Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-23T03:26:32.476Z Has data issue: false hasContentIssue false

Ecological divergence of closely related Diplostomum (Trematoda) parasites

Published online by Cambridge University Press:  02 May 2006

A. KARVONEN
Affiliation:
Department of Biological and Environmental Science, P.O. Box 35, FI-40014 University of Jyväskylä, Finland
P. TERHO
Affiliation:
Department of Biological and Environmental Science, P.O. Box 35, FI-40014 University of Jyväskylä, Finland
O. SEPPÄLÄ
Affiliation:
Department of Biological and Environmental Science, P.O. Box 35, FI-40014 University of Jyväskylä, Finland
J. JOKELA
Affiliation:
EAWAG, Department of Limnology, ETH-Zürich, Department of Environmental Sciences, Überlandstrasse 133, CH-8600 Dübendorf, Switzerland
E. T. VALTONEN
Affiliation:
Department of Biological and Environmental Science, P.O. Box 35, FI-40014 University of Jyväskylä, Finland

Abstract

Parasite life-cycles present intriguing model systems to study divergence in resource use and ecology between parasite taxa. In ecologically similar taxa, consistent selective forces may lead to convergence of life-history traits, but resource overlap and similarity of life-cycles may also promote divergence between the taxa in (1) use of host species or (2) specific niche within a host. We studied the life-history characteristics of 2 sympatric species of Diplostomum parasites, D. spathaceum and D. gasterostei, concentrating particularly on differences in intermediate host use and characteristics of the infective stages between the species. This group of trematodes is a notoriously difficult challenge for morphological taxonomy and therefore any information on the ecology of these species can also be helpful in resolving their taxonomy. We observed that these species indeed had diverged as they used mainly different snail and fish species as intermediate hosts and in controlled experiments infected different regions of the eye (lens and vitreous body) of a novel fish host. Interestingly, cercarial characteristics (activity and life-span) were similar between the species and the species were difficult to separate at the cercarial stage unless one observes their swimming behaviour. The release of cercaria from the snail hosts was higher in D. spathaceum, but when cercarial numbers were proportioned to the volume of the snail host, the production was higher in D. gasterostei suggesting differences in the rate of snail host exploitation between the parasite species. These results corroborate the prediction that closely related parasite taxa which are competing for the same resources should have diverged in their life-history characteristics and host use.

