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Preliminary phylogenetic analysis of subfamilies of the Proteocephalidea (Eucestoda)

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Abstract

Cladistic analysis based on comparative morphology was used to examine the subfamily-level relationships within the cestode order Proteocephalidea. A single most parsimonious tree (70 steps, CI = 0.571; RC = 0.295; HI = 0.471) is consistent with monophyly for the Proteocephalidea and showed a relatively high consistency at the family level with the diagnosis of two major subclades. Unambiguous support for a Proteocephalidae subclade, including the Corallobothriinae, Proteocephalinae, Gangesiinae and Sandonellinae, and a Monticelliidae subclade, including the Marsypocephalinae, Zygobothriinae, Monticelliinae, Rudolphiellinae, Ephedrocephalinae and Othinoscolecinae was evident. Two subfamilies, the Acanthotaeniinae (historically in the Proteocephalidae) and Nupeliinae (historically in the Monticelliidae), were however, basal to all other subfamilies, indicating that neither family as currently conceived is monophyletic. Trees one or two steps longer, however, would be consistent with monophyly for the Proteocephalidae and Monticelliidae (excluding Acanthotaeniinae) or would result in the monophyly for both families, including all respective subfamilies congruent with current concepts for systematics of the order. Zoogeographical analysis demonstrated a strong Gondwanan association; proteocephalideans originated in Africa, with subsequent development linking Africa and South America. Colonisation of the Northern Hemisphere by proteocephalid subfamilies, the Proteocephalinae, Corallobothriinae and Gangesiinae, was secondary. Analysis of parasite-host relationships indicated that the basal hosts for the Proteocephalidea are equivocal; siluriform teleosts were, however, the basal hosts for the Nupeliinae + the Monticelliidae and Proteocephalidae subclades and an extensive co-evolutionary history with this host group is postulated. Independent colonisation events of reptilians by species of the Proteocephalinae and Acanthotaeniinae, non-siluriform teleosts associated with the Sandonellinae and some Proteocephalinae, and amphibians by some Proteocephalinae, are recognised. Some points which should be considered for further development of the systematics of the group are proposed, with special emphasis given to thorough morphological descriptions and investigations of life-cycles.

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References

  • Anonymous (1957) How to collect parasites. Methods adopted by the First Symposium on Host Specificity among Parasites of Vertebrates. In: Attinger, P. (Ed.) First Symposium on Host Specificity among Parasites of Vertebrates. Neuchâtel, 324 pp.

  • Brooks, D.R. (1978a) Systematic status of the proteocephalid cestodes of North American reptiles and amphibians. Proceedings of the Helminthological Society of Washington, 45, 1–28.

    Google Scholar 

  • Brooks, D.R. (1978b) Evolutionary history of the cestode order Proteocephalidea. Systematic Zoology, 27, 312–323.

    Google Scholar 

  • Brooks, D.R. (1995) Phylogenetic hypothesis, cladistic diagnoses, and classification of the Monticelliidae (Eucestoda: proteocephaliformes). Revista Brasileira de Biologia, 55, 359–367.

    Google Scholar 

  • Brooks, D.R., Hoberg, E.P. & Weekes, P.J. (1991) Preliminary phylogenetic systematic analysis of the major lineages of the Eucestoda (Platyhelminthes: Cercomeria). Proceedings of the Biological Society of Washington, 104, 651–668.

    Google Scholar 

  • Brooks, D.R. & McLennan, D. A. (1993) Parascript. Parasites and the language of Evolution. Washington & London: Smithsonian Institution Press, 429 pp.

    Google Scholar 

  • Brooks, D.R. & Rasmussen, G. (1984) Proteocephalid cestodes from Venezuelan catfish, with a new classification of the Monticelliidae. Proceedings of the Biological Society of Washington, 97, 748–760.

    Google Scholar 

  • de Chambrier, A. (1987) Vaucheriella bicheti n. gen., n. sp. (Cestoda: Monticelliidae, Zygobothriinae) parasite de Tropidophis cf. taczanowskyi (Steindachner, 1880) (Serpentes: Tropidophidae) des Andes équatoriennes. Revue Suisse de Zoologie, 94, 829–840.

