Hostname: page-component-84b7d79bbc-x5cpj Total loading time: 0 Render date: 2024-07-26T11:28:24.598Z Has data issue: false hasContentIssue false

Infection success of different trematode genotypes in two alternative intermediate hosts: evidence for intraspecific specialization?

Published online by Cambridge University Press:  21 September 2009

T. L. F. LEUNG*
Affiliation:
Department of Zoology, University of Otago, P. O. Box 56, Dunedin9054, New Zealand
R. POULIN
Affiliation:
Department of Zoology, University of Otago, P. O. Box 56, Dunedin9054, New Zealand
*
*Corresponding author: Tel: +64 3 4797964. Fax: +64 3 479 7584. E-mail: tommylfleung@gmail.com

Summary

The evolution of host specificity and the potential trade-off between being a generalist and a specialist are central issues in the evolutionary ecology of parasites. Different species of parasites or even different populations of the same species often show different degrees of host specificity. However, less is known about intraspecific variation in host specificity within a population. We investigated intraspecific variation by experimentally exposing cercariae from different clones of the trematode Curtuteria australis to two species of second intermediate hosts, the New Zealand cockle Austrovenus stutchburyi and the wedge shell Macomona liliana. We found an overall difference in infection success between the two bivalve species, with A. stutchburyi being the more heavily infected host. However, the cercariae showed a consistent preference for encysting at the tip of the bivalve's foot, regardless of host species. Importantly, there were no significant differences among parasite clones in either relative infection success in the two hosts or preference for the host foot tip. This lack of intraspecific variation may be due to the life-history traits of both parasite and hosts in our system, which may limit opportunities for variation in performance and exploitation strategies in different hosts to evolve within the population.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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

