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Prior residency does not always pay off – co-infections in Daphnia

Published online by Cambridge University Press:  06 May 2010

JENNIFER N. LOHR ,
MINGBO YIN  and
JUSTYNA WOLINSKA
JENNIFER N. LOHR*
Affiliation:
Ludwig-Maximilians-Universität München, Department Biologie II, Evolutionsökologie, Großhaderner Strasse 2, D-82152Planegg-Martinsried, Germany
MINGBO YIN
Affiliation:
Ludwig-Maximilians-Universität München, Department Biologie II, Evolutionsökologie, Großhaderner Strasse 2, D-82152Planegg-Martinsried, Germany
JUSTYNA WOLINSKA
Affiliation:
Ludwig-Maximilians-Universität München, Department Biologie II, Evolutionsökologie, Großhaderner Strasse 2, D-82152Planegg-Martinsried, Germany
*
*Corresponding author, present address: University of Fribourg, Department of Biology, Unit of Ecology and Evolution, Chemin du Musée 10, CH-1700Fribourg, Switzerland. Tel: +41 (0) 26 300 88 57. Fax: +41 (0) 26 300 96 98. E-mail: [email protected]
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Summary

The epidemiological and ecological processes which govern the success of multiple-species co-infections are as yet unresolved. Here we investigated prior versus late residency within hosts, meaning which parasite contacts the host first, to determine if the outcomes of intra-host competition are altered. We infected a single genotype of the waterflea Daphnia galeata with both the intestinal protozoan Caullerya mesnili and the haemolymph fungus Metschnikowia sp. (single genotype of each parasite species), as single infections, simultaneous co-infections and as sequential co-infections, with each parasite given 4 days prior residency. Simultaneous co-infections were significantly more virulent than both single infections and sequential co-infections, as measured by a decreased host life span and fecundity. Further, in addition to the Daphnia host, the parasites also suffered fitness decreases in simultaneous co-infections, as measured by spore production. The sequential co-infections, however, had mixed effects: C. mesnili benefited from prior residency, whereas Metschnikowia sp. experienced a decline in fitness. Our results show that multiple-species co-infections of Daphnia may be more virulent than single infections, and that prior residency does not always provide a competitive advantage.

