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Filling the gaps in the classification of the Digenea Carus, 1863: systematic position of the Proterodiplostomidae Dubois, 1936 within the superfamily Diplostomoidea Poirier, 1886, inferred from nuclear and mitochondrial DNA sequences

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Abstract

The Diplostomida Olson, Cribb, Tkach, Bray & Littlewood, 2003 is the less diverse order of the two orders within the subclass Digenea Carus, 1863 and is currently classified into three superfamilies, i.e. Brachylaimoidea Joyeux & Foley, 1930, Diplostomoidea Poirier, 1886, and Schistosomatoidea Stiles & Hassall, 1898. Although the suprageneric-level relationships have been elucidated with the use of molecular markers, the lack of representation of some groups obscure the phylogenetic relationships among families, rendering the classification unstable. Here, we tested the phylogenetic position of the family Proterodiplostomidae Dubois, 1936 based on partial 28S rDNA and complete 18S rDNA sequences for Crocodilicola pseudostoma (Willemoes-Suhm, 1870), a crocodile parasite that has been found as a progenetic metacercaria parasitising the pale catfish Rhamdia guatemalensis (Günther) in Mexico and in other siluruforms in the Neotropics. We augmented the representation of the species, genera and families within the Diplostomida, including mostly representatives of the superfamily Diplostomoidea, and assembled a dataset that contains 49 species for the 28S rRNA gene, and 45 species for the 18S rRNA gene. Additionally, we explored the phylogenetic signal of the mitochondrial gene cox1 in reconstructing the phylogenetic relationships of selected members of the superfamily. Our analyses showed that the family Proterodiplostomidae is the sister taxon to the paraphyletic Diplostomidae Poirier, 1886 and Strigeidae Railliet, 1919, with Cyathocotylidae Mühling, 1898 + Brauninidae Wolf, 1903 as their sister group. Analysis of concatenated 18S + 28S sequences revealed the Liolopidae Odhner, 1912 as the basal group of the superfamily Diplostomoidea, although analyses of independent datasets showed that the position of this family remains uncertain. Analysis based on cox1 unequivocally resolved the Proterodiplostomidae as the sister taxon to the Diplostomidae and Strigeidae, although the Cyathocotylidae was nested in a different clade, along with brachylaimoids and schistosomatoids.

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References

  • Baba, T., Hosoi, M., Urabe, M., Shimazu, T., Tochimoto, T., & Hasegawa, H. (2011). Liolope copulans (Trematoda: Digenea: Liolopidae) parasitic in Andrias japonicus (Amphibia: Caudata: Cryptobranchidae) in Japan: Life cycle and systematic position inferred from morphological and molecular evidence. Parasitology International, 60, 181–192.

    Article  PubMed  Google Scholar 

  • Bell, A. S., Sommerville, S., & Valtonen, E. T. (2001). A molecular phylogeny of the genus Ichthyocotylurus (Digenea, Strigeidae). International Journal for Parasitology, 31, 833–842.

    Article  CAS  PubMed  Google Scholar 

  • Blasco-Costa, I., Poulin, R., & Presswell, B. (2016a). Species of Apatemon Szidat, 1928 and Australapatemon Sudarikov, 1959 (Trematoda: Strigeidae) from New Zealand: Linking and characterising life cycle stages with morphology and molecules. Parasitology Research, 115, 271–289.

    Article  PubMed  Google Scholar 

  • Blasco-Costa, I., Cutmore, S. C., Miller, T. L., & Nolan, M. J. (2016b). Molecular approaches to trematode systematics: ‘Best practice’ and implications for future study. Systematic Parasitology, 93, 295–306.

    Article  PubMed  Google Scholar 

  • Bray, R. A., Gibson, D. I., & Jones, A. (Eds) (2008). Keys to the Trematoda. Volume 3. Wallingford, UK: CAB International & The Natural History Museum, 824 pp.

  • Briscoe, A. G., Bray, R. A., Brabec, J., & Littlewood, D. T. J. (2016). The mitochondrial genome and ribosomal operon of Brachycladium goliath (Digenea: Brachycladiidae) recovered from a stranded minke whale. Parasitology International, 65, 271–275.

    Article  CAS  PubMed  Google Scholar 

  • Brooks, D. R., & Overstreet, R. (1978). The family Liolopidae (Digenea) including a new genus and two new species from crocodilians. International Journal for Parasitology, 8, 267–273.