    Google Scholar 

  • de Chambrier, A. (1988) Crepidobothrium garzonii n. sp. (Cestoda: Proteocephalidae) parasite de Bothrops alternatus Dum. Bibr. & Dum., 1854 (Serpentes: Viperidae) au Paraguay. Revue Suisse de Zoologie, 95, 1,163–1,170.

    Google Scholar 

  • de Chambrier, A. (1989a) Révision du genre Crepidobothrium Monticelli, 1900 (Cestoda: Proteocephalidae) parasite d'Ophidiens néotropicaux. I. C. gerrardii (Baird, 1860) et C. viperis (Beddard, 1913). Revue Suisse de Zoologie, 96, 191–217.

    Google Scholar 

  • de Chambrier, A. (1989b) Révision du genre Crepidobothrium Monticelli, 1900 (Cestoda: Proteocephalidae) parasite d'Ophidiens néotropicaux. II. C. dollfusi Freze, 1965, C. lachesidis (MacCallum, 1921) et conclusions. Revue Suisse de Zoologie, 96, 345–380.

    Google Scholar 

  • de Chambrier, A. (1990) Redescription de Proteocephalus paraguayensis (Rudin, 1917) (Cestoda: Proteocephalidae) parasite de Hydrodynastes gigas (Dum., Bibr. & Dum., 1854) du Paraguay. Systematic Parasitology, 16, 85–97.

    Google Scholar 

  • de Chambrier, A. & Rego, A.A. (1994) Proteocephalus sophiae n. sp. (Cestoda: Proteocephalidae) a parasite of the siluroid fish Paulicea luetkeni (Pisces: Pimelodidae) from the Brazilian Amazon. Revue Suisse de Zoologie, 101, 361–368.

    Google Scholar 

  • de Chambrier, A. & Rego, A.A. (1995) Mariauxiella pimelodi n. g., n. sp. (Cestoda: Monticelliidae): a parasite of pimelodid siluroid fishes from South America. Systematic Parasitology, 30, 57–65.

    Google Scholar 

  • de Chambrier, A., Scholz, T. & Vaucher, C. (1996) Tapeworms (Cestoda: Proteocephalidea) of Hoplias malabaricus (Pisces: Characiformes, Erythrinidae) in Paraguay: description of Proteocephalus regoi sp. n., and redescription of Nomimoscolex matogrossensis. Folia Parasitologica, 43, 133–140.

    Google Scholar 

  • de Chambrier, A. & Vaucher, C. (1984) Proteocephalus gaspari n. sp. (Cestoda: Proteocephalidae), parasite de Lepisosteus tropicus (Gill) au Lac Managua (Nicaragua). Revue Suisse de Zoologie, 91, 229–233.

    Google Scholar 

  • de Chambrier, A., Vaucher, C. & Renaud, F. (1992) Etude des caracteres morpho-anatomiques et des flux géniques chez quatre Proteocephalus (Cestoda: Proteocephalidae) parasites de Bothrops jararaca au Brésil et description de trois especes nouvelles. Systematic Parasitology, 23, 141–156.

    Google Scholar 

  • de Chambrier, A. & Vaucher, C. (1992) Nomimoscolex touzeti n. sp. (Cestoda), a parasite of Ceratophrys cornuta (L.): first record of a Monticelliidae in an amphibian host. Memorias do Instituto Oswaldo Cruz, 87, 61–67.

    Google Scholar 

  • de Chambrier, A. & Vaucher, C. (1994) Etude morpho-anatomique et génétique de deux nouveaux Proteocephalus Weinland, 1858 (Cestoda: Proteocephalidae) parasites de Platydoras costatus (L.), poisson siluriforme du Paraguay. Systematic Parasitology, 27, 173–185.

    Google Scholar 

  • de Chambrier, A. & Vaucher, C. (1997) Révision des cestodes (Monticelliidae) décrits par Woodland (1934) chez Brachyplatystoma filamentosum avec redéfinition des genres Endorchis Woodland, 1934 et Nomimoscolex Woodland, 1934. Systematic Parasitology, 37, 219–233.