Type
Research Article
Copyright
2006 Cambridge University Press

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

Adamson, M. L. and Caira, J. N. ( 1994). Evolutionary factors influencing the nature of parasite specificity. Parasitology 109 (Suppl.), S85S95.CrossRefGoogle Scholar
Anderson, R. M. and Whitfield, P. J. ( 1975). Survival characteristics of the free-living cercarial population of the ectoparasitic digenean Transversotrema patialensis (Soparker, 1924). Parasitology 70, 295310.CrossRefGoogle Scholar
Bargues, M. D., Vigo, M., Horak, P., Dvorak, J., Patzner, R. A., Pointier, J. P., Jackiewicz, M., Meier-Brook, C. and Mas-Coma, S. ( 2001). European Lymnaeidae (Mollusca: Gastropoda), intermediate hosts of trematodiases, based on nuclear ribosomal DNA ITS-2 sequences. Infection, Genetics and Evolution 1, 85107.CrossRefGoogle Scholar
Chappell, L. H., Hardie, L. J. and Secombes, C. J. ( 1994). Diplostomiasis: the disease and host-parasite interactions. In Parasitic Diseases of Fish ( ed. Pike, A. W. and Lewis, J. W.), pp. 5986. Samara Publishing Limited, Dyfed.
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, 172181.Google Scholar
Criscione, C. D., Poulin, R. and Blouin, M. S. ( 2005). Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Molecular Ecology 14, 22472257.CrossRefGoogle Scholar
Dieckmann, U. and Doebeli, M. ( 1999). On the origin of species by sympatric speciation. Nature, London 400, 354357.CrossRefGoogle Scholar
Doebeli, M. and Dieckmann, U. ( 2000). Evolutionary branching and sympatric speciation caused by different types of evolutionary interactions. American Naturalist 156, S77S101.CrossRefGoogle Scholar
Donald, K. M., Kennedy, M., Poulin, R. and Spencer, H. G. ( 2004). Host specificity and molecular phylogeny of larval Digenea isolated from New Zealand and Australian topshells (Gastropoda: Trochidae). International Journal for Parasitology 34, 557568.CrossRefGoogle Scholar
Drossel, B. and McKane, A. ( 2000). Competitive speciation in quantitative genetic models. Journal of Theoretical Biology 204, 467478.CrossRefGoogle Scholar
Esch, G. W., Bush, A. O. and Aho, J. M. ( 1990). Parasite Communities: Patterns and Processes. Chapman and Hall, London.
Galazzo, D. E., Dayanandan, S., Marcogliese, D. J. and McLaughlin, J. D. ( 2002). Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNA-sequence data and comparisons with European congeners. Canadian Journal of Zoology 80, 22072217.CrossRefGoogle Scholar
Gibson, D. I. and Bray, R. A. ( 1994). The evolutionary expansion and host-parasite relationship of the Digenea. International Journal for Parasitology 24, 12131226.CrossRefGoogle Scholar
Haas, W. and Haberl, B. ( 1997). Host recognition by trematode miracidia and cercariae. In Advances in Trematode Biology ( ed. Fried, B. and Graczyk, T. K.), pp. 197227. CRC Press LLC, Boca Raton.
Karvonen, A., Paukku, S., Valtonen, E. T. and Hudson, P. J. ( 2003). Transmission, infectivity and survival of Diplostomum spathaceum cercariae. Parasitology 127, 217224. DOI: 10.1017/S0031182003003561.CrossRefGoogle Scholar
Karvonen, A., Kirsi, S., Hudson, P. J. and Valtonen, E. T. ( 2004 a). Patterns of cercarial production from Diplostomum spathaceum: terminal investment or bet hedging? Parasitology 129, 8792. DOI: 10.1017/S0031182004005281.CrossRefGoogle Scholar
Karvonen, A., Seppälä, O. and Valtonen, E. T. ( 2004 b). Parasite resistance and avoidance behaviour in preventing eye fluke infections in fish. Parasitology 129, 159164. DOI: 10.1017/S0031182004005505.CrossRefGoogle Scholar
Karvonen, A., Seppälä, O. and Valtonen, E. T. ( 2004 c). Eye fluke-induced cataract formation in fish: quantitative analysis using an ophthalmological microscope. Parasitology 129, 473478. DOI: 10.1017/S0031182004006006.CrossRefGoogle Scholar
Karvonen, A., Paukku, S., Seppälä, O. and Valtonen, E. T. ( 2005). Resistance against eye flukes: naïve versus previously infected fish. Parasitology Research 95, 5559.CrossRefGoogle Scholar
Karvonen, A., Cheng, G.-H., Seppälä, O. and Valtonen, E. T. ( 2006). Intestinal distribution and fecundity of two species of Diplostomum parasites in definitive hosts. Parasitology 132, 357362.CrossRefGoogle Scholar
Kennedy, C. R. ( 2001). Interspecific interactions between larval digeneans in the eyes of perch, Perca fluviatilis. Parasitology 122 (Suppl.), S13S22.CrossRefGoogle Scholar
Koli, L. ( 1990). Suomen kalat. Werner Söderström Ltd, Porvoo (in Finnish).
Kondrashov, A. S. and Kondrashov, F. A. ( 1999). Interactions among quantitative traits in the course of sympatric speciation. Nature, London 400, 351354.CrossRefGoogle Scholar
Lello, J., Boag, B., Fenton, A., Stevenson, I. R. and Hudson, P. J. ( 2004). Competition and mutualism among the gut helminths of a mammalian host. Nature, London 428, 840844.CrossRefGoogle Scholar
Lively, C. M. and Jokela, J. ( 1996). Clinal variation for local adaptation in a host-parasite interaction. Proceedings of the Royal Society of London, B 263, 891897.CrossRefGoogle Scholar
Lively, C. M. and Dybdahl, M. F. ( 2000). Parasite adaptation to locally common host genotypes. Nature, London 405, 679681.CrossRefGoogle Scholar
Niewiadomska, K. ( 1986). Verification of the life-cycles of Diplostomum spathaceum (Rudolphi, 1819) and D. pseudospathaceum Niewiadomska, 1984 (Trematoda, Diplostomidae). Systematic Parasitology 8, 2331.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, London 425, 480484.CrossRefGoogle Scholar
Poulin, R. ( 1998). Evolutionary Ecology of Parasites: From Individuals to Communities. Chapman and Hall, London.
Poulin, R. and Mouillot, D. ( 2003). Parasite specialization from a phylogenetic perspective: a new index of host specificity. Parasitology 126, 473480.CrossRefGoogle Scholar
Rauch, G., Kalbe, M. and Reusch, T. B. H. ( 2005). How a complex life cycle can improve parasite's sex life. Journal of Evolutionary Biology 18, 10691075.CrossRefGoogle Scholar
Reusch, T. B. H., Rauch, G. and Kalbe, M. ( 2004). Polymorphic microsatellite loci for the trematode Diplostomum pseudospathaceum. Molecular Ecology Notes 4, 577579.CrossRefGoogle Scholar
Schluter, D. ( 2000). Ecological character displacement in adaptive radiation. American Naturalist 156, S4S16.CrossRefGoogle Scholar
Simberloff, D. and Moore, J. ( 1997). Community ecology of parasites and free-living animals. In Host-Parasite Evolution: General Principles and Avian Models ( ed. Clayton, D. H. and Moore, J.), pp. 174197. Oxford University Press, Oxford.
Sousa, W. P. ( 1994). Patterns and processes in communities of helminth parasites. Trends in Ecology and Evolution 9, 5257.CrossRefGoogle Scholar
Valtonen, E. T. and Gibson, D. I. ( 1997). Aspects of the biology of diplostomid metacercarial (Digenea) populations occurring in fishes in different localities in northern Finland. Annales Zoologici Fennici 34, 4759.Google Scholar
Valtonen, E. T., Holmes, J. C. and Koskivaara, M. ( 1997). Eutrophication, pollution, and fragmentation: effects on the parasite communities in roach (Rutilus rutilus) and perch (Perca fluviatilis) in four lakes in central Finland. Canadian Journal of Fisheries and Aquatic Science 54, 572585.CrossRefGoogle Scholar
Valtonen, E. T., Holmes, J. C., Aronen, J. and Rautalahti, I. ( 2003). Parasite communities as indicators of recovery from pollution: parasites of roach (Rutilus rutilus) and perch (Perca fluviatilis) in Central Finland. Parasitology 126 (Suppl.), S43S52. DOI: 10.1017/S0031182003003494.CrossRefGoogle Scholar
Williams, M. O. ( 1966). Studies on the morphology and life-cycle of Diplostomum (Diplostomum) gasterostei (Strigeida: Trematoda). Parasitology 56, 693706.CrossRefGoogle Scholar