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The ups and downs of life: population expansion and bottlenecks of helminth parasites through their complex life cycle

Published online by Cambridge University Press:  12 January 2015

ROBERT POULIN  and
CLÉMENT LAGRUE
ROBERT POULIN*
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
CLÉMENT LAGRUE
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
*
*Corresponding author. Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand. E-mail: [email protected]
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Summary

The fundamental assumption underpinning the evolution of numerous adaptations shown by parasites with complex life cycles is that huge losses are incurred by infective stages during certain transmission steps. However, the magnitude of transmission losses or changes in the standing crop of parasites passing from upstream (source) to downstream (target) hosts have never been quantified in nature. Here, using data from 100 pairs of successive upstream–downstream life stages, from distinct populations representing 10 parasite species, we calculated the total density per m2 of successive life stages. We show that clonal amplification of trematodes in their first intermediate host leads to an average 4-fold expansion of numbers of individuals at the next life stage, when differences in the longevity of successive life stages are taken into account. In contrast, trophic transmission to the definitive host results in almost no numerical change for trematodes, but possibly in large decreases for acanthocephalans and nematodes, though a correction for longevity was not possible for the latter groups. Also, we only found a positive association between upstream and downstream stage densities for transmission involving free-swimming cercariae in trematodes, suggesting a simple output-recruitment process. For trophic transmission, there was no coupling between downstream and upstream parasite densities. These first quantitative estimates of ontogenetic rises and falls in numbers under natural conditions provide new insights into the selective pressures acting on parasites with complex cycles.