    Google Scholar 

  • de Chambrier, A. & Paulino, R. C. (1997) Proteocephalus joanae sp. n., a parasite of Xenodon neuwiedi (Serpentes: Colubridae) from South America. Folia Parasitologica, 44, 289–296.

    Google Scholar 

  • Dubinina, M.N. (1971) Tapeworms of fish of the Amur River basin. Parazitogicheskii sbornik of the Zoological Institute of the Academy of Sciences of the USSR, 25, 77–119. (In Russian).

    Google Scholar 

  • Dubinina, M.N. (1987) Class Cestoda Rudolphi, 1808. In: Bauer, O.N. (Ed.) Key to the parasites of freshwater fishes. Vol. 3., Leningrad: Nauka, pp. 5–76. (In Russian).

    Google Scholar 

  • Euzet, L. (1994) Order Tetraphyllidea Carus, 1863. In: Khalil, L.F, Jones, A. & Bray, R.A. (Eds) Keys to the cestode parasites of vertebrates, Wallingford: CAB International, pp. 149–194.

    Google Scholar 

  • Freze, V.I. (1965) Essentials of cestodology. Vol. V. Proteocephalata in fish, amphibians and reptiles. Moskva: Izdatel'stvo “Nauka”, 538 pp. (In Russian: English translation, Israel Program of Scientific Translation, 1969, Cat. No. 1853. v + 597 pp).

    Google Scholar 

  • Fuhrmann, O. (1931) Dritte Klasse des Cladus Plathelminthes Cestoidea. In: Kukenthal, W. & Krumbach, T. (Eds) Handbuch der Zoologie, Berlin und Leipzig: Bogen, 1930–1931, Vol. 2, 141–416.

    Google Scholar 

  • Georgiev, B., Biserkov, V. & Genov, T. (1986) In toto staining method for cestodes with iron acetocarmine. Helminthologia, 23, 279–281.

    Google Scholar 

  • Gibson, D.I. (1984) Technology as applied to museum collections: the collection, fixation and conservation of Helminths. Systematic Parasitology, 6, 241–255.

    Google Scholar 

  • Hanzelová, V. & Scholz, T. (1992) Redescription of Proteocephalus neglectus La Rue, 1911 (Cestoda: Proteocephalidae), a trout parasite, including designation of its lectotype. Folia Parasitologica, 39, 317–323.

    Google Scholar 

  • Hanzelová, V. & Scholz, T. (1993) Systematic status of Proteocephalus tumidocollis (Cestoda: Proteocephalidae), a parasite of salmonid fishes in North America. Helminthologia, 30, 157–161.

    Google Scholar 

  • Hanzelová, V. & Spakulová, M. (1992) Biometric variability of Proteocephalus neglectus (Cestoda: Proteocephalidae) in two different age groups in the rainbow trout from the Dobsiná dam (East Slovakia). Folia Parasitologica, 39, 307–316.

    Google Scholar 

  • Hanzelová, V., Scholz, T. & Fagerholm, H.-P. (1995a) Synonymy of Proteocephalus neglectus La Rue, 1911, with P. exiguus La Rue, 1911, two fish cestodes from the Holarctic Region. Systematic Parasitology, 30, 173–185.

    Google Scholar 

  • Hanzelová, V., Spakulová, M., Snábel, V., Kralová, I. & Fagerholm, H.-P. (1995b) A comparative study of the fish parasites Proteocephalus exiguus and P. percae (Cestoda: Proteocephalidae): morphology, isoenzymes, and karyotype. Canadian Journal of Zoology, 73, 1191–1198.

    Google Scholar 

  • Hennig, W. (1950) Grundzüge einer Theorie der phylogenetischen Systematik. Berlin: Deutscher Zentralverlag, 370 pp.

    Google Scholar 

  • Hennig, W. (1966) Phylogenetic systematics. Urbana: University of Illinois Press, 263 pp.

