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Conditional persistence and tolerance characterize endoparasite–colonial host interactions

Published online by Cambridge University Press:  14 March 2017

INÊS FONTES
Affiliation:
Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK Scottish Fish Immunology Research Centre, University of Aberdeen, Aberdeen AB24 2TZ, UK Eawag, Swiss Federal Institute of Aquatic Science and Technology, Dübendorf, Switzerland ETH Zürich, Institute of Integrative Biology (IBZ), Zürich, Switzerland
HANNA HARTIKAINEN
Affiliation:
Eawag, Swiss Federal Institute of Aquatic Science and Technology, Dübendorf, Switzerland ETH Zürich, Institute of Integrative Biology (IBZ), Zürich, Switzerland
NICK G. H. TAYLOR
Affiliation:
Centre for Environment Fisheries and Aquaculture Science (Cefas), Weymouth, Barrack Road, Dorset DT4 8UB, UK
BETH OKAMURA*
Affiliation:
Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK
*
*Corresponding author: Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK. E-mail: b.okamura@nhm.ac.uk

Summary

Colonial hosts offer unique opportunities for exploitation by endoparasites resulting from extensive clonal propagation, but these interactions are poorly understood. The freshwater bryozoan, Fredericella sultana, and the myxozoan, Tetracapsuloides bryosalmonae, present an appropriate model system for examining such interactions. F. sultana propagates mainly asexually, through colony fragmentation and dormant propagules (statoblasts). Our study examines how T. bryosalmonae exploits the multiple transmission routes offered by the propagation of F. sultana, evaluates the effects of such transmission on its bryozoan host, and tests the hypothesis that poor host condition provokes T. bryosalmonae to bail out of a resource that may soon be unsustainable, demonstrating terminal investment. We show that infections are present in substantial proportions of colony fragments and statoblasts over space and time and that moderate infection levels promote statoblast hatching and hence effective fecundity. We also found evidence for terminal investment, with host starvation inducing the development of transmission stages. Our results contribute to a growing picture that interactions of T. bryosalmonae and F. sultana are generally characterized by parasite persistence, facilitated by multiple transmission pathways and host condition-dependent developmental cycling, and host tolerance, promoted by effective fecundity effects and an inherent capacity for renewed growth and clonal replication.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Abd-Elfattah, A., Fontes, I., Kumar, G., Soliman, H., Hartikainen, H., Okamura, B. and El-Matbouli, M. (2014). Vertical transmission of the Tetracapsuloides bryosalmonae (Myxozoa), the causative agent of proliferative kidney disease. Parasitology 141, 482490.CrossRefGoogle ScholarPubMed
Acosta, A., Sammarco, P. and Duarte, L. (2001). Asexual reproduction in a zoanthid by fragmentation: the role of exogenous factors. Bulletin of Marine Science 68, 363381.Google Scholar
Bates, D., Maechler, M., Bolker, B. and Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 148.CrossRefGoogle Scholar
Bavestrello, G., Puce, S., Cerrano, C., Castellano, L. and Arillo, A. (2000). Water movement activating fragmentation: a new dispersal strategy for hydractiniid hydroids. Journal of the Marine Biological Association of the United Kingdom 80, 361362.CrossRefGoogle Scholar
Baxa, D. V., Kelley, G. O., Mukkatira, K. S., Beauchamp, K. A., Rasmussen, C. and Hedrick, R. P. (2008). Arrested development of the myxozoan parasite, Myxobolus cerebralis, in certain populations of mitochondrial 16S lineage III Tubifex tubifex . Parasitology Research 102, 219228.CrossRefGoogle ScholarPubMed
Bonsall, M. B., Sait, S. M. and Hails, R. S. (2005). Invasion and dynamics of covert infection strategies in structured insect–pathogen populations. Journal of Animal Ecology 74, 464474.CrossRefGoogle Scholar