Keywords

co-infectionmultiple infectionwithin-host competitionDaphniaCaullerya mesniliMetschnikowia sp
Type
Research Article
Information
Parasitology , Volume 137 , Issue 10 , September 2010 , pp. 1493 - 1500
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Ampel, N. M. (1996). Emerging disease issues and fungal pathogens associated with HIV infection. Emerging Infectious Diseases 2, 109–116.CrossRefGoogle ScholarPubMed
Anderson, R. M. and May, R. M. (1982). Coevolution of hosts and parasites. Parasitology 85, 411–426.CrossRefGoogle ScholarPubMed
Ben-Ami, F., Mouton, L. and Ebert, D. (2008). The effects of multiple infections on the expression and evolution of virulence in a Daphnia-endoparasite system. Evolution 62, 1700–1711.CrossRefGoogle Scholar
Bittner, K., Rothaupt, K.-O. and Ebert, D. (2002). Ecological interactions of the microparasite Caullerya mesnili on its host Daphnia galeata. Limnology and Oceanography 4, 300–305.CrossRefGoogle Scholar
Brown, S. P., Inglis, R. F. and Taddei, F. (2009). Evolutionary ecology of microbial wars: within-host competition and (incidental) virulence. Evolutionary Applications 2, 32–39.CrossRefGoogle ScholarPubMed
Carius, H. J., Little, T. J. and Dieter, E. (2001). Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution 55, 1136–1145.Google Scholar
Chatton, E. (1907). Caullerya mesnili n. g. n. sp. Haplosporidie parasite des Daphnies. Société du Biologie 62, 529–531.Google Scholar
Codreanu, R. and Codreanu-Balcescu, D. (1981), On two Metschnikowia yeast species producing hemocoelic infections in Daphnia magna and Artemia salina (Crustacea, Phyllopoda) from Romania. Journal of Invertebrate Pathology 37, 22–27.CrossRefGoogle Scholar
Craig, B. H., Tempest, L. J., Pilkington, J. G. and Pemberton, J. M. (2008). Metazoan-protozoan parasite co-infections and host body weight in St Kilda Soay sheep. Parasitology 135, 433–441.CrossRefGoogle ScholarPubMed
Decaestecker, E., Declerck, S., De Meester, L. and Ebert, D. (2005). Ecological implications of parasites in natural Daphnia populations. Oecologia 144, 382–390.CrossRefGoogle ScholarPubMed
de Roode, J. C., Helinski, M. H., Anwar, M. A. and Read, A. F. (2005). Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. The American Naturalist 166, 531–542.CrossRefGoogle ScholarPubMed
Duffy, M. A. and Sivars-Becker, L. (2007). Rapid evolution and ecological host-parasite dynamics. Ecology Letters 10, 44–53.CrossRefGoogle ScholarPubMed
Duffy, M. A. and Hall, S. R. (2008). Selective predation and rapid evolution can jointly dampen effects of virulent parasites on Daphnia populations. The American Naturalist 171, 499–510.CrossRefGoogle ScholarPubMed
Ebert, D. (2005). Ecology, Epidemiology, and Evolution of Parasitism in Daphnia [Internet]. Bethesda (MD): National Library of Medicine (US), National Center for Biotechnology Information. Available from: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=Books.Google Scholar
Ebert, D., Zschokke-Rohringer, C. D. and Carius, H. J. (2000). Dose effects and density-dependent regulation of two microparasites of Daphnia magna. Oecologia 122, 200–209.CrossRefGoogle ScholarPubMed
Esch, G. W. and Fernandez, J. C. (1994). Snail-trematode interactions and parasite community dynamics in aquatic systems: a review. The American Midland Naturalist 131, 209–237.CrossRefGoogle Scholar
Escribano, A., Williams, T., Goulson, D., Cave, R. D., Chapman, J. W. and Caballero, P. (2001). Consequences of interspecific competition on the virulence and genetic composition of a nucleopolyhedrovirus in Spodoptera frugiperda larvae parasitized by Chelonus insularis. Biocontrol Science and Technology 11, 649–662.CrossRefGoogle Scholar
Fellous, S. and Koella, J. (2009). Infectious dose affects the outcome of the within-host competition between parasites. The American Naturalist 173, 177–184.CrossRefGoogle ScholarPubMed
Frank, S. A. (1996). Models of parasite virulence. The Quarterly Review of Biology 71, 37–78.CrossRefGoogle ScholarPubMed
Green, J. (1974). Parasites and epibionts of Cladocera. Philosophical Transactions of the Royal Society of London 32, 417–515.Google Scholar
Haghighat-Jahromi, M., Asasi, K., Nili, H., Dadras, H. and Shooshtari, A. H. (2008). Coinfection of avian influenza virus (H9N2 subtype) with infectious bronchitis live vaccine. Archives of Virology 153, 651–655.CrossRefGoogle ScholarPubMed
Hall, S. R., Tessier, A. J., Duffy, M. A., Huebner, M. and Cáceres, C. E. (2006). Warmer does not have to mean sicker: Temperature and predators can jointly drive timing of epidemics. Ecology 87, 1684–1695.CrossRefGoogle Scholar
