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Host and ecology both play a role in shaping distribution of digenean parasites of New Zealand whelks (Gastropoda: Buccinidae: Cominella)

Published online by Cambridge University Press:  09 June 2016

KIRSTEN M. DONALD  and
HAMISH G. SPENCER
KIRSTEN M. DONALD*
Affiliation:
Department of Zoology, Allan Wilson Centre, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
HAMISH G. SPENCER
Affiliation:
Department of Zoology, Allan Wilson Centre, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
*
*Corresponding author: Department of Zoology, Allan Wilson Centre, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand. Tel: 00 64 3 479 5096. Fax: 00 64 3 479 7584. E-mail: kirsten.donald@otago.ac.nz
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Summary

Digenean parasites infecting four Cominella whelk species (C. glandiformis, C. adspersa, C. maculosa and C. virgata), which inhabit New Zealand's intertidal zone, were analysed using molecular techniques. Mitochondrial 16S and cytochrome oxidase 1 (COI) and nuclear rDNA ITS1 sequences were used to infer phylogenetic relationships amongst digenea. Host species were parasitized by a diverse range of digenea (Platyhelminthes, Trematoda), representing seven families: Echinostomatidae, Opecoelidae, Microphallidae, Strigeidae and three, as yet, undetermined families A, B and C. Each parasite family infected between one and three host whelk species, and infection levels were typically low (average infection rates ranged from 1·4 to 3·6%). Host specificity ranged from highly species-specific amongst the echinostomes, which were only ever observed infecting C. glandiformis, to the more generalist opecoelids and strigeids, which were capable of infecting three out of four of the Cominella species analysed. Digeneans displayed a highly variable geographic range; for example, echinostomes had a large geographic range stretching the length of New Zealand, from Northland to Otago, whereas Family B parasites were restricted to fairly small areas of the North Island. Our results add to a growing body of research identifying wide ranges in both host specificity and geographic range amongst intertidal, multi-host parasite systems.

Keywords

Cominelladigeneageographic rangehost specificity
Type
Research Article
Information
Parasitology , Volume 143 , Issue 9 , August 2016 , pp. 1143 - 1156
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Copyright
Copyright © Cambridge University Press 2016 

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Footnotes

Nucleotide sequence data reported in this paper are available in the GenBank, EMBL and DDBJ databases under accession numbers KU525036-KU525077, KU695753-KU695802 and KU748678-748725.