    Google Scholar 

  • Hoberg, E.P. & Lichtenfels, J.R. (1994) Phylogenetic systematic analysis of the Trichostrongylidae (Nematoda), with an initial assessment of coevolution and biogeography. Journal of Parasitology, 80, 976–996.

    Google Scholar 

  • Hoberg,. E.P., Mariaux, J., Justine, J.-L., Brooks, D.R. & Weekes, P. (1997) Phylogeny of the orders of the Eucestoda (Cercomermomorphae) based on comparative morphology: historical prespectives and a new working hypothesis. Journal of Parasitology, 83, In Press.

  • La Rue, R.B. (1911) A revision of the cestode family Proteocephalidae. Zoologischer Anzeiger, 38, 473–482.

    Google Scholar 

  • La Rue, R.B. (1914) A revision of the cestode family Proteocephalidae. Illinois Biological Monographs, 1, 3–351.

    Google Scholar 

  • Lynsdale, J.A. (1959) On a new species of Proteocephalus from Brazil. Journal of Helminthology, 34, 43–46.

    Google Scholar 

  • Maddison, W.P. & Maddison, D.R. (1993) MacClade: analysis of phylogeny and character evolution. Version 3.05. Sunderland, Massachusetts: Sinauer Associates.

    Google Scholar 

  • Maddison, W.P., Donoghue, M.J., & Maddison D.R. (1984) Outgroup analysis and parsimony. Systematic Zoology, 33, 83–103.

    Google Scholar 

  • Mariaux, J. (1996) Cestode systematics: Any progress? International Journal for Parasitology, 26, 231–243.

    Google Scholar 

  • Pavanelli, G. & Rego, A.A. (1991) Cestoides proteocephalideos de Sorubim lima (Schneider, 1801) (Pisces: Pimelodidae) do Rio Parana e reservatorio de Itaipu. Revista Brasileira de Biologia, 51, 7–12.

    Google Scholar 

  • Pritchard, M.H. & Kruse, G.O.W. (1982) The collection and preservation of animal parasites. Lincoln and London: University of Nebraska Press, 141 pp.

    Google Scholar 

  • Rego, A.A. (1987) Cestoides proteocefalideos do Brasil, reorganizaçao taxonomica. Revista Brasileira de Biologia, 47, 203–212.

    Google Scholar 

  • Rego, A.A. (1991) Redescription of Nomimoscolex piraeeba Woodland, 1934 (Cestoda: Proteocephalidea), from the amazon cat-fishes, Brachyplatystoma spp. with proposal of synonyms and invalidation of Endorchiinae and Endorchis. Memorias do Instituto Oswaldo Cruz, 86, 229–232.

    Google Scholar 

  • Rego, A.A. (1994) Order Proteocephalidea Mola, 1928. In: Khalil L.F, Jones A. & Bray R.A. (Eds) Keys to the cestode parasites of vertebrates. Wallingford: CAB International, pp. 257–293.

    Google Scholar 

  • Rego, A.A. (1995) A new classification of the cestode order Proteocephalidea Mola. Revista Brasileira de Zoologia, 12, 791–814.

    Google Scholar 

  • Rego, A.A. & de Chambrier, A. (1995) Crepidobotrium eirasi n. sp. (Cestoda: Proteocephalidae), a parasite of the siluroid fish Phractocephalus hemioliopterus (Schneider, 1801) (Pisces: Pimelodidae from the Brazilian Amazon. Revue Suisse de Zoologie, 102, 3–11.

    Google Scholar 

  • Rego, A.A., Dos Santos, J.C. & Silva, P.P. (1974) Estudos de cestoides de peixes do Brasil. Memorias do Instituto Oswaldo Cruz, 72, 187–204.

    Google Scholar 

  • Rego, A.A., & Pavanelli, G.C. (1985) Jauella glandicephalus gen. n., sp. n. e Megathylacus brooksi sp.n., cestoides patogenicos para o Jau, Paulicea luetkeni, peixe pimelodideos. Revista Brasileira de Biologia, 45, 643–652.

