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Cryptic species complexes in manipulative echinostomatid trematodes: when two become six

Published online by Cambridge University Press:  18 December 2008

T. L. F. LEUNG ,
D. B. KEENEY  and
R. POULIN
T. L. F. LEUNG*
Affiliation:
Department of Zoology, University of Otago, P. O. Box 56, Dunedin 9054, New Zealand
D. B. KEENEY
Affiliation:
Department of Zoology, University of Otago, P. O. Box 56, Dunedin 9054, New Zealand Department of Biological Sciences, Le Moyne College, 1419 Salt Springs Road, Syracuse, New York13214-1301, USA
R. POULIN
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, Dunedin9054, New Zealand. Tel: +64 3 479 7964. Fax: +64 3 479 7584. E-mail: [email protected]
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Summary

Recent studies have shown that some digenean trematodes previously identified as single species due to the lack of distinguishing morphological characteristics actually consist of a number of genetically distinct cryptic species. We obtained mitochondrial 16S and nuclear ITS1 sequences for the redial stages of Acanthoparyphium sp. and Curtuteria australis collected from snails and whelks at various locations around Otago Peninsula, New Zealand. These two echinostomes are well-known host manipulators whose impact extends to the entire intertidal community. Using phylogenetic analyses, we found that Acanthoparyphium sp. is actually composed of at least 4 genetically distinct species, and that a cryptic species of Curtuteria occurs in addition to C. australis. Molecular data obtained for metacercariae dissected from cockle second intermediate hosts matched sequences obtained for Acanthoparyphium sp. A and C. australis rediae, respectively, but no other species. The various cryptic species of both Acanthoparyphium and Curtuteria also showed an extremely localized pattern of distribution: some species were either absent or very rare in Otago Harbour, but reached far higher prevalence in nearby sheltered inlets. This small-scale spatial segregation is unexpected as shorebird definitive hosts can disperse trematode eggs across wide geographical areas, which should result in a homogeneous mixing of the species on small geographical scales. Possible explanations for this spatial segregation of the species include sampling artefacts, local adaptation by first intermediate hosts, environmental conditions, and site fidelity of the definitive hosts.

Keywords

cryptic speciesphylogenyEchinostomatidae16SITS1spatial segregation
Type
Research Article
Information
Parasitology , Volume 136 , Issue 2 , February 2009 , pp. 241 - 252
Copyright
Copyright © 2008 Cambridge University Press

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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, 13–20.CrossRefGoogle Scholar
Babirat, C., Mouritsen, K. N. and Poulin, R. (2004). Equal partnership: two trematode species, not one, manipulate the burrowing behaviour of the New Zealand cockle, Austrovenus stutchburyi. Journal of Helminthology 78, 195–199.CrossRefGoogle Scholar
Bayne, C. J., Hahn, U. K. and Bender, R. C. (2001). Mechanisms of molluscan host resistance and of parasite strategies for survival. Parasitology 123, S159–S167.CrossRefGoogle ScholarPubMed
Beauchamp, K. A., Gay, M., Kelley, G. O., El-Matbouli, M., Kathman, R. D., Nehring, R. B. and Hedrick, R. P. (2002). Prevalence and susceptibility of infection to Myxobolus cerebalis, and genetic differences among populations of Tubifex tubifex. Diseases of Aquatic Organisms 51, 113–121.CrossRefGoogle ScholarPubMed
Bickford, D., Lohman, D. J., Sodhi, N. S., Ng, P. K. L., Meier, R., Winker, K., Ingram, K. K. and Das, I. (2006). Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22, 148–155.CrossRefGoogle ScholarPubMed
