolutionary Biology 19, 1620–1630.CrossRefGoogle Scholar
Herre, E. A. (1995). Factors affecting the evolution of virulence: nematode parasites of fig wasps as a case study. Parasitology 111 (Suppl.), S179–S191.CrossRefGoogle Scholar
Jensen, K. N., Little, T. J., Skorping, A. and Ebert, D. (2006). Empirical support for an optimal virulence in a castrating parasite. Plos Biology 4, e197. doi: 10.1371/journal.pbio.0040197.CrossRefGoogle Scholar
Lefebvre, T., Sanchez, M., Ponton, F., Hughes, D. and Thomas, F. (2007). Virulence and resistance in malaria: who drives the outcome of infection. Trends in Parasitology 23, 299–302.Google Scholar
Lipsitch, M. and Moxon, E. R. (1997). Virulence and transmissibility of pathogens: What is the relationship? Trends in Microbiology 5, 31–37.CrossRefGoogle ScholarPubMed
Little, T. J. and Ebert, D. (2000). The cause of parasitic infection in natural populations of Daphnia: the role of host genetics. Proceedings of the Royal Society of London, B 267, 2037–2042.CrossRefGoogle ScholarPubMed
Little, T. J. and Killick, S. C. (2007). Evidence for a cost of immunity when the crustacean Daphnia magna is exposed to the bacterial pathogen Pasteuria ramosa. Journal of Animal Ecology 76, 1202–1207.CrossRefGoogle Scholar
Little, T. J., Watt, K. and Ebert, D. (2006). Parasite-host specificity: experimental studies on the basis of parasite adaptation. Evolution 60, 31–38.Google ScholarPubMed
Mackinnon, M. J. and Read, A. F. (1999). Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution 53, 689–703.CrossRefGoogle ScholarPubMed
May, R. M. and Anderson, R. M. (1983). Epidemiology and genetics in the coevolution of parasites and hosts. Proceedings of the Royal Society of London, B 219, 281–313.Google ScholarPubMed
Pagan, I. (2007). The relationship of within-host multiplication and virulence in a plant-virus system. PLoS ONE 2, e786. doi: 10.1371/journal.pone.000786.CrossRefGoogle Scholar
Read, A. F. and Taylor, L. H. (2001). The ecology of genetically diverse infections. Science 292, 1099–1102.Google Scholar
Sacristán, S., Fraile, A., , MALPICA, , J. M. and García-Arenal, F. (2005). An analysis of host adaptation and its relationship with virulence in cucumber mosaic virus. Phytopathology 95, 827–833.CrossRefGoogle ScholarPubMed
Sas Institute Inc (2002). SAS, Version 9.0. SAS Institute Inc., Cary, NC, USA.Google Scholar
Stewart, A. D., Logsdon, J. M. and Kelley, S. E. (2005). An empirical study of the evolution of virulence under both horizontal and vertical transmission. Evolution 59, 730–739.Google ScholarPubMed
Weiss, R. A. (2002). Virulence and pathogenesis. Trends in Microbiology 10, 314–317.CrossRefGoogle ScholarPubMed