References

REFERENCES

Abdul-Salam, J. and Al-Khedery, B. (1992). The occurrence of larval Digenea in some snails in Kuwait Bay. Hydrobiologia 248, 161–165.Google Scholar
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.Google Scholar
Anderson, D. (1960). The life-histories of marine prosobranch molluscs. Journal of the Malacological Society of Australia 4, 16–29.Google Scholar
Bowles, J. and McManus, D. P. (1993). Rapid discrimination of Echinococcus species and strains using a PCR-based RFLP method. Molecular Biochemistry and Parasitology 57, 231–239.Google Scholar
Carrasco, S. A., Phillips, N. E. and Perez-Matus, A. (2012). Offspring size and maternal environments mediate the early juvenile performance of two congeneric whelks. Marine Ecology Progress Series 459, 73–83.CrossRefGoogle Scholar
Charleston, M. A. (1998). Jungles: a new solution to the host/parasite phylogeny reconciliation problem. Mathematical Biosciences 149, 191–223. http://dx.doi.org/10.1016/S0025-5564(97)10012-8.Google Scholar
Charleston, M. A., and Perkins, S. L. (2002 a). Lizards, malaria, and jungles in the Caribbean. In Tangled Trees: Phylogeny, Cospeciation and Coevolution (ed. Page, R. D. M.), pp. 65–92. University of Chicago Press, Chicago.Google Scholar
Charleston, M. A. and Robertson, D. L. (2002 b). Preferential host switching by primate lentiviruses can account for phylogenetic similarity with the primate phylogeny. Systematic Biology 51, 528–535.Google Scholar
Clayton, D. A. (1986). Ecology of mudflats with particular reference to those of the northern Arabian Gulf. In Marine Environment and Pollution (eds. Halwagy, R., Clayton, D. A., Behbehani, M.), pp. 83–86. Kuwait University, Kuwait. Proceedings of the First Arabian Gulf Conference on Environment and Pollution, Kuwait, 7–9 February, 1982.Google Scholar
Criscione, C. D. and Blouin, M. S. (2004). Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evolution 58, 198–202.Google 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 of Parasitology 34, 557–568.Google Scholar
Donald, K. M., Winter, D. J., Ashcroft, A. L. and Spencer, H. G. (2015). Phylogeography of the whelk genus Cominella (Gastropoda, Buccinidae) suggests long-distance counter-current dispersal of a direct developer. Biological Journal of the Linnean Society 115, 315–332.Google Scholar
Farris, J. S., Källersjö, M., Kluge, A. G. and Bult, C. (1995). Constructing a significance test for incongruence. Systematic Biology 44, 570–572.Google Scholar
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.CrossRefGoogle ScholarPubMed
Gustafsson, D. R. and Olsson, U. (2012). Flyaway homogenisation or differentiation? Insights from the phylogeny of the sandpiper (Charadriiformes: Scolopacidae: Calidrinae) wing louse genus Lunaceps (Phthiraptera: Ischnoceras). International Journal for Parasitology 42, 93–102.CrossRefGoogle ScholarPubMed
Hafner, M. S. and Nadler, S. A. (1988). Phylogenetic trees support the coevolution of parasites and their hosts. Nature 332, 258–259.Google Scholar
Hechinger, R. F. and Lafferty, K. D. (2005). Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society B 272, 1059–1066.Google Scholar
Huelsenbeck, J. P. and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 654–755.Google Scholar
Irwin, S. W. B. (1983). Incidence of trematode parasites in two populations of Littorina saxatilis (Olivi) from the North Shore of Belfast Lough. Irish Naturalists Journal 21, 26–29.Google Scholar
Johnson, K. P., Adams, R. J. and Clayton, D. H. (2002). The phylogeny of the louse genus Brueelia does not reflect host phylogeny. Biological Journal of the Linnean Society 77, 233–247.Google Scholar
Jousson, O., Bartoli, P. and Pawlowski, J. (2000). Cryptic speciation among intestinal parasites (Trematoda: Digenea) infecting sympatric host fishes (Sparidae). Journal of Evolutionary Biology 13, 778–785.Google Scholar
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.Google Scholar
Králová-Hromadová, I., Špakulová, M., Horácková, E., Turceková, L., Novobilsky, A., Beck, R., Koudela, B., Marinculic, A., Rajsky, D. and Pybus, M. (2001). Sequence analysis of ribosomal and mitochondrial genes of the giant liver fluke Fascioloides magna (Trematoda: Fasciolidae): intraspecific variation and differentiation from Fasciola hepatica . Journal of Parasitology 94, 58–67.Google Scholar
Leung, T. L. F., Keeney, D. B. and Poulin, R. (2009 a). Cryptic species complexes in manipulative echinostomatid trematodes: when two become six. Parasitology 136, 241–252.Google Scholar
Leung, T. L. F., Donald, K. M., Keeney, D. B., Koehler, A. V., Peoples, R. C. and Poulin, R. (2009 b). 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
Lively, C. M. and Jokela, J. (1996). Clinical variation for local adaptation in the host-parasite interaction. Proceedings of the Royal Society of London B 263, 891–897.Google Scholar
Marcogliese, D. J. and Cone, D. K. (1997). Food webs: a plea for parasites. Trends in Ecology and Evolution 12, 320–325.CrossRefGoogle ScholarPubMed
Martinů, J., Sychra, O., Literák, I., Čapek, M., Gustafsson, D. L. and Štefka, J. (2015). Host generalists and specialists emerging side by side: an analysis of evolutionary patterns in the cosmopolitan chewing louse genus Menacanthus . International Journal for Parasitology 45, 63–73.CrossRefGoogle ScholarPubMed
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.Google 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.Google Scholar
Mouritsen, K. N. and Poulin, R. (2002). Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124, S101–S117.Google Scholar
Paterson, A. M., Gray, R. D. and Wallis, G. P. (1993). Parasites, petrels and penguins: does louse presence reflect seabird phylogeny? International Journal for Parasitology 23, 515–526.Google Scholar
Paterson, A. M., Wallis, G. P., Wallis, L. J. and Gray, R. D. (2000). Seabird and louse coevolution: complex histories revealed by 12S rRNA sequences and reconciliation analyses. Systematic Biology 49, 383–399.Google Scholar
Posada, D. and Crandall, K. A. (1998). Modeltest: Testing the model of DNA substitution. Bioinformatics 14, 817–818.Google Scholar
Poulin, R. (2006). Variation in infection parameters among populations within parasite species: Intrinsic properties versus local factors. International Journal for Parasitology, 36, 877–885.Google Scholar
Poulin, R. and Mouritsen, K. N. (2003). Large-scale determinants of trematode infections in intertidal gastropods. Marine Ecology Progress Series 254, 187–198.Google Scholar
Raffaelli, D. (2000). Trends in research on shallow water food webs. Journal of Experimental Marine Biology and Ecology 250, 223–232.Google Scholar
Refrégier, G., Le Gac, M., Jabbour, F., Widner, A., Shykoff, J. A., Yockteng, R., Hood, M. A. and Giraud, T. (2008). Cophylogeny of the anther smut fungi and their caryophyllaceous hosts: prevalence of host shifts and importance of delimiting parasite species for inferring cospeciation. BMC Evolutionary Biology 8, 100.CrossRefGoogle ScholarPubMed
Sousa, W.P. (1991). Can models of soft-sediment community structure be complete without parasites. American Zoologist 31, 821–830.CrossRefGoogle Scholar
Swofford, D. L. (2002). PAUP - Phylogenetic Analysis Using Parsimony. Ver. 4. [Computer software and manual]. Sinauer Associates, Sunderland, MA, USA.Google Scholar
Walsh, P. S., Metzger, D. A. and Higuchi, R. (1991). Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10, 506–513.Google Scholar
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