Bidochka, M. J., Kamp, A. M., Lavender, T. M., Dekoning, J. and de Croos, J. N. A. (2001). Habitat association in two genetic groups of the insect-pathogenic fungus Metarhizium anisopliae: uncovering cryptic species? Applied and Environmental Microbiology 67, 1335–1342.CrossRefGoogle ScholarPubMed
Bowles, J. and McManus, D. P. (1993). Rapid discrimination of Echinococcus species and strains using a polymerase chain reaction-based RFLP method. Molecular and Biochemical Parasitology 57, 231–240.CrossRefGoogle ScholarPubMed
Byers, J. E., Blakeslee, A. M. H., Linder, E., Cooper, A. B. and Maguire, T. J. (2008). Control of spatial variation in prevalence of trematode parasites infecting a marine snail. Ecology 89, 439–451.CrossRefGoogle ScholarPubMed
Cepicka, I., Kutišova, K., Tachezy, J., Kulda, J. and Flegr, J. (2005). Cryptic species within the Tetratrichomonas gallinarum species complex revealed by molecular polymorphism. Veterinary Parasitology 128, 11–21.CrossRefGoogle ScholarPubMed
Criscione, C. D. and Blouin, M. S. (2004). Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evolution 58, 198–202.Google ScholarPubMed
De Montaudouin, X., Jensen, K. T., Desclaux, C., Wegeberg, A. M. and Sajus, M. C. (2005). Effect of intermediate host size (Cerastoderma edule) on infectivity of cercariae of Himasthla quissetensis (Echinostomatidae: Trematoda). Journal of the Marine Biological Association of the United Kingdom 85, 809–812.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, 557–568.CrossRefGoogle ScholarPubMed
Donald, K. M., Sijnja, A. and Spencer, H. G. (2007). Species assignation amongst morphologically cryptic larval Digenea isolated from New Zealand topshells (Gastropoda: Trochidae). Parasitology Research 101, 433–441.CrossRefGoogle ScholarPubMed
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the boostrap. Evolution 39, 783–791.CrossRefGoogle Scholar
Finn, P. G., Catterall, C. P. and Driscoll, P. V. (2007). Determinants of preferred intertidal feeding habitat for Eastern Curlew: a study at two spatial scales. Austral Ecology 32, 131–144.CrossRefGoogle Scholar
Fredensborg, B. L. and Poulin, R. (2006). Parasitism shaping host life-history evolution: adaptive responses in a marine gastropod to infection by trematodes. Journal of Animal Ecology 75, 44–53.CrossRefGoogle Scholar
Fredensborg, B. L., Mouritsen, K. N. and Poulin, R. (2006). Relating bird host distribution and spatial heterogeneity in trematode infections in an intertidal snail – from small to large scale. Marine Biology 149, 275–283.CrossRefGoogle Scholar
Gibson, D. I. and Bray, R. A. (1994). The evolutionary expansion and host-parasite relationships of Digenea. International Journal for Parasitology 24, 1213–1226.CrossRefGoogle ScholarPubMed
Geller, J. B. (1999). Decline of a native mussel masked by sibling species invasion. Conservation Biology 13, 661–664.CrossRefGoogle Scholar
Geller, J. B., Walton, E. D., Grosholz, E. D. and Ruiz, G. M. (1997). Cryptic invasions of the crab Carcinus detected by molecular phylogeography. Molecular Ecology 6, 901–906.CrossRefGoogle ScholarPubMed
Hechinger, R. F. and Lafferty, K. D. (2005). Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate host. Proceedings of the Royal Society of London, B 272, 1059–1066.Google Scholar
Huelsenbeck, J. P. and Ronquist, F. (2001) MARBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.CrossRefGoogle ScholarPubMed
Iribarne, O., Bruschetti, M., Escapa, M., Bava, J., Botto, F., Gutierrez, J., Palomo, G., Delhey, K., Petracci, P. and Gagliardini, A. (2005). Small- and large-scale effect of the SW Atlantic burrowing crab Chasmagnathus granulatus on habitat use by migratory shorebirds. Journal of Experimental Marine Biology and Ecology 315, 87–101.CrossRefGoogle Scholar
Jing, K., Ma, Z., Li, B., Li, J. and Chen, J. (2007). Foraging strategies involved in habitat use of shorebirds at the intertidal area of Chongming Dongtan, China. Ecological Research 22, 559–570.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, 183–190.CrossRefGoogle Scholar
