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New species of Plagioporus Stafford, 1904 (Digenea: Opecoelidae) from California, with an amendment of the genus and a phylogeny of freshwater plagioporines of the Holarctic

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Abstract

Plagioporus hageli n. sp. is described from the intestine of Oncorhynchus mykiss (Walbaum) collected from the River Yuba, California, USA. Of the accepted, nominal species of Plagioporus Stafford, 1904 from the Nearctic, the new species is morphologically similar to three intestinal species from the western USA parasitising diadromous fishes, including Plagioporus shawi (McIntosh, 1939), Plagioporus kolipinskii Tracey, Choudhury, Cheng & Ghosh, 2009 and Plagioporus siliculus Sinitsin, 1931, and is also similar to Plagioporus serotinus Stafford, 1904 from catostomids from eastern Canada. Plagioporus hageli n. sp. is distinguished from the former three species in lacking a dorsal vitelline field and from the latter species in having a consistent interruption in the distribution of the vitellarium at the level of the ventral sucker. The new species is also morphologically similar to an unnamed species of Plagioporus and a species misidentified as ‘Plagioporus angusticolle’ that were collected from California, but it is easily distinguished from both in its shorter body length. To estimate the placement of the new species within Plagioporus and within the Opecoelidae Ozaki, 1925, we conducted a Bayesian inference (BI) analysis of partial 28S rDNA sequence data that included sequences from Plagioporus hageli n. sp., five other species of Plagioporus, three species of Neoplagioporus Shimazu, 1990, including the type-species, Neoplagioporus zacconis (Yamaguti, 1934), two species of Urorchis Ozaki, 1927 (including the type-species, Urorchis goro Ozaki, 1927) and sequences of 42 opecoelid species obtained from GenBank. Our phylogenetic analysis revealed (i) plagioporines parasitising freshwater hosts form a monophyletic group; (ii) Plagiocirrus loboides Curran, Overstreet & Tkach, 2007 nested within the rest of the members of Plagioporus; (iii) the new species was closer to Plagiocirrus loboides than to Plagioporus shawi, the other salmonid parasite included in our analysis; (iv) P. shawi was the poorly supported sister to its congeners; (v) Neoplagioporus elongatus (Goto & Ozaki, 1930) Shimazu, 1990 was closer to the two species of Urorchis than to the other two species of Neoplagioporus; and (vi) the paraphyly of the Plagioporinae Manter, 1947 was reinforced. Based on 28S rDNA sequence data and our BI analysis, we propose Plagioporus loboides (Curran, Overstreet & Tkach, 2007) n. comb., and amend Plagioporus accordingly. This analysis represents the first phylogenetic study of the opecoelids that estimates the interrelationships of the Plagioporinae that includes a member of Plagioporus.

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References

  • Andres, M. J., Pulis, E. E., & Overstreet, R. M. (2014a). New genus of opecoelid trematode from Pristipomoides aquilonaris (Perciformes: Lutjanidae) and its phylogenetic affinity within the family Opecoelidae. Folia Parasitologica, 61, 223–230.

    Article  PubMed  Google Scholar 

  • Andres, M. J., Ray, C. L., Pulis, E. E., Curran, S. S., & Overstreet, R. M. (2014b). Molecular characterization of two opecoelid trematodes from fishes in the Gulf of Mexico, with a description of a new species of Helicometra. Acta Parasitologica, 59, 405–412.

    Article  CAS  PubMed  Google Scholar 

  • Antar, R., Georgieva, S., Gargouri, L., & Kostadinova, A. (2015). Molecular evidence for the existence of species complexes within Macvicaria Gibson & Bray, 1982 (Digenea: Opecoelidae) in the western Mediterranean. Systematic Parasitology, 91, 211–229.

    PubMed  Google Scholar 

  • Barger, M. A., & Esch, G. W. (1999). Allopodocotyle chiliticorum n. sp. (Digenea: Opecoelidae) from redlip shiners, Notropis chiliticus, in Basin Creek, North Carolina. Journal of Parasitology, 85, 891–892.

    Article  CAS  PubMed  Google Scholar 

  • Born-Torrijos, A., Kostadinova, A., Raga, J. A., & Holzer, A. S. (2012). Molecular and morphological identification of larval opecoelids (Digenea: Opecoelidae) parasitising prosobranch snails in a western Mediterranean lagoon. Parasitology International, 61, 450–460.