Keywords

complex life cyclestransmission modeparasite evolutionhelminthslongevitytrematodes
Type
Research Article
Information
Parasitology , Volume 142 , Issue 6 , May 2015 , pp. 791 - 799
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Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Adamson, M. L. (1986). Modes of transmission and evolution of life histories in zooparasitic nematodes. Canadian Journal of Zoology 64, 1375–1384.Google Scholar
Amundsen, P. A., Knudsen, R., Kuris, A. M. and Kristoffersen, R. (2003). Seasonal and ontogenetic dynamics in trophic transmission of parasites. Oikos 102, 285–293.CrossRefGoogle Scholar
Blaxter, M. and Koutsovoulos, G. (2014). The evolution of parasitism in Nematoda. Parasitology. doi: 10.1017/S0031182014000791.Google ScholarPubMed
Brown, S. P., Renaud, F., Guégan, J.-F. and Thomas, F. (2001). Evolution of trophic transmission in parasites: the need to reach a mating place? Journal of Evolutionary Biology 14, 815–820.Google Scholar
Choisy, M., Brown, S. P., Lafferty, K. D. and Thomas, F. (2003). Evolution of trophic transmission in parasites: why add intermediate hosts? American Naturalist 162, 172–181.Google Scholar
Combes, C., Fournier, A., Moné, H. and Théron, A. (1994). Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology 109, S3–S13.Google Scholar
Cribb, T. H., Bray, R. A., Olson, P. D. and Littlewood, D. T. J. (2003). Life cycle evolution in the Digenea: a new perspective from phylogeny. Advances in Parasitology 54, 197–254.Google Scholar
Curtis, L. A. (2003). Tenure of individual larval trematode infections in an estuarine gastropod. Journal of the Marine Biological Association of the UK 83, 1047–1051.CrossRefGoogle Scholar
Galaktionov, K. V. and Dobrovolskij, A. A. (2003). The Biology and Evolution of Trematodes. Kluwer Academic Publishers, Dordrecht, The Netherlands.Google Scholar
Haas, W., Haberl, B., Kalbe, M. and Körner, M. (1995). Snail-host-finding by miracidia and cercariae: chemical host cues. Parasitology Today 11, 468–472.Google Scholar
Herlyn, H., Piskurek, O., Schmitz, J., Ehlers, U. and Zischler, H. (2003). The syndermatan phylogeny and the evolution of acanthocephalan endoparasitism as inferred from 18S rDNA sequences. Molecular Phylogenetics and Evolution 26, 155–164.CrossRefGoogle ScholarPubMed
Herrmann, K. K. and Poulin, R. (2011). Encystment site affects the reproductive strategy of a progenetic trematode in its fish intermediate host: is host spawning an exit for parasite eggs? Parasitology 138, 1183–1192.CrossRefGoogle ScholarPubMed
Holton, A. L. (1984). Progenesis as a means of abbreviating life histories in two New Zealand trematodes, Coitocaecum parvum Crowfton, 1945 and Stegodexamene anguillae MacFarlane, 1951. Mauri Ora 11, 63–70.Google Scholar
Jellyman, D. J., Sagar, P. M., Glova, G. J. and Sykes, J. R. E. (2000). Age, growth, and movements of giant bullies (Gobiomorphus gobioides) in the Kakanui River estuary, South Island, New Zealand. New Zealand Journal of Marine and Freshwater Research 34, 523–530.Google Scholar
Jennings, J. B. and Calow, P. (1975). The relationship between high fecundity and the evolution of entoparasitism. Oecologia 21, 109–115.Google Scholar
Johnson, P. T. J. and Thieltges, D. W. (2010). Diversity, decoys and the dilution effect: how ecological communities affect disease risk. Journal of Experimental Biology 213, 961–970.CrossRefGoogle ScholarPubMed
Kaldonski, N., Perrot-Minnot, M.-J., Motreuil, S. and Cézilly, F. (2008). Infection with acanthocephalans increases the vulnerability of Gammarus pulex (Crustacea, Amphipoda) to non-host invertebrate predators. Parasitology 135, 627–632.Google Scholar
Keeney, D. B., Waters, J. M. and Poulin, R. (2007). Clonal diversity of the marine trematode Maritrema novaezealandensis within intermediate hosts: the molecular ecology of parasite life cycles. Molecular Ecology 16, 431–439.Google Scholar
Kennedy, C. R. (2006). Ecology of the Acanthocephala. Cambridge University Press, Cambridge.Google Scholar
Koehler, A. V., Brown, B., Poulin, R., Thieltges, D. W. and Fredensborg, B. L. (2012). Disentangling phylogenetic constraints from selective forces in the evolution of trematode transmission stages. Evolutionary Ecology 26, 1497–1512.Google Scholar
Koprivnikar, J., Lim, D., Fu, C. and Brack, S. H. M. (2010). Effects of temperature, salinity, and pH on the survival and activity of marine cercariae. Parasitology Research 106, 1167–1177.Google Scholar
Lafferty, K. D. (1999). The evolution of trophic transmission. Parasitology Today 15, 111–115.CrossRefGoogle ScholarPubMed
Lagrue, C. and Poulin, R. (2008 a). Lack of seasonal variation in the life-history strategies of the trematode Coitocaecum parvum: no apparent environmental effect. Parasitology 135, 1243–1251.Google Scholar
Lagrue, C. and Poulin, R. (2008 b). Intra- and interspecific competition among helminth parasites: effects on Coitocaecum parvum life history strategy, size and fecundity. International Journal for Parasitology 38, 1435–1444.Google Scholar
Lagrue, C., McEwan, J., Poulin, R. and Keeney, D. B. (2007). Co-occurrences of parasite clones and altered host phenotype in a snail-trematode system. International Journal for Parasitology 37, 1459–1467.Google Scholar
Levri, E. P. and Lively, C. M. (1996). The effects of size, reproductive condition, and parasitism on foraging behaviour in a freshwater snail, Potamopyrgus antipodarum . Animal Behaviour 51, 891–901.CrossRefGoogle Scholar
Lewis, E. E., Grewal, P. S. and Gaugler, R. (1995). Hierarchical order of host cues in parasite foraging strategies. Parasitology 110, 207–213.Google Scholar
McCallum, H. (2000). Population Parameters: Estimation for Ecological Models. Blackwell Science, Oxford.Google Scholar
McCarthy, H. O., Fitzpatrick, S. M. and Irwin, S. W. B. (2002). Life history and life cycles: production and behavior of trematode cercariae in relation to host exploitation and next-host characteristics. Journal of Parasitology 88, 910–918.Google Scholar
Moore, J. (1984). Altered behavioral responses in intermediate hosts: an acanthocephalan parasite strategy. American Naturalist 123, 572–577.Google Scholar
Moore, J. and Brooks, D. R. (1987). Asexual reproduction in cestodes (Cyclophyllidea: Taeniidae): ecological and phylogenetic influences. Evolution 41, 882–891.Google Scholar
Mouritsen, K. N. and Poulin, R. (2003). Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator's nightmare. International Journal for Parasitology 33, 1043–1050.Google Scholar
Nakagawa, S. and Schielzeth, H. (2013). A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods in Ecology and Evolution 4, 133–142.Google Scholar
Parker, G. A., Chubb, J. C., Ball, M. A. and Roberts, G. N. (2003). Evolution of complex life cycles in helminth parasites. Nature 425, 480–484.CrossRefGoogle ScholarPubMed
Pietrock, M. and Marcogliese, D. J. (2003). Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19, 293–299.Google Scholar
Poulin, R. (1996). The evolution of life history strategies in parasitic animals. Advances in Parasitology 37, 107–134.Google Scholar
Poulin, R. (2010). Parasite manipulation of host behaviour: an update and frequently asked questions. Advances in the Study of Behavior 41, 151–186.CrossRefGoogle Scholar
Rauch, G., Kalbe, M. and Reusch, T. B. H. (2005). How a complex life cycle can improve a parasite's sex life. Journal of Evolutionary Biology 18, 1069–1075.Google Scholar
Rowe, D. K. (1999). Factors influencing the abundance of the common bully, Gobiomorphus cotidianus McDowall, in small, North Island, New Zealand, lakes. Fisheries Management and Ecology 6, 377–386.Google 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.Google Scholar
Thieltges, D. W., Jensen, K. T. and Poulin, R. (2008). The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135, 407–426.Google Scholar
Thieltges, D. W., Amundsen, P.-A., Hechinger, R. F., Johnson, P. T. J., Lafferty, K. D., Mouritsen, K. N., Preston, D. L., Reise, K., Zander, C.D. and Poulin, R. (2013). Parasites as prey in aquatic food webs: implications for predator infection and parasite transmission. Oikos 122, 1473–1482.Google Scholar
Trouvé, S., Sasal, P., Jourdane, J., Renaud, F. and Morand, S. (1998). The evolution of life-history traits in parasitic and free-living Platyhelminthes: a new perspective. Oecologia 115, 370–378.Google Scholar
Winterbourn, M. J. (1970). Population studies on the New Zealand freshwater gastropod, Potamopyrgus antipodarum (Gray). Journal of Molluscan Studies 39, 139–149.Google Scholar
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