Kimura, M. (1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.CrossRefGoogle ScholarPubMed
Koprivnikar, J., Baker, R. L. and Forbes, M. R. (2007). Environmental factors influencing community composition of gastropods and their trematode parasites in southern Ontario. Journal of Parasitology 93, 992–998.CrossRefGoogle ScholarPubMed
Kostadinova, A. (2005) Family Echinostomatidae Looss, 1899. In Keys to the Trematoda, Vol. 2, (ed. Jones, A., Bray, R. A. and Gibson, D. I.), pp. 9–64. CABI Publishing, Oxford, UK.Google Scholar
Kumar, S., Tamura, K. and Nei, M. (2004). MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.CrossRefGoogle ScholarPubMed
Leung, T. L. F. and Poulin, R. (2007). Interactions between parasites of the cockle Austrovenus stutchburyi: Hitch-hikers, resident-cleaners, and habitat-facilitators. Parasitology 134, 247–255.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, 177–180.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, 891–897.Google Scholar
Martorelli, S. R., Fredensborg, B. L., Mouritsen, K. N. and Poulin, R. (2004). Description and proposed life cycle of Maritrema novaezealandensis n. sp. (Microphallidae) parasitic in red-billed gulls, Larus novaehollandiae scopulinus, from Otago Harbor, South Island, New Zealand. Journal of Parasitology 90, 272–277.CrossRefGoogle Scholar
Martorelli, S. R., Fredensborg, B. L., Leung, T. L. F. and Poulin, R. (2008). Four trematode cercariae from the New Zealand intertidal snail Zeacumantus subcarinatus (Batillariidae). New Zealand Journal of Zoology 35, 73–84.CrossRefGoogle Scholar
Martorelli, S. R., Poulin, R. and Mouritsen, K. N. (2006). A new cercaria and metacercaria of Acanthoparyphium (Echinostomatidae) found in an intertidal snail Zeacumantus subcarinatus (Batillaridae) from New Zealand. Parasitology International 55, 163–167.CrossRefGoogle Scholar
Miura, O., Kuris, A. M., Torchin, M. E., Hechinger, R. F., Dunham, E. J. and Chiba, S. (2005). Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse). International Journal for Parasitology 35, 793–801.CrossRefGoogle ScholarPubMed
Miura, O., Torchin, M. E., Kuris, A. M., Hechinger, R. F. and Chiba, S. (2006). Introduced cryptic species of parasites exhibit different invasion pathways. Proceedings of the National Academy of Sciences, USA 103, 19818–19823.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, 521–528.CrossRefGoogle ScholarPubMed
Mouritsen, K. N. and Jensen, K. T. (1992). Choice of microhabitat in tactile foraging dunlins Calidris alpine: importance of sediment penetrability. Marine Ecology Progress Series 85, 1–8.CrossRefGoogle Scholar
Mouritsen, K. N. and Poulin, R. (2002). Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124, S101–S117.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Mouritsen, K. N. and Poulin, R. (2005). Parasites boost biodiversity and change animal community structure by trait-mediated indirect effects. Oikos 108, 344–350.CrossRefGoogle Scholar
Nolan, M. J. and Cribb, T. H. (2005). The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Advances in Parasitology 60, 101–163.CrossRefGoogle ScholarPubMed
Olson, P. D., Cribb, T. H., Tkach, V. V., Bray, R. A. and Littlewood, D. T. J. (2003). Phylogeny and classification of the Digenea. International Journal for Parasitology 33, 733–755.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.CrossRefGoogle ScholarPubMed
Pilkington, M. C. (1974). The eggs and hatching stages of some New Zealand prosobranch molluscs. Journal of the Royal Society of New Zealand 4, 411–431.CrossRefGoogle Scholar
Posada, D. and Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle ScholarPubMed
