Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-20T03:15:28.116Z Has data issue: false hasContentIssue false
  • English
  • Français

Parasitism and phenotypic change in colonial hosts

Published online by Cambridge University Press:  21 August 2013

HANNA HARTIKAINEN ,
INÊS FONTES  and
BETH OKAMURA
HANNA HARTIKAINEN*
Affiliation:
Department of Aquatic Ecology, EAWAG, Überlandstrasse 133, Dübendorf 8600, Switzerland Department of Life Sciences, Natural History Museum, London SW7 5BD, UK
INÊS FONTES
Affiliation:
Department of Life Sciences, Natural History Museum, London SW7 5BD, UK
BETH OKAMURA
Affiliation:
Department of Life Sciences, Natural History Museum, London SW7 5BD, UK
*
*Corresponding author: Department of Life Sciences, Natural History Museum, London SW7 5BD, UK. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Changes in host phenotype are often attributed to manipulation that enables parasites to complete trophic transmission cycles. We characterized changes in host phenotype in a colonial host–endoparasite system that lacks trophic transmission (the freshwater bryozoan Fredericella sultana and myxozoan parasite Tetracapsuloides bryosalmonae). We show that parasitism exerts opposing phenotypic effects at the colony and module levels. Thus, overt infection (the development of infectious spores in the host body cavity) was linked to a reduction in colony size and growth rate, while colony modules exhibited a form of gigantism. Larger modules may support larger parasite sacs and increase metabolite availability to the parasite. Host metabolic rates were lower in overtly infected relative to uninfected hosts that were not investing in propagule production. This suggests a role for direct resource competition and active parasite manipulation (castration) in driving the expression of the infected phenotype. The malformed offspring (statoblasts) of infected colonies had greatly reduced hatching success. Coupled with the severe reduction in statoblast production this suggests that vertical transmission is rare in overtly infected modules. We show that although the parasite can occasionally infect statoblasts during overt infections, no infections were detected in the surviving mature offspring, suggesting that during overt infections, horizontal transmission incurs a trade-off with vertical transmission.