    Article  Google Scholar 

  • Brooks, D. R., Catto, J. B., & Amato, F. R. (1992). A new phylogenetic classification of the genera of the Proterodiplostomatidae Dubois, 1936 (Digenea: Strigeiformes). Proceedings of the Biological Society of Washington, 105, 143–147.

    Google Scholar 

  • Brooks, D. R., O’Grady, T., & Glen, D. R. (1985). Phylogenetic analysis of the Digenea (Platyhelminthes: Cercomeria) with comments in their adaptive radiation. Canadian Journal of Zoology, 63, 873–883.

    Article  Google Scholar 

  • Caballero, E. (1948). Estudios helmintológicos de la Cuenca del río Papaloapan III. Strigeidos de los lagartos de México. 2. Anales de la escuela Nacional de Ciencias Biológicas, 5, 217–221.

    Google Scholar 

  • Conroy, G. A. (1986). Crocodilicola pseudostoma (Willemoes-Suhm, 1870) Poche, 1925 (Trematoda: Proterodiplostomidae), endoparásito del bagre pimelódido Rhamdia hilarii Val., 1840 del Estado de São Paulo, Brasil. Revista Ibérica de Parasitología, 46, 35–38.

    Google Scholar 

  • Cribb, T. H., Bray, R. A., Littlewood, D. T. J., Pichelin, S., & Herniou, E. A. (2001). The Digenea. In: Littlewood, D. T. J. & Bray, R. A. (Eds) Interrelationships of the Platyhelminthes. London: Taylor & Francis, pp. 168–185.

    Google Scholar 

  • Cribb, T. H., Bray, R. A., Olson, P. D., & Littlewood, D. T. J. (2003). Life cycle evolution in the Digenea: A new perspective from phylogeny. Advances in Parasitology, 54, 197–254.

    Article  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 

  • Dubois, G. (1936). Les Diplostomes de Reptiles (Trematoda: Proterodiplostomidae nov. fam.) du Musée de Vienne. Bulletin de la Société Neuchateloise des Sciences Naturelles, 61, 5–80.

    Google Scholar 

  • Dubois, G. (1938). Monographie des Strigeida (Trematoda). Mémoires de la Société Neuchateloise des Sciences Naturelles, 6, 1–535.

    Google Scholar 

  • Dubois, G. (1970). Revision des Proterodiplostomatidae Dubois, 1936 (Trematoda: Strigeta). Anales del Instituto de Biología, Universidad Nacional Autónoma de México, Serie Zoología, 41, 51–60.

    Google Scholar 

  • Dzikowski, R., Levy, M., Poore, M. F., Flowers, J. R., & Paperna, I. (2003). Genetic and morphologic differentiation of Bolbophorus confusus and B. levantinus (Digenea: Diplostomatidae), based on rDNA SSU polymorphism and SEM. Diseases of Aquatic Organisms, 57, 231–235.

    Article  CAS  PubMed  Google Scholar 

  • Dzikowski, R., Levy, M. G., Poore, M. F., Flowers, J. R., & Paperna, I. (2004). Clinostomum complanatum and Clinostomum marginatum (Rudolphi, 1819) (Digenea: Clinostomidae) are separate species based on differences in ribosomal DNA. Journal of Parasitology, 90, 413–414.

    Article  CAS  PubMed  Google Scholar 

  • Ferrari-Hoeinghaus, A. P., Takemoto, R. M., & Pavanelli, G. C. (2007). Digenetic trematode parasites of Loricariichthys platymetopon (Loricariidae, Siluriformes) of the upper Paraná river floodplain, Brazil. Acta Scientarumn Biological Sciences, 29, 327–329.

    Google Scholar 

  • Fraija-Fernández, N., Olson, P. D., Crespo, E. A., Raga, J. A., Aznar, F. J., & Fernández, M. (2015). Independent host switching events by digenean parasites of cetaceans inferred from ribosomal DNA. International Journal for Parasitology, 45, 167–173.

    Article  PubMed  Google Scholar 

  • Froese, R., & Pauly, D. (Eds) (2017). FishBase. World Wide Web electronic publication. http://www.fishbase.org, version 06/2017.

  • Galazzo, D. E., Dayanandan, S., Marcogliese, D. J., & 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, 30, 2207–2217.

    Article  Google Scholar 

  • García-Varela, M., & Nadler, S. A. (2005). Phylogenetic relationships of Palaeacanthocephala (Acanthocephala) inferred from SSU and LSU rDNA gene sequences. Journal of Parasitology, 91, 1401–1409.