    Google Scholar 

  • Rego, A.A. & Pavanelli, G.C. (1990) Novas especies de cestoides proteocephalideos parasitas de peixes nao siluriformes. Revista Brasileira de Biologia, 50, 91–101.

    Google Scholar 

  • Rego, A.A. & Pavanelli, G.C. (1991) Proteocephalus gibsoni nom. nov. for Proteocephalus ocellatus Rego & Pavanelli, 1990 preoccupied by Proteocephalus ocellatus (Rudolphi, 1802). Revista Brasileira de Biologia, 51, 701.

    Google Scholar 

  • Rego, A.A. & Pavanelli, G.C. (1992) Checklist of the cestode order Proteocephalidea parasites from South America freshwater fishes. Revista Unimar, Maringa, 14(Suppl.), 109–137.

    Google Scholar 

  • Riggenbach, E. (1896) Das Genus Ichthyotaenia. Revue Suisse de Zoologie, 4, 165–275.

    Google Scholar 

  • Schmidt, G.D. (1986) Handbook of tapeworm identification. Boca Raton, Florida: C.R.C. Press Inc., 675 pp.

    Google Scholar 

  • Scholz, T. (1989) Amphilinida and Cestoda, parasites of fish in Czechoslovakia. Acta Scientiarum Naturalium Academiae Scientiarum Bohemoslovacae Brno, 23,No. 4, 56 pp.

  • Scholz, T. (1991) Studies on the development of the cestode Proteocephalus neglectus La Rue, 1911 (Cestoda: Proteocephalidea) under experimental conditions. Folia Parasitologica, 38, 309–318.

    Google Scholar 

  • Scholz, T. (1993) Development of Proteocephalus torulosus (Batsch, 1786) (Cestoda: Proteocephalidae) in the intermediate host under experimental conditions. Journal of Helminthology, 67, 316–324.

    Google Scholar 

  • Scholz, T., de Chambrier, A., Prouza, A. & Royero, R. (1996) Redescription of Proteocephalus macrophallus, a parasite of Cichla ocellaris (Pisces: Cichlidae) from South America. Folia Parasitologica, 43, 287–291.

    Google Scholar 

  • Scholz, T. & Cappellaro, H. (1993) Corallobothrium parafimbriatum Befus et Freeman, 1973 (Cestoda, Proteocephalidae), a parasite of North American catfishes (Ictalurus spp.) newly introduced into Europe. Folia Parasitologica, 40, 105–108.

    Google Scholar 

  • Scholz, T. & Ergens, R. (1990) Cestodes of fishes from Mongolia. Acta Societatis Zoologicae Bohemoslovacae, 54, 287–304.

    Google Scholar 

  • Scholz, T. & Hanzelová, V. (1994) Taxonomic study of two Proteocephalus species (Cestoda: Proteocephalidae) parasitising coregonid fishes: the synonymy of P. fallax La Rue, 1911 with P. exiguus La Rue, 1911. Systematic Parasitology, 27, 1–12.

    Google Scholar 

  • Scholz, T., Hanzelová, V. & Snábel, V. (1995) The taxonomic status of Proteocephalus dubius La Rue, 1911 (Cestoda: Proteocephalidae), a puzzling parasite of perch (Perca fluviatilis L.). Parasite, 2, 231–234.

    Google Scholar 

  • Scholz, T., Spakulová, M., Snábel, V., Kralová, I. & Hanzelová, V. (1997) A multidisciplinary approach to the systematics of Proteocephalus macrocephalus (Cestoda: Proteocephalidae). Systematic Parasitology, 38, 1–12.

    Google Scholar 

  • Swofford, D. (1993) Phylogenetic analysis using parsimony. Version 3.1.1. Computer program distributed by the Illinois Natural History Survey, Champaign, illinois.

  • Thompson, R.C.A., Hayton, A.R. & Jue Sue, L.P. (1980) An ultrastructural study of the microtriches of adult Proteocephalus tidswelli (Cestoda: Proteocephalidea). Zeitschrift für Parasitenkunde, 64, 95–111.