Hall, R. S., Sivars-Becker, L., Becker, C., Duffy, M. A., Tessier, A. J. and Cáceres, C. E. (2007). Eating yourself sick: transmission of a disease as a function of foraging ecology. Ecology Letters 10, 207–218.CrossRefGoogle ScholarPubMed
Harter, H. L. (1961). Expected values of normal order statistics. Biometrics 48, 151.CrossRefGoogle Scholar
Harvell, D., Altizer, S., Cattadori, I. M., Harrington, L. and Weil, E. (2009). Climate change and wildlife diseases: When does the host matter the most? Ecology 90, 912–920.CrossRefGoogle ScholarPubMed
Holmes, J. C. (2002). Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). I. General effects and comparison with crowding. Journal of Parasitology 88, 434–439.Google ScholarPubMed
Hood, M. E. (2003). Dynamics of multiple infection and within-host competition by the anther-smut pathogen. The American Naturalist 162, 122–133.CrossRefGoogle ScholarPubMed
Hughes, W. O. H. and Boomsma, J. J. (2004). Let your enemy do the work: within-host interactions between two fungal parasites of leaf-cutting ants. Proceedings of the Royal Society of London, B 271, S104–S106.CrossRefGoogle ScholarPubMed
Jackson, J. A., Pleass, R. J., Cable, J., Bradley, J. E. and Tinsley, R. C. (2006). Heterogenous interspecific interactions in a host–parasite system. Parasitology 36, 1341–1349.Google Scholar
Jäger, I. and Schjørring, S. (2006). Multiple infections: relatedness and time between infections affect the establishment and growth of the cestode Schistocephalus solidus in its stickleback host. Evolution 60, 616–622.Google ScholarPubMed
Kurtz, J. and Armitage, S. O. (2006). Alternative adaptive immunity in invertebrates. Trends in Immunology 27, 493–496.CrossRefGoogle ScholarPubMed
Lampert, W. and Sommer, U. (1999). Limnooekologie, 2nd Edn.Georg Thieme Verlag, Stuttgart, Germany and New York, USA.Google Scholar
Lello, J., Boag, B., Fenton, A., Stevenson, I. R. and Hudson, P. J. (2004). Competition and mutualism among gut helminths of a mammalian host. Nature, London 428, 840–844.CrossRefGoogle ScholarPubMed
Lello, J., Norman, R. A., Boag, B., Hudson, P. J. and Fenton, A. (2008). Pathogen interactions, population cycles, and phase shifts. The American Naturalist 171, 176–182.CrossRefGoogle ScholarPubMed
Lohr, J. N., Yin, M. and Wolinska, J. (2010). A Daphnia parasite (Coullerya mesnili) constitutes a new member of the Ichthyosporea, a group of protists near the animal-fungi divergence. Journal of Eukaryotic Microbiology (in the Press).CrossRefGoogle ScholarPubMed
Mosquera, J. and Adler, F. R. (1998). Evolution of virulence: a unified framework for coinfection and superinfection. Journal of Theoretical Biology 195, 293–313.CrossRefGoogle ScholarPubMed
Read, A. F. and Taylor, L. H. (2001). The ecology of genetically diverse infections. Science 292, 1099–1102.CrossRefGoogle ScholarPubMed
Rolff, J. and Siva-Jothy, M. T. (2003). Invertebrate ecological immunology. Science 301, 472–475.CrossRefGoogle ScholarPubMed
Stentiford, G. D., Evans, M., Bateman, K. and Feist, S. W. (2003). Co-infection by a yeast-like organism in Hematodinium-infected European edible crabs Cancer pagurus and velvet swimming crabs Necora puber from the Engish Channel. Diseases of Aquatic Organisms 54, 195–202.CrossRefGoogle Scholar
Stirnadel, H. A. and Ebert, D. (1997). Prevalence, host specificity and impact on host fecundity of microparasites and epibionts in tree sympatric Dahpnia species. Journal of Animal Ecology 66, 212–222.CrossRefGoogle Scholar
Tellenbach, C., Wolinska, J. and Spaak, P. (2007). Epidemiology of a Daphnia brood parasite and its implications on host life-history traits. Oecologia 154, 369–375.CrossRefGoogle ScholarPubMed
Wille, P., Boller, T. and Kaltz, O. (2002). Mixed inoculation alters infection success of strains of the endophyte Epichloë bromicola on its grass host Bromus erectus. Proceedings of the Royal Society of London, B 269, 397–402.CrossRefGoogle ScholarPubMed
Wolinska, J., Bittner, K., Ebert, D. and Spaak, P. (2006). The coexistence of hybrid and parental Daphnia: the role of parasites. Proceedings of the Royal Society of London, B 273, 1977–1983.Google ScholarPubMed
Wolinska, J., Keller, B., Manca, M. and Spaak, P. (2007). Parasite survey of a Daphnia hybrid complex: host-specificity and environment determine infection. Journal of Animal Ecology 76, 191–200.CrossRefGoogle ScholarPubMed
Wolinska, J., Giessler, S. and Koerner, H. (2009). Molecular identification and hidden diversity of novel Daphnia parasites from European lakes. Applied and Environmental Microbiology 75, 7051–7059.CrossRefGoogle ScholarPubMed