    Article  PubMed  Google Scholar 

  • García-Varela, M., Sereno-Uribe, A. L., Pinacho-Pinacho, C. D., Domínguez- Domínguez, O., & Pérez-Ponce de León, G. (2016a). Molecular and morphological characterization of Austrodiplostomum ostrowskiae Dronen, (Digenea: Diplostomatidae), a parasite of cormorants in the Americas. Journal of Helminthology, 90, 174–185.

    Article  PubMed  Google Scholar 

  • García-Varela, M., Sereno-Uribe, A. L., Pinacho-Pinacho, C. D., Hernández- Cruz, E., & Pérez-Ponce de León, G. (2016b). An integrative taxonomic study reveals a new species of Tylodelphys Diesing, 1950 (Digenea: Diplostomidae) in central and northern Mexico. Journal of Helminthology, 90, 668–679.

    Article  PubMed  Google Scholar 

  • Georgieva, S., Soldánová, M., Pérez-del-Olmo, A., Dangel, D. R., Sitko, J., Sures, B., et al. (2013). Molecular prospecting for European Diplostomum (Digenea: Diplostomidae) reveals cryptic diversity. International Journal for Parasitology, 43, 57–72.

    Article  CAS  PubMed  Google Scholar 

  • Gibson, D. I., Jones, A., & Bray, R. A. (Eds) (2002). Keys to the Trematoda. Volume 1. Wallingford, UK: CAB International & The Natural History Museum, 521 pp.

  • Guidelli, G. M., Isaac, A., Takemoto, R. M., & Pavanelli, G. C. (2003). Endoparasite infracommunities of Hemisorubi platyrhynchos (Valenciennes, 1840) (Pisces: Pimelodidae) of the Baía river, upper Paraná river floodplain, Brazil: Specific composition and ecological aspects. Brazilian Journal of Biology, 63, 261–268.

    Article  CAS  Google Scholar 

  • Hernández-Mena, D. I., García-Prieto, L., & García-Varela, M. (2014). Morphological and molecular differentiation of Parastrigea (Trematoda: Strigeidae) from Mexico, with the description of a new species. Parasitology International, 63, 315–323.

    Article  PubMed  Google Scholar 

  • Jones, A., Bray, R. A., & Gibson, D. I. (Eds) (2005). Keys to the Trematoda. Volume 2. Wallingford, UK: CAB International & The Natural History Museum, 745 pp.

  • Kanev, I., Radev, V., & Fried, B. (2002). Superfamily Clinostomoidea Lühe, 1901. In: Gibson, D. I., Jones, A. & Bray, R. A. (Eds). Keys to the Trematoda, Volume 1. Wallingford, UK: CABI Publishing and The Natural History Museum, pp. 111–112.

    Google Scholar 

  • Kostadinova, A., & Pérez-del Olmo, A. (2014). The systematics of the Trematoda. In: Toldedo, R. & Fried, B. (Eds). Digenetic Trematodes. Advances in Experimental Medicine and Biology. New York: Springer, pp. 21–44.

  • Littlewood, D. T. J. (2008). Platyhelminth systematics and the emergence of new characters. Parasite, 15, 333–341.

    Article  CAS  PubMed  Google Scholar 

  • Littlewood, D. T. J., Bray, R. A., & Waeschenbach, A. (2015). Phylogenetic patterns of diversity in the cestodes and trematodes. In: Morand, S., Krasnov, B. R. & Littlewood, D. T. J. (Eds) Parasite diversity and diversification: Evolutionary ecology meets phylogenetics. Cambridge: Cambridge University Press, pp. 304–319.

    Chapter  Google Scholar 

  • Littlewood, D. T., Lockyer, A. E., Webster, B. L., Johnston, D. A., & Le, T. H. (2006). The complete mitochondrial genomes of Schistosoma haematobium and Schistosoma spindale and the evolutionary history of mitochondrial genome changes among parasitic flatworms. Molecular Phylogeneics and Evolution, 39, 452–467.

    Article  CAS  Google Scholar 

  • Liu, K., Raghavan, S., Nelesen, S., Linder, C. R., & Warnow, T. (2009). Rapid and accurate large-scale coestimation of sequence alignments and phylogenetic trees. Science, 324, 1561–1564.

    Article  CAS  PubMed  Google Scholar 

  • Liu, K., Warnow, T., Holder, M., Nelesen, S., Yu, J., Stamatakis, P., & Linder, R. (2012). SATé-II: Very fast and accurate simultaneous estimation of multiple sequence alignments and phylogenetic trees. Systematic Biology, 61, 90–106.