    Google Scholar 

  • Wiley, E.O., Siegel-Causey, D., Brooks, D.R. & Funk, V.A. (1991) The compleat cladist a primer of phylogenetic procedures. Special Publication 19. Lawrence, Kansas: University of Kansas Museum of Natural History, 158 pp.

    Google Scholar 

  • Willemse, J.J. (1968) Proteocephalus filicollis (Rudolphi, 1802) and Proteocephalus ambiguus (Dujardin, 1845), two hitherto confused species of cestodes. Journal of Helminthology, 42, 395–410.

    Google Scholar 

  • Willemse, J.J. (1969) The Genus Proteocephalus in the Netherlands. Journal of Helminthology, 43, 207–222.

    Google Scholar 

  • Woodland, W.N.F. (1933a) On a new subfamily of Proteocephalid cestodes — the Othinoscolecinae — from the Amazon Siluroid fish Platystomatichthys sturio (Kner). Parasitology, 25, 491–500.

    Google Scholar 

  • Woodland, W.N.F. (1933b) On the anatomy of some fish cestodes described by Diesing from the Amazon. Quarterly Journal of Microscopical Science, 76, 175–208.

    Google Scholar 

  • Woodland, W.N.F. (1933c) On two new cestodes from the Amazon siluroid fish Brachyplatystoma vaillanti Cuv. and Val. Parasitology, 25, 485–490.

    Google Scholar 

  • Woodland, W.N.F. (1934a) On the Amphilaphorchidinae, a new subfamily of Proteocephalid cestodes, and Myzophorus admonticellia, gen. and sp. n., parasitic in Pirinampus spp. from the Amazon. Parasitology, 26, 141–149.

    Google Scholar 

  • Woodland, W.N.F. (1934b) On some remarkable new cestodes from the Amazon siluroid fish, Brachyplatystoma filamentosum (Lichtenstein). Parasitology, 26, 268–277.

    Google Scholar 

  • Woodland, W.N.F. (1934c) On six new Cestodes from Amazon Fishes. Proceedings of the Zoological Society London, 104, 33–44.

    Google Scholar 

  • Woodland, W.N.F. (1935a) Additional cestodes from the Amazon siluroids Pirarará, Dorad and Sudobim. Proceedings of the Zoological Society London, 104, 851–862.

    Google Scholar 

  • Woodland, W.N.F. (1935b) Some more remarkable cestodes from Amazon siluroids fish. Parasitology, 27, 207–225.

    Google Scholar 

  • Woodland, W.N.F. (1935 c) Some new proteocephalids and a ptychobothriid (Cestoda) from the Amazon. Proceedings of the Zoological Society of London, 105, 619–623.

    Google Scholar 

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Authors and Affiliations

  1. Department of Helminthology, Instituto Oswaldo Cruz, PO Box 926, 21045-900, Rio de Janeiro, Brasil (with financial support of CNPq, Brasil)

    Amilcar Arandas Rego

  2. Department of Invertebrates, Natural History Museum, PO Box 6434, 1211, Geneva 6, Switzerland

    Alain de Chambrier

  3. Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 040 01, Kosice, Slovak Republic

    Vladimira Hanzelová

  4. United States Department of Agriculture, Agricultural Research Service, Biosystematics and National Parasite Collection Unit, BARC East, Building 1180, 10300 Baltimore Avenue, Beltsville, Maryland, 20705-2350, USA

    Eric Hoberg

  5. Institute of Parasitology, Academy of Sciences of the Czech Republic, Branisovska 31, 370 05 Ceské, Budejovice, Czech Republic

    Tomás Scholz

  6. Institute of Environmental Science & Research Limited, Communicable Disease Centre, Kenepuru Drive, PO Box 50-348, Porirua, New Zealand

    Peter Weekes

  7. Institut de Zoologie, Université de Neuchâtel, E.-Argand 11, 2007, Neuchâtel, Switzerland

    Marc Zehnder

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Rego, A.A., de Chambrier, A., Hanzelová, V. et al. Preliminary phylogenetic analysis of subfamilies of the Proteocephalidea (Eucestoda). Syst Parasitol 40, 1–19 (1998). https://doi.org/10.1023/A:1005903506363

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