    Article  CAS  PubMed  Google Scholar 

  • Bray, R. A., Cribb, T. H., Littlewood, D. T. J., & Waeschenbach, A. (2016). The molecular phylogeny of the digenean family Opecoelidae Ozaki, 1925 and the value of morphological characters, with the erection of a new subfamily. Folia Parasitologica, 63, 013.

    Article  Google Scholar 

  • Bray, R. A., Waeschenback, A., Cribb, T. H., Weedall, G. D., Dyal, P., & Littlewood, D. T. J. (2009). The phylogeny of the Lepocreadioidea (Platyhelminthes, Digenea) inferred from nuclear and mitochondrial genes: implications for their systematics and evolution. Acta Parasitologica, 54, 310–329.

    Google Scholar 

  • Bray, R. A., Waeschenback, A., Dyal, P., Littlewood, D. T. J., & Morand, S. (2014). New digeneans (Opecoelidae) from hydrothermal vent fishes in the southeastern Pacific Ocean, including one new genus and five new species. Zootaxa, 3768, 73–87.

    Article  CAS  PubMed  Google Scholar 

  • Bray, R. A., Webster, B. L., Bartoli, P., & Littlewood, D. T. J. (2005). Relationships within the Acanthocolpidae Lühe, 1906 and their place among the Digenea. Acta Parasitologica, 50, 281–291.

    CAS  Google Scholar 

  • Constenla, M., Carrassón, M., Moyà, C. M., Fernàndez-Chacón, A., Padrós, F., Repullés-Albelda, A., et al. (2011). Parasitisation by Bathycreadium elongatum (Digenea, Opecoelidae) in pyloric caeca of Trachyrincus scabrus. Diseases of Aquatic Organisms, 96, 239–247.

    Article  CAS  PubMed  Google Scholar 

  • Cribb, T. H. (2005). Family Opecoelidae Ozaki, 1925. In: Jones, A., Bray, R. A., & Gibson, D. I. (Eds) Keys to the Trematoda. Volume 2. Wallingford, UK: CAB International, pp. 443–532.

    Google Scholar 

  • Curran, S. S., Overstreet, R. M., & Tkach, V. V. (2007). Phylogenetic affinities of Plagiocirrus Van Cleave and Mueller, 1932 with description of a new species from the Pascagoula River, Mississippi. Journal of Parasitology, 93, 1452–1458.

    Article  CAS  PubMed  Google Scholar 

  • Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dobrovolny, C. G. (1939a). The life history of Plagioporus lepomis, a new trematode from fishes. Journal of Parasitology, 25, 461–470.

    Article  Google Scholar 

  • Dobrovolny, C. G. (1939b). Life history of Plagioporus sinitsini Mueller and embryology of a new cotylocercous cercariae (Trematoda). Transactions of the American Microscopical Society, 58, 121–155.

    Article  Google Scholar 

  • Gibson, D. I., & Bray, R. A. (1982). A study and reorganization of Plagioporus Stafford, 1904 (Digenea: Opecoelidae) and related genera, with special reference to forms from European Atlantic waters. Journal of Natural History, 16, 529–559.

    Article  Google Scholar 

  • Haderlie, E. C. (1953). Parasites of the freshwater fishes of Northern California. University of California Publications in Zoology, 57, 303–440.

    Google Scholar 

  • Hausmann, I. (1896). Ueber Trematoden der Süsswasserfische. Vorlaüfige Mitteilung. Centralblatt für Bakteriologie, l. Abt., 19, 389–392.

    Google Scholar 

  • Hendrix, S. S. (1978). Life history and biology of Plagioporus hypentelii Hendrix, 1973 (Trematoda: Opecoelidae). Journal of Parasitology, 64, 606–612.

    Article  Google Scholar 

  • Huelsenbeck, J. P., & Ronquist, F. (2001). Mr Bayes: Bayesian inference of phylogeny. Bioinformatics, 17, 754–755.

    Article  CAS  PubMed  Google Scholar 

  • Huelsenbeck, J. P., Ronquist, F., Nielsen, R., & Bollback, J. P. (2001). Bayesian inference of phylogeny and its impact on evolutionary biology. Science, 294, 2310–2314.

    Article  CAS  PubMed  Google Scholar 

  • Katoh, K., Kuma, K.-I., Toh, H., & Miyata, T. (2005). MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research, 33, 511–518.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keller, A., Schleicher, T., Schultz, J., Müller, T., Dandekar, T., & Wolf, M. (2009). 5.8S–28S rRNA interaction and HMM-based ITS2 annotation. Gene, 430, 50–57.