    Article  PubMed  Google Scholar 

  • Locke, S. A., Al-Nasiri, F. S., Caffara, M., Drago, F., Kalbe, M., Lapierre, A. R., et al. (2015). Diversity, specificity and speciation in larval Diplostomidae (Platyhelminthes: Digenea) in the eyes of freshwater fish, as revealed by DNA barcodes. International Journal for Parasitology, 45, 841–855.

    Article  CAS  PubMed  Google Scholar 

  • Locke, S. A., McLaughlin, J. D., Dayanandan, S., & Marcogliese, D. J. (2010). Diversity and specificity in Diplostomum spp. metacercariae in freshwater fishes revealed by cytochrome c oxidase I and internal transcribed spacer sequences. International Journal for Parasitology, 40, 333–343.

    Article  CAS  PubMed  Google Scholar 

  • Locke, S. A., McLaughlin, J. D., Lapierre, A. R., Johnson, P. T. J., & Marcogliese, D. J. (2011). Linking larvae and adults of Apharyngostrigea cornu, Hysteromorpha triloba, and Alaria mustelae (Diplostomoidea: Digenea) using molecular data. Journal of Parasitology, 97, 846–851.

    Article  PubMed  Google Scholar 

  • Lockyer, A. E., Olson, P. D., & Littlewood, D. T. J. (2003). Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): Implications and a review of the cercomer theory. Biological Journal of the Linnean Society, 78, 155–171.

    Article  Google Scholar 

  • Messing, J. (1983). New M13 vectors for cloning. Methods in Enzymology, 101, 20–78.

    Article  CAS  PubMed  Google Scholar 

  • Nadler, S. A., & Hudspeth, D. S. S. (1998). Ribosomal DNA and phylogeny of the Ascaridoidea (Nemata: Secernentea): Implications for morphological evolution and classification. Molecular Phylogenetics and Evolution, 10, 221–236.

    Article  CAS  PubMed  Google Scholar 

  • Nadler, S. A., Carreno, R. A., Mejia-Madrid, H., Ullberg, J., Pagan, C., Houston, R., & Hugot, J. P. (2000). Molecular phylogeny of clade III nematodes reveals multiple origins of tissue parasitism. Parasitology, 134, 1421–1442.

    Article  Google Scholar 

  • Niewiadomska, K. (2002a). Superfamily Diplostomoidea Poirier, 1886. In: Gibson, D. I., Jones, A. & Bray, R. A. (Eds). Keys to the Trematoda, Volume 1. Wallingford, UK: CABI Publishing and The Natural History Museum, pp. 159–196.

    Google Scholar 

  • Niewiadomska, K. (2002b). Family Diplostomidae Poirier, 1886. In: Gibson, D. I., Jones, A. & Bray, R. A. (Eds). Keys to the Trematoda, Volume 1. Wallingford: CABI Publishing and The Natural History Museum, pp. 167–166.

    Google Scholar 

  • Niewiadomska, K. (2002c). Family Brauninidae Wolf, 1936. In: Gibson, D. I., Jones, A. & Bray, R. A. (Eds). Keys to the Trematoda, Volume 1. Wallingford, UK: CABI Publishing and The Natural History Museum, pp. 199–200.

    Google Scholar 

  • Niewiadomska, K. (2002d). Family Cyathocotylidae Mühling, 1898. Gibson, D. I., Jones, A. & Bray, R. A. (Eds). Keys to the Trematoda, Volume 1. Wallingford, UK: CABI Publishing and The Natural History Museum, pp. 201–214.

    Google Scholar 

  • Niewiadomska, K. (2002e). Family Proterodiplostomidae Dubois, 1936. In: Gibson, D. I., Jones, A., and Bray, R. A. (Eds). Keys to the Trematoda, Volume 1. Wallingford, UK: CABI Publishing and The Natural History Museum, pp. 215–230.

    Google Scholar 

  • Niewiadomska, K. (2002f). Family Strigeidae Railliet, 1919. In: Gibson, D. I., Jones, A. & Bray, R. A. (Eds). Keys to the Trematoda, Volume 1. Wallingford, UK: CABI Publishing and The Natural History Museum, pp. 231–244.

    Google Scholar 

  • Niewiadomska, K. (2002g). Family Liolopidae Odhner, 1912. In: Gibson, D. I., Jones, A. & Bray, R. A. (Eds). Keys to the Trematoda, Volume 1. Wallingford, UK: CABI Publishing and The Natural History Museum, pp. 121–125.