Allison, F. R. (1979). Life cycle of Curtuteria australis n.sp. (Digenea: Echinostomatidae: Himasthlinae), intestinal parasite of the South Island pied oystercatcher. New Zealand Journal of Zoology 6, 1320.CrossRefGoogle Scholar
Arnaud-Haond, S. and Belkhir, K. (2007). GENCLONE: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Molecular Ecology Notes 7, 1517.CrossRefGoogle Scholar
Batista, F. M., Boudry, P., Dos Santos, A., Renault, T. and Ruano, F. (2009). Infestation of the cupped oysters Crassostrea angulata, C. gigas and their first-generation hybrids by the copepod Myicola ostreae: differences in susceptibility and host response. Parasitology 136, 537543.CrossRefGoogle ScholarPubMed
Blaustein, A. R., Romansic, J. M., Scheessele, E. A., Han, B. A., Pessier, A. P. and Longcore, J. E. (2005). Interspecific variation in susceptibility of frog tadpoles to the pathogenic fungus Batrachochytrium dendrobatidis. Conservation Biology 19, 14601468.CrossRefGoogle Scholar
Booth, J. D. (1983). Studies on twelve common bivalve larvae, with notes on bivalve spawning season in New Zealand. New Zealand Journal of Marine and Freshwater Research 17, 231265.CrossRefGoogle Scholar
Dang, C., de Montaudouin, X., Bald, J., Jude, F., Raymond, N., Lanceleur, L., Paul-Pont, I. and Caill-Milly, N. (2009). Testing the Enemy Release Hypothesis: trematode parasites in the non indigenous Manila clam Ruditapes philippinarum. Hydrobiologia 630, 139148.CrossRefGoogle Scholar
Detwiler, J. T. and Minchella, D. J. (2009). Intermediate host availability masks the strength of experimentally-derived colonisation patterns in echinostome trematodes. Interntional Journal for Parasitology 39, 585590.CrossRefGoogle ScholarPubMed
Dybdahl, M. F. and Lively, C. M. (1996). The geography of coevolution: comparative population structures for a snail and its trematode parasite. Evolution 50, 22642275.CrossRefGoogle ScholarPubMed
Edwards, D. D. and Vidrine, M. F. (2006). Host specificity among Unionicola spp. (Acari: Unionicolidae) parasitizing freshwater mussels. Journal of Parasitology 92, 977983.CrossRefGoogle ScholarPubMed
Egas, M., Dieckmann, U. and Sabelis, M. W. (2004). Evolution restricts the coexistence of specialists and generalists: the role of trade-off structure. American Naturalist 163, 518531.CrossRefGoogle ScholarPubMed
Ferry-Graham, L. A., Bolnick, D. I. and Wainright, P. C. (2002). Using functional morphology to examine the ecology and evolution of specialization. Integrative and Comparative Biology 13, 245258.Google Scholar
Futuyma, D. J. and Moreno, G. (1988). The evolution of ecological specialisation. Annual Review of Ecology and Systematics 19, 207233.CrossRefGoogle Scholar
Glennon, V., Chisholm, L. A. and Whittington, I. D. (2007). Experimental infections, using a fluorescent marker, of two elasmobranch species by uniciliated larvae Branchotenthes octahamatus (Monogenea: Hexabothriidae): invasion route, host specificity and post-larval development. Parasitology 134, 12431252.CrossRefGoogle Scholar
González, L., Carvajal, J. and George-Nascimento, M. (2000). Differential infectivity of Caligus flexispina (Copepoda, Caligidae) in three farmed salmonids in Chile. Aquaculture 183, 1323.CrossRefGoogle Scholar
Huyse, T., Poulin, R. and Théron, A. (2005). Speciation in parasites: a population genetic approach. Trends in Parasitology 21, 469475.CrossRefGoogle Scholar
Johnson, P. T. J. and Hartson, R. B. (2009). All hosts are not equal: explaining differential patterns of malformations in an amphibian community. Journal of Animal Ecology 78, 191201.CrossRefGoogle ScholarPubMed
Johnson, P. T. J., Sutherland, D. R., Kinsella, J. M. and Lunde, K. B. (2004). Review of the trematode genus Ribeiroia (Psilostomidae): ecology, life history, and pathogenesis with special emphasis on the amphibian malformation problem. Advances in Parasitology 57, 191253.CrossRefGoogle ScholarPubMed
Jones, C. M., Nagel, L., Hughes, G. L., Cribb, T. H. and Grutter, A. S. (2007). Host specificity of two species of Gnathia (Isopoda) determined by DNA sequencing blood meals. International Journal for Parasitology 37, 927935.CrossRefGoogle ScholarPubMed
Kalbe, M., Haberl, B., Hertel, J. and Haas, W. (2004). Heredity of specific host-finding behaviour in Schistosoma mansoni miracidia. Parasitology 128, 635643.CrossRefGoogle ScholarPubMed
Kassen, R. (2002). The experimental evolution of specialist, generalists, and the maintenance of diversity. Journal of Evolutionary Biology 15, 173190.CrossRefGoogle Scholar