    Article  CAS  PubMed  Google Scholar 

  • Littlewood, D. T. L., Curini-Galletti, M., & Herniou, E. A. (2000). The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics and Evolution, 16, 449–466.

    Article  CAS  PubMed  Google Scholar 

  • Manter, H. W. (1954). Some digenetic trematodes from fishes of New Zealand. Transactions of the Royal Society of New Zealand, 82, 475–568.

    Google Scholar 

  • Mathias, P. (1936). Sur le cycle evolutif d’un Trematode Digenetique, Allocreadium angusticolle (Hausmann). Société de Biologie, 122, 1175–1176.

    Google Scholar 

  • Mathias, P. (1937). Cycle evolutif d’un Trematode de la famille des Allocreadiidae Stossish (Allocreadium angusticolle [Hausmann]). Société de Biologie, 205, 626–628.

    Google Scholar 

  • Møller, P. R., Knudsen, S. W., Schwarzhans, W., & Nielsen, J. G. (2016). A new classification of viviparous brotulas (Bythitidae) - with family status for Dinematichthyidae - based on molecular, morphological and fossil data. Molecular Phylogenetics and Evolution, 100, 391–408.

    Article  PubMed  Google Scholar 

  • Near, T. J., Eytan, R. I., Dornburg, A., Kuhn, K. L., Moore, J. A., Davis, M. P., et al. (2012). Resolution of ray-finned fish phylogeney and timing of diversification. Proceedings of the National Academy of Sciences, 109, 13698–13703.

    Article  CAS  Google Scholar 

  • Olson, P. D., Cribb, T. H., Tkach, V. V., Bray, R. A., & Littlewood, D. T. J. (2003). Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology, 33, 733–755.

    Article  CAS  PubMed  Google Scholar 

  • Schell, S. C. (1974). Two new genera and three new species of allocreadid trematodes (Digenea: Allocreadiidae) from freshwater fishes. Journal of Parasitology, 60, 243–246.

    Article  CAS  PubMed  Google Scholar 

  • Schell, S. C. (1975). The life history of Plagioporus shawi (McIntosh 1939) (Trematoda: Opecoelidae), an intestinal parasite of salmonid fishes. Journal of Parasitology, 61, 899–905.

    Article  CAS  PubMed  Google Scholar 

  • Shedko, M. B., Sokolov, S. G., & Atopkin, D. M. (2015). The first record of Dimerosaccus oncorhynchi (Trematoda: Opecoelidae) in fish from rivers of Primorsky territory, Russia, with a discussion on its taxonomic position using morphological and molecular data. Parazitologiya, 49, 171–189.

    CAS  Google Scholar 

  • Shimazu, T. (1990a). Trematodes of the genus Urorchis (Digenea: Opecoelidae: Urorchiinae) from freshwater fishes of Japan. Japanese Journal of Parasitology, 39, 204–212.

    Google Scholar 

  • Shimazu, T. (1990b). Trematodes of a new genus, Neoplagioporus gen. n. (Digenea: Opecoelidae: Plagioporinae), and an unidentified opecoelid from freshwater fishes of Japan. Japanese Journal of Parasitology, 39, 384–396.

    Google Scholar 

  • Sinitsin, D. F. (1931). Studien uber die Phylogenie der Trematoden, IV. The life histories of Plagioporus siliculus and Plagioporus virens, with special reference to the origin of the Digenea. Zeitschrift fur Wissenschaftliche Zoologie, 138, 409–456.

    Google Scholar 

  • Tkach, V. V., & Snyder, S. D. (2007). Choanocotyle platti sp. nov. from the northern long-necked turtle, Chelodina rugosa (Pleurodira, Chelidae) in Australia. Acta Parasitologica, 52, 318–324.

    Article  Google Scholar 

  • Tkach, V., Grabda-Kazubska, B., Pawlowski, J., & Swiderski, Z. (1999). Molecular and morphological evidence for close phylogenetic affinities of the genera Macrodera, Leptophallus, Metaleptophallus and Paralepoderma (Digenea, Plagiorchiata). Acta Parasitologica, 44, 170–179.

    CAS  Google Scholar 

  • Tkach, V. V., Pawlowski, J., & Mariaux, J. (2000). Phylogenetic analysis of the suborder plagiochiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. International Journal for Parasitology, 30, 83–93.

