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Broad geographic analyses reveal varying patterns of genetic diversity and host specificity among echinostome trematodes in New Zealand snails

Published online by Cambridge University Press:  26 August 2014

DEVON B. KEENEY ,
JASON PALLADINO  and
ROBERT POULIN
DEVON B. KEENEY*
Affiliation:
Department of Biological Sciences, Le Moyne College, 1419 Salt Springs Road, Syracuse, New York 13214-1301, USA
JASON PALLADINO
Affiliation:
Department of Biological Sciences, Le Moyne College, 1419 Salt Springs Road, Syracuse, New York 13214-1301, USA
ROBERT POULIN
Affiliation:
Department of Zoology, University of Otago, PO Box 56, Dunedin, New Zealand
*
*Corresponding author: Department of Biological Sciences, Le Moyne College, 1419 Salt Springs Road, Syracuse, New York 13214-1301, USA. E-mail: keeneydb@lemoyne.edu
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Summary

Host specificity is a fundamental component of a parasite's life history. However, accurate assessments of host specificity, and the factors influencing it, can be obscured by parasite cryptic species complexes. We surveyed two congeneric species of intertidal snail intermediate hosts, Zeacumantus subcarinatus and Zeacumantus lutulentus, throughout New Zealand to identify the number of genetically distinct echinostome trematodes infecting them and determine the levels of snail host specificity among echinostomes. Two major echinostome clades were identified: a clade consisting of an unidentified species of the subfamily Himasthlinae and a clade consisting of five species of the genus Acanthoparyphium. All five Acanthoparyphium species were only found in a single snail species, four in Z. subcarinatus and one in Z. lutulentus. In contrast, the Himasthlinae gen. sp. was found in both hosts, but was more prevalent in Z. lutulentus (97 infections) than Z. subcarinatus (10 infections). At least two of the Acanthoparyphium spp. and the Himasthlinae gen. sp. are widespread throughout New Zealand, and can therefore encounter both snail species. Our results suggest that host specificity is determined by host–parasite incompatibilities, not geographic separation, and that it can evolve in different ways in closely related parasite lineages.