Keywords

host manipulationresource competitionBryozoaMyxozoaFredericella sultanaTetracapsuloides bryosalmonaeovert infectiongigantismmetabolic ratematernal effects
Type
Research Article
Information
Parasitology , Volume 140 , Issue 11 , September 2013 , pp. 1403 - 1412
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aeby, G. S. (2003). Corals in the genus Porites are susceptible to infection by a larval trematode. Coral Reefs 22, 216.CrossRefGoogle Scholar
Baayen, R. H., Davidson, D. J. and Bates, D. M. (2008). Mixed-effects modelling with crossed random effects for subjects and items. Journal of Memory and Language 59, 390–412.CrossRefGoogle Scholar
Backus, B. T. and Wood, T. S. (1981). Karyotypic and morphological confirmation of species in Fredericella australiensis (Bryozoa: Phylactolaemata). Transactions of the American Microscopical Society 100, 253–263.CrossRefGoogle Scholar
Cézilly, F. and Perrot-Minnot, M.-J. (2010). Interpreting multidimensionality in parasite-induced phenotypic alterations: panselectionism versus parsimony. Oikos 119, 1224–1229.CrossRefGoogle Scholar
Chadwick, W. and Little, T. J. (2005). A parasite-mediated life-history shift in Daphnia magna. Proceedings of the Royal Society of London Series B 272, 505–509.Google ScholarPubMed
Collins, T. J. (2007). ImageJ for microscopy. BioTechniques 43, S25–S30.CrossRefGoogle ScholarPubMed
Ebert, D. (2005). Ecology, Epidemiology and Evolution of Parasitism in Daphnia. NCBI, Bethesda, MD, USA.Google Scholar
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, 133–139.CrossRefGoogle ScholarPubMed
Hartikainen, H. and Okamura, B. (2012). Castrating parasites and colonial hosts. Parasitology 139, 547–556.CrossRefGoogle ScholarPubMed
Hartikainen, H., Johnes, P., Moncrieff, C. and Okamura, B. (2009). Bryozoan populations reflect nutrient enrichment and productivity gradients in rivers. Freshwater Biology 54, 2320–2334.CrossRefGoogle Scholar
Hudson, P. J., Dobson, A. P. and Lafferty, K. D. (2006). Is a healthy ecosystem one that is rich in parasites? Trends in Ecology and Evolution 21, 381–385.CrossRefGoogle Scholar
Kuris, A. M., Hechinger, R. F., Shaw, J. C., Whitney, K., Aguirre-Macedo, L., Boch, C., Dobson, A., Dunham, E. J., Fredensborg, B. L., Huspeni, T. C. et al. (2008). Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454, 515–518.CrossRefGoogle ScholarPubMed
Lafferty, K. D. and Kuris, A. M. (2009). Parasitic castration: the evolution and ecology of body snatchers. Trends in Parasitology 25, 564–572.CrossRefGoogle ScholarPubMed
Lafferty, K. D., Dobson, A. P. and Kuris, A. M. (2006). Parasites dominate food web links. Proceedings of the National Academy of Sciences USA 103, 11211–11216.CrossRefGoogle ScholarPubMed
Lafferty, K. D., Allesina, S., Arim, M., Briggs, C. J., De Leo, G., Dobson, A. P., Dunne, J. A., Johnson, P. T. J., Kuris, A. M., Martinez, N. D. et al. (2008). Parasites in food webs: the ultimate missing links. Ecology Letters 11, 533–546.CrossRefGoogle ScholarPubMed
McGurk, C., Morris, D. J., Auchinachie, N. A. and Adams, A. (2006). Development of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) in bryozoan hosts (as examined by light microscopy) and quantitation of infective dose to rainbow trout (Oncorhynchus mykiss). Veterinary Parasitology 135, 249–257.CrossRefGoogle ScholarPubMed
Médoc, V. and Beisel, J.-N. (2011). When trophically-transmitted parasites combine predation enhancement with predation suppression to optimize their transmission. Oikos 120, 1452–1458.CrossRefGoogle Scholar
Minchella, D. J. (1985). Host life-history variation in response to parasitism. Parasitology 90, 205–216.CrossRefGoogle Scholar
Morris, D. and Adams, A. (2006). Proliferative, presaccular stages of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) within the invertebrate host Fredericella sultana (Bryozoa: Phylactolaemata). Journal of Parasitology 92, 984–989.CrossRefGoogle ScholarPubMed
Okamura, B., Hartikainen, H., Schmidt-Posthaus, H. and Wahli, T. (2011). Proliferative kidney disease as an emerging disease: the importance of life cycle complexity and environmental change. Freshwater Biology 56, 735–753.CrossRefGoogle Scholar
Palmer, C. V., Roth, M. S. and Gates, R. D. (2009). Red fluorescent protein responsible for pigmentation in trematode-infected Porites compressa tissues. Biological Bulletin 216, 68–74.CrossRefGoogle ScholarPubMed
Parker, G. A., Ball, M. A., Chubb, J. C., Hammerschmidt, K. and Milinski, M. (2009). When should a trophically transmitted parasite manipulate its host? Evolution 63, 448–458.CrossRefGoogle ScholarPubMed
Poulin, R. (1998). Evolutionary Ecology of Parasites – from Individuals to Communities. Chapman & Hall, London, UK.Google Scholar
Poulin, R. (2010). Parasite manipulation of host behavior: an update and frequently asked questions. In Advances in the Study of Behavior (ed. Brockmann, H. J., Roper, T. J., Naguib, M., Wynne-Edwards, K., E., Mitani, J. C. and Simmons, L. W.), pp. 151–186. Academic Press, Cambridge, UK.Google Scholar
Poulin, R. and Thomas, F. (1999). Phenotypic variability induced by parasites: extent and evolutionary implications. Parasitology Today 15, 28–32.CrossRefGoogle Scholar
Rogick, M. D. (1945). Studies on fresh-water Bryozoa XVI. Fredericella australiensis var. browni n. var. Biological Bulletin 89, 215–228.CrossRefGoogle Scholar
Seppälä, O. and Jokela, J. (2008). Host manipulation as a parasite transmission strategy when manipulation is exploited by non-host predators. Biology Letters 4, 663–666.CrossRefGoogle ScholarPubMed
Smith, V. (2007). Host resource supplies influence the dynamics and outcome of infectious disease. Integrative and Comparative Biology 47, 310–316.CrossRefGoogle ScholarPubMed
Thomas, F., Adamo, S. and Moore, J. (2005). Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185–199.CrossRefGoogle ScholarPubMed
Tops, S. (2004). Ecology, life history and diversity of malacosporeans. Ph.D. thesis, Animal and Microbial Sciences, University of Reading, Reading, UK.Google Scholar
Tops, S., Hartikainen, H. and Okamura, B. (2009). The effects of myxozoan infection and temperature on fitness of colonial hosts. International Journal for Parasitology 39, 1003–1010.CrossRefGoogle Scholar
Toriumi, M. (1951). Taxonomical study of fresh-water Bryozoa. I. Fredericella sultana (Blumenbach). Science Reports of the Tohôku University 19, 167–177.Google 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. 395–432. Dowden, Hutchinson and Ross, Stroudsburg, PA, USA.Google Scholar
Wood, T. S. (1996). Aquarium culture of freshwater invertebrates. American Biology Teacher 58, 46–50.CrossRefGoogle Scholar
Wood, T. S. and Okamura, B. (2005). A Key to the British and European Freshwater Bryozoans with Ecological Notes. Freshwater Biological Association, Ambleside, UK.Google Scholar