    Article  CAS  PubMed  Google Scholar 

  • Tkach, V. V., Pawlowski, J., Mariaux, J., & Swiderski, Z. (2001). Molecular phylogeny of the suborder Plagiorchiata and its position in the system of Digenea. In D. T. J. Littlewood & R. A. Bray (Eds.), Interrelationships of the Platyhelminthes (pp. 186–193). London, UK: Taylor & Francis.

    Google Scholar 

  • Tkach, V. V., Littlewood, D. T. J., Olson, P. D., Kinsella, J. M., & Swiderski, Z. (2003). Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology, 56, 1–15.

    Article  PubMed  Google Scholar 

  • Tracey, J. K., Choudhury, A., Cheng, J. M., & Ghosh, S. (2009). A new opecoelid species (Trematoda: Opecoelidae) from the threespine stickleback Gasterosteus aculeatus L. in California. Journal of Parasitology, 95, 1177–1182.

    Article  PubMed  Google Scholar 

  • Turgeon, D. D., Quinn, J. F., Bogan, A. E., Coan, E. V., Hochberg, F. G., Lyons, W. G., et al. (1998). Common and scientific names of aquatic invertebrates from the United States and Canada: Mollusks. Second Edition. American Fisheries Society, Special Publication 26, Bethesda, Maryland, 526 pp.

  • Van Cleave, H. J., & Mueller, J. F. (1932). Parasites of Oneida Lake fishes. Part I. Descriptions of new genera and species. Roosevelt Wild Life Annals, 3, 9–71.

    Google Scholar 

  • Van Cleave, H. J., & Mueller, J. F. (1934). Parasites of Oneida Lake Fishes. Part IV. Additional notes on parasites of Oneida Lake fishes, including descriptions of new species. Roosevelt Wild Life Annals, 3, 336–358.

    Google Scholar 

  • Wu, M., Chatterji, S., & Eisen, J. A. (2012). Accounting for alignment uncertainty in phylogenomics. PLOS ONE, 7, e30288.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We are indebted to Anindo Choudhury (St. Norbert College) for providing specimens of P. boleosomi, P. kolipinskii and P. shawi and also to Charles Criscione (Texas A&M) for providing specimens of P. shawi. We thank Urabe Misako (University of Shiga Prefecture) and Takeshi Shimazu for providing their insights on and specimens of opecoelids from Japan. We are also thankful to Sean Locke (University of Puerto Rico-Mayagüez), David Marcogliese (Environment Canada) and associated personnel from Environment Canada who aided in the collection of fish hosts of P. sinitsini and provided lab space for dissections in Montreal, Canada. From the University of Southern Mississippi, we thank Jean Jovonovich Alvillar and Janet Wright for their assistance with DNA sequencing reactions and Richard Heard and Robin Overstreet for provision of microscopy equipment and funds for molecular work. This work would not have been possible without the support of Vassar College Fellowships awarded to TJF that provided funds for the collection of freshwater plagioporines and also living expenses while working up species descriptions at St. Norbert College, including an Adolph Sutro Fellowship in 2013/2014, a Nancy Skinner Clark Fellowship in 2014/2015 and an additional Nancy Skinner Clark Fellowship in 2015/2016. The material treated here is based on work supported by the National Science Foundation under grant no. 0529684 and Ocean and Human Health Initiative grant no. NA08NOS4730322.

Funding

Funding for this research included Vassar College fellowships awarded to TJF, including an Adolph Sutro Fellowship in 2013/2014, a Nancy Skinner Clark Fellowship in 2014/2015 and an additional Nancy Skinner Clark Fellowship in 2015/2016; National Science Foundation grant no. 0529684 and Ocean and Human Health Initiative grant no. NA08NOS4730322 awarded to Robin Overstreet (University of Southern Mississippi); and funds from Richard Heard’s (University of Southern Mississippi) indirect account through the School of Ocean Science and Technology.

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Correspondence to Thomas J. Fayton.

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All applicable institutional, national and international guidelines for the care and use of animals were followed. The Oncorhynchus mykiss examined in this study and specimens of Plagioporus chiliticorum were collected using recreational fishing licenses respectively from California and North Carolina (TJF); hosts of the other opecoelids included in this study were collected with the appropriate permits assigned to Anindo Choudhury, Charles Criscione, Environment Canada, Takeshi Shimazu and Urabe Misako.

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Fayton, T.J., Andres, M.J. New species of Plagioporus Stafford, 1904 (Digenea: Opecoelidae) from California, with an amendment of the genus and a phylogeny of freshwater plagioporines of the Holarctic. Syst Parasitol 93, 731–748 (2016). https://doi.org/10.1007/s11230-016-9664-6

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