Keeney, D. B., Bryan-Walker, K., King, T. M. and Poulin, R. (2008). Local variation of within-host clonal diversity coupled with genetic homogeneity in a marine trematode. Marine Biology 154, 183190.CrossRefGoogle Scholar
Krasnov, B. R., Poulin, R., Shenbrot, G. I., Mouillot, D. and Khokhlova, I. S. (2004). Ectoparasitic “jacks-of-all-trades”: relationship between abundance and host specificity in fleas (Siphonaptera) parasitic on small mammals. American Naturalist 164, 506516.CrossRefGoogle ScholarPubMed
Lajeunesse, M. J., Forbes, M. R. and Smith, B. P. (2004). Species and sex biases in ectoparasitism of dragonflies by mites. Oikos 106, 501508.CrossRefGoogle Scholar
Leung, T. L. F., Keeney, D. B. and Poulin, R. (2009). Genetics, intensity-dependence, and host manipulation in the trematode Curtuteria australis: following the strategies of others? Oikos (in the Press).Google Scholar
Leung, T. L. F., King, T. M., Poulin, R. and Keeney, D. B. (2008). Ten polymorphic microsatellite loci for the trematode Curtuteria australis (Echinostomatidae). Molecular Ecology Resources 8, 10461048.CrossRefGoogle ScholarPubMed
Leung, T. L. F. and Poulin, R. (2008). Size-dependent pattern of metacercariae accumulation in Macomona liliana: the threshold for infection in a dead-end host. Parasitology Research 104, 177180.CrossRefGoogle Scholar
Montresor, L. C., Vidigal, T. H. D. A., Mendonça, C. L. G. F., Fernandes, A. A., de Souza, K. N., Carvalho, O. S., Caputo, L. F. G., Mota, E. M. and Lenzi, H. L. (2008). Angiostrongylus costaricensis (Nematoda: Protostrongylidae): migration route in experimental infection of Omalonyx sp. (Gastropoda: Succineidae). Parasitology Research 103, 13391346.CrossRefGoogle ScholarPubMed
Mouritsen, K. N. (2002). The parasite-induced surfacing behaviour in the cockle Austrovenus stutchburyi: a test of an alternative hypothesis and identification of potential mechanisms. Parasitology 124, 521528.CrossRefGoogle ScholarPubMed
Mouritsen, K. N. and Poulin, R. (2003). Parasite-induced trophic facilitation exploited by non-host predator: a manipulator's nightmare. International Journal for Parasitology 33, 10431050.CrossRefGoogle ScholarPubMed
Olstad, K., Robertson, G., Bachmann, L. and Bakke, T. A. (2007). Variation in host preference within Gyrodactylus salaries (Monogenea): an experimental approach. Parasitology 134, 589597.CrossRefGoogle Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites. Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
Poulin, R. and Keeney, D. B. (2008). Host specificity under molecular and experimental scrutiny. Trends in Parasitology 24, 2428.CrossRefGoogle ScholarPubMed
Randhawa, H. S., Saunders, G. W. and Burt, M. D. B. (2007). Establishment of the onset of host specificity in four phyllobothriid tapeworm species (Cestoda: Tetraphyllidea) using a molecular approach. Parasitology 134, 12911300.CrossRefGoogle ScholarPubMed
Rauch, G., Kalbe, M. and Reusch, T. B. H. (2006). One day is enough: rapid and specific host-parasite interactions in a stickleback-trematode system. Biology Letters 2, 382384.CrossRefGoogle Scholar
Smith, N. F., Ruiz, G. M. and Reed, S. A. (2007). Habitat and host specificity of trematode metacercariae in fiddler crabs from mangrove habitats in Florida. Journal of Parasitology 93, 999–1005.CrossRefGoogle ScholarPubMed
Štefka, J., Hypša, V. and Scholz, T. (2009). Interplay of host specificity and biogeography in the population structure of a cosmopolitan endoparasite: microsatellite study of Ligula intestinalis (Cestoda). Molecular Ecology 18, 11871206.CrossRefGoogle ScholarPubMed
Thomas, F., Brown, S. P., Sukhdeo, M. and Renaud, F. (2002). Understanding parasite strategies: a state-dependent approach? Trends in Parasitology 18, 387390.CrossRefGoogle ScholarPubMed
Thomas, F. and Poulin, R. (1998). Manipulation of a mollusc by a trophically transmitted parasite: convergent evolution or phylogenetic inheritance? Parasitology 116, 431436.CrossRefGoogle ScholarPubMed
Whitlock, M. C. (1996). The red queen beats the jack-of-all-trades: the limitations on the evolution of phenotypic plasticity and niche breadth. American Naturalist 159, S76S88.Google Scholar
Yokoyama, H., Kim, J-H. and Urawa, S. (2006). Differences in host selection of actinospores of two myxosporeans Myxobolus arcticus and Thelohanellus hovorkai. Journal of Parasitology 92, 725729.CrossRefGoogle ScholarPubMed