    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 

  • Patrelle, C., Portier, J., Jouet, D., Delorme, D., & Ferté, H. (2015). Prevalence and intensity of Alaria alata (Goeze, 1792) in water frogs and brown frogs in natural conditions. Parasitology Research, 114, 4405–4412.

    Article  PubMed  Google Scholar 

  • Pérez-Ponce de León, G., García-Prieto, L., & Osorio-Sarabia, D. (1992). Helmintofauna del “juile” Rhamdia guatemalensis (Pisces: Pimelodidae), del lago de Catemaco, Veracruz. Revista de la Sociedad Mexicana de Historia Natural, 43, 25–31.

    Google Scholar 

  • Pérez-Ponce de León, G., García-Varela, M., Pinacho-Pinacho, C. D., Sereno-Uribe, A. L., & Poulin, R. (2016). Species delimitation in trematodes using DNA sequences: Middle-American Clinostomum as a case study. Parasitology, 143, 1773–1789.

    Article  PubMed  Google Scholar 

  • Pulis, E. E., Fayton, T. J., Curran, S. S., & Overstreet, R. M. (2013). A new species of Intromuguil (Digenea: Haploporidae) and redescription of Intromugul mugilicolus. Journal of Parasitology, 99, 501–508.

    Article  PubMed  Google Scholar 

  • Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., et al. (2012). MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shoop, W. L. (1989). Systematic analysis of the Diplostomidae and Strigeidae (Trematoda). Journal of Parasitology, 75, 21–32.

    Article  CAS  PubMed  Google Scholar 

  • Stamatakis, A. (2006). RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.

    Article  CAS  PubMed  Google Scholar 

  • Stock, S. P., Campbell, J. F., & Nadler, S. A. (2001). Phylogeny of Steinerma Travassos, 1927 (Cephalobina: Steinermatidae) inferred from ribosomal DNA sequences and morphological characters. Journal of Parasitology, 87, 877–899.

    Article  CAS  PubMed  Google Scholar 

  • Waeschenbach, A., Webster, B. L., Bray, R. A., & Littlewood, D. T. J. (2007). Added resolution among ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with complete small and large subunit nuclear ribosomal RNA genes. Molecular Phylogenetics and Evolution, 45, 311–325.

    Article  CAS  PubMed  Google Scholar 

  • Webster, B. L., & Littlewood, D. T. J. (2012). Mitochondrial gene order change in Schistosoma (Platyhelminthes: Digenea: Schistosomatidae). International Journal for Parasitology, 42, 313–321.

    Article  CAS  PubMed  Google Scholar 

  • Willemoes-Suhm, R. (1871). Uber einige Trematoden u. Nemathelminthen. Zeitschrift für wissenschaftliche Zoologie, 2, 175–203.

    Google Scholar 

  • Yamaguti, S. (1971). Synopsis of digenetic trematodes of vertebrates. Tokyo: Keigaku Publishing Co., Parts I & II. 1074 pp. + 349 pl.

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Acknowledgements

This study represent a partial fulfillment of DIHM for the requirements to obtain PhD degree in the Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México. DIHM also thanks the Consejo Nacional de Ciencia y Tecnología (CONACyT) for student grant 245193. We thank Dr. Miguel Rubio-Godoy for the donation of specimens of Mesostephanus for molecular work. We thank two anonymous reviewers for their comments on the manuscript.

Funding

This project was funded by the Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT-UNAM) IN204514 and IN202617 to GPPL, and PAPIIT-UNAM IN206716 to M.G.V.

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Correspondence to Gerardo Pérez-Ponce de León.

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All applicable institutional, national and international guidelines for the care and use of animals were followed. Hosts were collected under the Cartilla Nacional de Colector Científico de Flora y Fauna Silvestre FAUT-0057 and 0202 issued to GPPL and MGV, respectively, by the Secretaria del Medio Ambiente y Recursos Naturales.

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Hernández-Mena, D.I., García-Varela, M. & Pérez-Ponce de León, G. Filling the gaps in the classification of the Digenea Carus, 1863: systematic position of the Proterodiplostomidae Dubois, 1936 within the superfamily Diplostomoidea Poirier, 1886, inferred from nuclear and mitochondrial DNA sequences. Syst Parasitol 94, 833–848 (2017). https://doi.org/10.1007/s11230-017-9745-1

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