Bruneaux, M., Visse, M., Gross, R., Pukk, L., Saks, L. and Vasemägi, A. (2016). Parasite infection and decreased thermal tolerance: impact of proliferative kidney disease on a wild salmonid fish in the context of climate change. Functional Ecology 31, 216226.CrossRefGoogle Scholar
Bullard, S. G., Sedlack, B., Reinhardt, J. F., Litty, C., Gareau, K. and Whitlatch, R. B. (2007). Fragmentation of colonial ascidians: differences in reattachment capability among species. Journal of Experimental Marine Biology and Ecology 342, 166168.CrossRefGoogle Scholar
Canning, E. U. and Okamura, B. (2003). Biodiversity and evolution of the Myxozoa. Advances in Parasitology 56, 43131.CrossRefGoogle Scholar
Clutton-Brock, T. H. (1984). Reproductive effort and terminal investment in iteroparous animals. The American Naturalist 123, 212229.CrossRefGoogle Scholar
De Kinkelin, P., Gay, M. and Forman, S. (2002). The persistence of infectivity of Tetracapsula bryosalmonae-infected water for rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 25, 477482.CrossRefGoogle Scholar
Feist, S. W., Longshaw, M., Canning, E. U. and Okamura, B. (2001). Induction of proliferative kidney disease (PKD) in rainbow trout Oncorhynchus mykiss via the bryozoan Fredericella sultana infected with Tetracapsula bryosalmonae . Diseases of Aquatic Organisms 45, 6168.CrossRefGoogle ScholarPubMed
Fontes, I. (2015). Life history, distribution and invertebrate host-parasite interactions of the causative agent of proliferative kidney disease (PKD), Tetracapsuloides bryosalmonae . Ph.D. thesis, The University of Aberdeen, Aberdeen, UK.Google Scholar
Gay, M., Okamura, B. and de Kinkelin, P. (2001). Evidence that infectious stages of Tetracapsula bryosalmonae for rainbow trout Oncorhynchus mykiss are present throughout the year. Diseases of Aquatic Organisms 46, 3140.CrossRefGoogle ScholarPubMed
Grabner, D. S. and El-Matbouli, M. (2008). Transmission of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) to Fredericella sultana (Bryozoa: Phylactolaemata) by various fish species. Diseases of Aquatic Organisms 79, 133139.CrossRefGoogle ScholarPubMed
Graham, A. L., Shuker, D. M., Pollitt, L. C., Auld, S. K. J. R., Wilson, A. J. and Little, T. J. (2011). Fitness consequences of immune responses: strengthening the empirical framework for ecoimmunology. Functional Ecology 25, 517.CrossRefGoogle Scholar
Hartikainen, H. and Okamura, B. (2012). Castrating parasites and colonial hosts. Parasitology 139, 547556.CrossRefGoogle ScholarPubMed
Hartikainen, H. and Okamura, B. (2015). Ecology and evolution of malacosporean-bryozoan interactions. In Myxozoan Evolution, Ecology and Development (ed. Okamura, B., Gruhl, A. and Bartholomew, J. L.), pp. 201216. Springer International Publishing, Cham, Switzerland.CrossRefGoogle Scholar
Hartikainen, H., Fontes, I. and Okamura, B. (2013). Parasitism and phenotypic change in colonial hosts. Parasitology 140, 14031412.CrossRefGoogle ScholarPubMed
Highsmith, R. C. (1982). Reproduction by fragmentation in corals. Marine Ecology Progress Series 7, 207226.CrossRefGoogle Scholar
Hill, S. L. and Okamura, B. (2007). Endoparasitism in colonial hosts: patterns and processes. Parasitology 134, 841852.CrossRefGoogle ScholarPubMed
Jackson, J. B. C. and Coates, A. G. (1986). Life cycles and evolution of clonal (modular) animals. Philosophical Transactions of the Royal Society B 313, 722.Google Scholar
Lasker, H. R. (1984). Asexual reproduction, fragmentation, and skeletal morphology of a plexaurid gorgonian. Marine Ecology Progress Series 19, 261268.CrossRefGoogle Scholar
Little, T. J., Shuker, D. M., Colegrave, N., Day, T. and Graham, A. L. (2010). The coevolution of virulence: tolerance in perspective. PLoS Pathogens 6, e1001006.CrossRefGoogle Scholar
Morris, D. J. and Adams, A. (2006). Transmission of freshwater myxozoans during the asexual propagation of invertebrate hosts. International Journal for Parasitology 36, 371377.CrossRefGoogle ScholarPubMed