Pringle, A., Baker, D. M., Platt, J. L., Ware, J. P., Latgé, J. P. and Taylor, J. W. (2005). Cryptic speciation in the cosmopolitan and clonal human pathogenic fungus Aspergillus fumigatus. Evolution 59, 1886–1899.Google ScholarPubMed
Rafter, M. A., Gillions, R. M. and Walter, G. H. (2008). Generalist herbivore in weed biological control – a natural experiment with reportedly polyphagous thrips. Biological Control 44, 188–195.CrossRefGoogle Scholar
Ribeiro, P. O., Iribarne, O. O., Navarro, D. and Jaureguy, L. (2004). Environmental heterogeneity, spatial segregation of prey, and the utilization of southwest Atlantic mudflats by migratory shorebirds. Ibis 146, 672–682.CrossRefGoogle Scholar
Saijuntha, W., Sithithaworn, P., Wongkham, S., Laha, T., Pipitgool, V., Tesana, S., Chilton, N. B., Petney, T. N. and Andrews, R. H. (2007). Evidence of a species complex within the food-borne trematode Opisthorchis viverrini and possible co-evolution with their first intermediate hosts. International Journal for Parasitology 37, 695–703.CrossRefGoogle ScholarPubMed
Sapp, K. K. and Loker, E. S. (2000). Mechanisms underlying digenean-snail specificity: role of miracidial attachment and host plasma factors. Journal of Parasitology 86, 1012–1019.Google ScholarPubMed
Skobgaard, K., Bødker, L. and Rosendahl, S. (2002). Population structure and pathogenicity of members of the Fusarium oxysporum complex isolated from soil and root necrosis of pea (Pisum sativum L.). FEMS Microbiology Ecology 42, 367–374.CrossRefGoogle Scholar
Smith, N. F. (2001). Spatial heterogeneity in recruitment of larval trematodes to snail intermediate hosts. Oecologia 127, 115–122.CrossRefGoogle ScholarPubMed
Swofford, D. L. (2002). PAUP – Phylogenetic Analysis Using Parsimony. Ver. 4. [Computer software and manual]. Sinauer Associates, Sunderland, MA, USA.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.CrossRefGoogle ScholarPubMed
Thomas, F., and Poulin, R. (1998). Manipulation of a mollusc by a trophically transmitted parasite: convergent evolution or phylogenetic inheritance? Parasitology 116, 431–436.CrossRefGoogle ScholarPubMed
Thomas, F., Renaud, F., de Meeüs, T. and Poulin, R. (1998 a). Manipulation of host behaviour by parasites: ecosystem engineering in the intertidal zone? Proceedings of the Royal Society of London, B 265, 1091–1096.CrossRefGoogle Scholar
Thomas, F., Renaud, F. and Poulin, R. (1998 b). Exploitation of manipulators: ‘hitch-hiking’ as a parasite transmission strategy. Animal Behaviour 56, 199–206.CrossRefGoogle ScholarPubMed
Vilas, R., Criscione, C. D. and Blouin, M. S. (2005). A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites. Parasitology 131, 1–8.CrossRefGoogle ScholarPubMed
Walter, D. E. and Campbell, N. J. H. (2003). Exotic vs endemic biocontrol agents: would the real Stratiolaelaps miles (Berlese) (Acari: Mesostigmata: Laelapidae), please stand up? Biological Control 26, 253–269.CrossRefGoogle Scholar
Wegeberg, A. M., de Montaudouin, X. and Jensen, K. T. (1999). Effect of intermediate host size (Cerastoderma edule) on infectivity of cercariae of three Himasthla species (Echinostomatidae, Trematoda). Journal of Experimental Marine Biology and Ecology 238, 259–269.CrossRefGoogle Scholar
Whitney, K. L., Hechinger, R. F., Kuris, A. M. and Lafferty, K. D. (2007). Endangered light-footed clapper rail affects parasite community structure in coastal wetlands. Ecological Applications 17, 1694–1702.CrossRefGoogle ScholarPubMed
Williams, J. A. and Esch, G. W. (1991). Infra- and component community dynamics in the pulmonate snail Helisoma anceps, with special emphasis on the hemiurid trematode Halipegus occidualis. Journal of Parasitology 77, 246–253.CrossRefGoogle Scholar
Wood, C. L., Byers, J. E., Cottingham, K. L., Altman, I., Donahue, M. J. and Blakeslee, A. M. H. (2007). Parasites alter community structure. Proceedings of the National Academy of Sciences, USA 104, 9335–9339.CrossRefGoogle ScholarPubMed