Keywords

host specificitytrematodeechinostomeZeacumantusAcanthoparyphiumCOIITS1
Type
Research Article
Information
Parasitology , Volume 142 , Issue 2 , February 2015 , pp. 406 - 415
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Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Adamson, M. L. and Caira, J. N. (1994). Evolutionary factors influencing the nature of parasite specificity. Parasitology 109, S85–S95.Google Scholar
Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.Google Scholar
Antonovics, J., Boots, M., Ebert, D., Koskella, B., Poss, M. and Sadd, B. M. (2013). The origin of specificity by means of natural selection: evolved and nonhost resistance in host–pathogen interactions. Evolution 67, 1–9.Google Scholar
Blair, D., Davis, G. M. and Wu, B. (2001). Evolutionary relationships between trematodes and snails emphasizing schistosomes and paragonimids. Parasitology 123, S229–S243.Google Scholar
Blasco-Costa, I. and Poulin, R. (2013). Host traits explain the genetic structure of parasites: a meta-analysis. Parasitology 140, 1316–1322.CrossRefGoogle ScholarPubMed
Blasco-Costa, I., Balbuena, J. A., Raga, J. A., Kostadinova, A. and Olson, P. D. (2010). Molecules and morphology reveal cryptic variation among digeneans infecting sympatric mullets in the Mediterranean. Parasitology 137, 287–302.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.Google Scholar
Bowles, J., Blair, B. and McManus, D. P. (1995). A molecular phylogeny of the human schistosomes. Molecular Phylogenetics and Evolution 4, 103–109.CrossRefGoogle ScholarPubMed
Brant, S. V. and Orti, G. (2003). Evidence for gene flow in parasitic nematodes between two host species of shrews. Molecular Ecology 12, 2853–2859.CrossRefGoogle ScholarPubMed
Combes, C. (2001). Parasitism: The Ecology and Evolution of Intimate Interactions. University of Chicago Press, Chicago, IL, USA.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
Curran, S. S., Tkach, V. V. and Overstreet, R. M. (2013). Molecular evidence for two cryptic species of Homalometron (Digenea: Apocreadiidae) in freshwater fishes of the southeastern United States. Comparative Parasitology 80, 186–195.Google Scholar
Detwiler, J. T., Bos, D. H. and Minchella, D. J. (2010). Revealing the secret lives of cryptic species: examining the phylogenetic relationships of echinostome parasites in North America. Molecular Phylogenetics and Evolution 55, 611–620.Google Scholar
Detwiler, J. T., Zajac, A. M., Minchella, D. J. and Belden, L. K. (2012). Revealing cryptic parasite diversity in a definitive host: echinostomes in muskrats. Journal of Parasitology 98, 1148–1155.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.Google Scholar
Dunn, R. R., Harris, N. C., Colwell, R. K., Koh, L. P. and Sodhi, N. S. (2009). The sixth mass extinction: are most endangered species parasites and mutualists? Proceedings of the Royal Society B 276, 3037–3045.CrossRefGoogle ScholarPubMed
Excoffier, L., Laval, G. and Schneider, S. (2005). Arlequin ver. 3·0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.Google Scholar
Gibson, D. I. and Bray, R. A. (1994). The evolutionary expansion and host–parasite relationships of the Digenea. International Journal for Parasitology 24, 1213–1226.Google Scholar
Hayward, A. (2010). Cryptic diversity and patterns of host specificity in trematode flatworms. Molecular Ecology 19, 2602–2604.Google Scholar
Keeney, D. B., Szymaniak, A. D. and Poulin, R. (2013). Complex genetic patterns and a phylogeographic disjunction among New Zealand mud snails Zeacumantus subcarinatus and Z. lutulentus . Marine Biology 160, 1477–1488.Google Scholar
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
Leung, T. L. F., Donald, K. M., Keeney, D. B., Koehler, A. V., Peoples, R. C. and Poulin, R. (2009 a). Trematode parasites of Otago Harbour (New Zealand) soft-sediment intertidal ecosystems: life cycles, ecological roles and DNA barcodes. New Zealand Journal of Marine and Freshwater Research 43, 857–865.Google Scholar
Leung, T. L. F., Keeney, D. B. and Poulin, R. (2009 b). Cryptic species complexes in manipulative echinostomatid trematodes: when two become six. Parasitology 136, 241–252.Google Scholar
Locke, S. A., McLaughlin, J. D. and Marcogliese, D. J. (2010). DNA barcodes show cryptic diversity and a potential physiological bias for host specificity among Diplostomoidea (Platyhelminthes: Digenea) parasitizing freshwater fishes in the St. Lawrence River, Canada. Molecular Ecology 19, 2813–2827.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
McCarthy, A. M. (1990). Speciation of echinostomes: evidence for the existence of two sympatric sibling species in the complex Echinoparyphium recurvatum (von Linstow) (Digenea: Echinostomatidae). Parasitology, 101, 35–42.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.Google Scholar
Morton, J. (2004). Seashore Ecology of New Zealand and the Pacific. David Bateman Ltd., Auckland, New Zealand.Google Scholar
Morton, J. and Miller, M. (1968). The New Zealand Sea Shore. Collins, Auckland, New Zealand.Google Scholar
Ozawa, T., Köhler, F., Reid, D. G. and Glaubrecht, M. (2009). Tethyan relicts on continental coastlines of the northwestern Pacific Ocean and Australasia: molecular phylogeny and fossil record of batillariid gastropods (Caenogastropoda, Cerithioidea). Zoologica Scripta 38, 503–525.CrossRefGoogle Scholar
Pearson, J. C. (1972). A phylogeny of life-cycle patterns of the Digenea. Advances in Parasitology 58, 760–788.Google Scholar
Peoples, R. C., Randhawa, H. S. and Poulin, R. (2012). Parasites of polychaetes and their impact on host survival in Otago Harbour, New Zealand. Journal of the Marine Biological Association of the United Kingdom 92, 449–455.Google Scholar
Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.Google Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn. Princeton University Press, Princeton, NJ, USA.Google Scholar
Poulin, R. (2011). Uneven distribution of cryptic diversity among higher taxa of parasitic worms. Biology Letters 7, 241–244.Google Scholar
Poulin, R. and Keeney, D. B. (2008). Host specificity under molecular and experimental scrutiny. Trends in Parasitology 24, 24–28.CrossRefGoogle ScholarPubMed
Poulin, R., Krasnov, B. R. and Mouillot, D. (2011). Host specificity in phylogenetic and geographic space. Trends in Parasitology 27, 355–361.CrossRefGoogle ScholarPubMed
Rambaut, A. (2009). FigTree v1.3.1. Available from http://tree.bio.ed.ac.uk/.Google Scholar
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A. and Huelsenbeck, J. P. (2012). MrBayes 3·2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.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 Scholar
Sukumaran, J. and Holder, M. T. (2010). DendroPy: a Python library for phylogenetic computing. Bioinformatics 26, 1569–1571.Google Scholar
Tamura, K. and Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512–526.Google ScholarPubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.Google Scholar
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, 839–846.Google Scholar
Yamaguti, S. (1975). A Synoptical Review of Life Histories of Digenetic Trematodes of Vertebrates, with a Special Reference to the Morphology of their Larval Forms. Keigaku Publishing Co., Tokyo, Japan.Google Scholar
Zwickl, D. J. (2006). Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. dissertation. The University of Texas, Austin, USA.Google Scholar