O'Dea, A. (2006). Asexual propagation in the marine bryozoan Cupuladria exfragminis . Journal of Experimental Marine Biology and Ecology 335, 312322.CrossRefGoogle Scholar
Okamura, B. (2016). Hidden infections and changing environments. Integrative and Comparative Biology 56, 620629.CrossRefGoogle ScholarPubMed
Okamura, B., Hartikainen, H., Schmidt-Posthaus, H. and Wahli, T. (2011). Life cycle complexity, environmental change and the emerging status of salmonid proliferative kidney disease. Freshwater Biology 56, 735753.CrossRefGoogle Scholar
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. and Team, R. C. (2016). nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1–117, http://CRAN.R-project.org/package=nlme.Google Scholar
R Core Team (2014). R: A Language and Environment for Statistical Computing. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.Google Scholar
Råberg, L., Graham, A. L. and Read, A. F. (2009). Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 364, 3749.CrossRefGoogle ScholarPubMed
Singer, M. S., Mason, P. A. and Smilanich, A. M. (2014). Ecological immunology mediated by diet in herbivorous insects. Integrative and Comparative Biology 54, 913921.CrossRefGoogle ScholarPubMed
Sorrell, I., White, A., Pedersen, A. B., Hails, R. S. and Boots, M. (2009). The evolution of covert, silent infection as a parasite strategy. Proceedings of the Royal Society of London. Series B, Biological Sciences 276, 22172226.Google ScholarPubMed
Sutherland, C. J. (2016). Persistent parasitism: the adaptive biology of malariae and ovale malaria. Trends in Parasitology 32, 808819.CrossRefGoogle ScholarPubMed
Tops, S. (2004). Ecology, life history and diversity of malacosporeans. Ph.D. thesis, University of Reading, Reading, UK.Google Scholar
Tops, S., Lockwood, W. and Okamura, B. (2006). Temperature-driven proliferation of Tetracapsuloides bryosalmonae in bryozoan hosts portends salmonid declines. Diseases of Aquatic Organisms 70, 227236.CrossRefGoogle ScholarPubMed
Tops, S., Hartikainen, H. and Okamura, B. (2009). The effects of infection by Tetracapsuloides bryosalmonae (Myxozoa) and temperature on Fredericella sultana (Bryozoa). International Journal for Parasitology 39, 10031010.CrossRefGoogle ScholarPubMed
Ushijima, B., Smith, A., Aeby, G. S. and Callahan, S. M. (2012). Vibrio owensii induces the tissue loss disease Montipora white syndrome in the Hawaiian reef coral Montipora capitata . PLoS ONE 7, e46717.CrossRefGoogle ScholarPubMed
Veening, J.-W., Smits, W. K. and Kuipers, O. P. (2008). Bistability, epigenetics, and bet-hedging in bacteria. Annual Review of Microbiology 62, 193210.CrossRefGoogle ScholarPubMed
Ward, J. R., Kim, K. and Harvell, C. D. (2007). Temperature affects coral disease resistance and pathogen growth. Marine Ecology Progress Series 329, 115121.CrossRefGoogle Scholar
Williams, D. E., Miller, M. W. and Baums, I. B. (2014). Cryptic changes in the genetic structure of a highly clonal coral population and the relationship with ecological performance. Coral Reefs 33, 595606.CrossRefGoogle Scholar
Wood, T. S. (1973). Colony development in species of Plumatella and Fredericella (Ectoprocta: Phylactolaemata). In Animal Colonies, Development and Function through Time (ed. Boardman, R. S., Cheetham, A. H. and Oliver, W. A. J.), pp. 395432. Hutchinson and Ross, Stroudsburg, USA.Google Scholar
Wood, T. S. and Okamura, B. (2005). A New Key to the Freshwater Bryozoans of Britain, Ireland and Continental Europe, with Notes on their Ecology. Freshwater Biological Association, Ambleside, Cumbria, UK.Google Scholar
Wulff, J. L. (1991). Asexual fragmentation, genotype success, and population dynamics of erect branching sponges. Journal of Experimental Marine Biology and Ecology 149, 227247.CrossRefGoogle Scholar
Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A. and Smith, G. M. (2009). Mixed Effects Models and Extensions in Ecology with R, 1st Edn. Springer, New York.CrossRefGoogle Scholar
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