Abstract
Phylogenetic relationships of all genera of the order Caryophyllidea, possibly the earliest branching group of true tapeworms (Platyhelminthes: Eucestoda) and the only one that is monozoic, have been assessed for the first time. Results of this cladistic analysis, inferred from 30 unweighted morphological characters, are only partly congruent with the existing classification, which consists of four families based on the position of the inner longitudinal muscles in relation to the internal genital organs. Whereas all but five genera of the Caryophyllaeidae form a monophyletic clade, members of the Capingentidae are split, occurring within six unrelated groups. The Lytocestidae is also paraphyletic, as some genera appear in four unrelated clades. Archigetes appears in a derived clade, indicating that its direct (monoxenous) life-cycle involving only tubificid oligochaetes is secondarily derived and not plesiomorphic among the Eucestoda, as postulated by some authors.
Similar content being viewed by others
References
Beveridge, I., Campbell, R. A., & Palm, H. W. (1999). Preliminary cladistic analysis of genera of the cestode order Trypanorhyncha Diesing, 1863. Systematic Parasitology, 42, 29–49.
Bovien, P. (1926). Caryophyllaeidae from Java. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening, 82, 157–181.
Bray, R. A., Jones, A., & Hoberg, E. P. (1999). Observations on the phylogeny of the cestode order Pseudophyllidea Carus, 1863. Systematic Parasitology, 42, 13–20.
Brabec, J., Kuchta, R., & Scholz, T. (2006). Paraphyly of the Pseudophyllidea (Platyhelminthes: Cestoda): Circumscription of monophyletic clades based on phylogenetic analysis of ribosomal RNA. International Journal for Parasitology, 36, 1535–1541.
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.
Caira, J. N., Jensen, K., & Healy, C. J. (1999). On the phylogenetic relationships among tetraphyllidean, lecanicephalidean and diphyllidean tapeworm genera. Systematic Parasitology, 42, 77–151.
Caira, J. N., & Jensen, K. (2001). An investigation of the co-evolutionary relationships between onchobothriid tapeworms and their elasmobranch hosts. International Journal for Parasitology, 31, 960–975.
Calentine, R. (1962). Archigetes iowensis sp. n. (Cestoda: Caryophyllaeidae) from Cyprinus carpio L. and Limnodrilus hoffmeisteri Claparede. Journal of Parasitology, 48, 513–524.
Cohn, L. (1908). Die Anatomie eines neuen Fischcestoden. Centralblatt für Bakteriologie, Parasitenkunde und Infectionkrankenheiten, 46, 134–139.
de Chambrier, A., Zehnder, M., Vaucher, C., & Mariaux, J. (2004). The evolution of the Proteocephalidea (Platyhelminthes, Eucestoda) based on an enlarged molecular phylogeny, with comments on their uterine development. Systematic Parasitology, 57, 159–171.
Gupta, S. P. (1961). Caryophyllaeids (Cestoda) from freshwater fishes of India. Proceedings of the Helminthological Society of Washington, 28, 38–50.
Hall, B. G. (2004). Phylogenetic trees made easy (221 pp). Sunderland, Massachusetts: Sinauer Associates.
Hoberg, E. P., Mariaux, J., Justine, J. L., Brooks, D. R., & Weekes, P. J. (1997). Phylogeny of the orders of the Eucestoda (Cercomeromorphae) based on comparative morphology: Historical perspectives and a new working hypothesis. Journal of Parasitology, 83, 1128–1147.
Hoberg, E. P., Mariaux, J., & Brooks, D. R. (2001). Phylogeny among orders of the Eucestoda (Cercomeromorphae): Integrating morphology, molecules and total evidence. In D. T. J. Littlewood & R. A. Bray (Eds.), Interrelationships of the Platyhelminthes (pp. 112–126). London, New York: Taylor and Francis.
Hypša, V., Škeříková, A., & Scholz, T. (2005). Phylogeny, evolution and host-parasite relationships of the order Proteocephalidea (Eucestoda) as revealed by combined analysis and secondary structure characters. Parasitology, 130, 359–371.
Ivanov, V. A., & Hoberg, E. P. (1999). Preliminary comments on a phylogenetic study of the order Diphyllidea van Beneden in Carus, 1863. Systematic Parasitology, 42, 21–27.
Janiszewska, J. (1950). Paraglaridacris silesiacus n. g., n. sp. de la famille Caryophyllaeidae. Zoologica Poloniae, 5, 67–72.
Kodedová, I., Doležel, D., Broučková, M., Jirků, M., Hypša, V., Lukeš, J., & Scholz, T. (2000). On the phylogenetic positions of the Caryophyllidea, Pseudophyllidea and Proteocephalidea (Eucestoda) inferred from 18S rRNA. International Journal for Parasitology, 30, 1109–1113.
Kuchta, R., Scholz, T., Brabec, J., & Bray, R. A. (2008). Dissolution of the tapeworm order Pseudophyllidea (Platyhelminthes: Eucestoda) and the proposal of two new orders, Bothriocephalidea and Diphyllobothriidea. International Journal for Parasitology, 38, 49–55.
Kulakovskaya, O. P. (1962). Progenetichni gvozdichniki (Caryophyllaeidae, Cestoda) v tili oligochet. Dopovidi Akademii Nauk Ukrayin’skoi SSR, 6, 825–829 (In Ukrainian).
Lipscomb, D. (1998). Basics of cladistic analysis. Washington, DC: George Washington University, 74 pp [PDF].
Mackiewicz, J. S. (1962). Hunterella nodulosa gen. n., sp. n. (Cestoidea: Caryophyllaeidae) from Catostomus commersoni (Lacépède) (Pisces: Catostomidae). Journal of Parasitology, 48, 798–806.
Mackiewicz, J. S. (1972). Caryophyllidea (Cestoidea): A review. Experimental Parasitology, 34, 417–512.
Mackiewicz, J. S. (1981). Caryophyllidea (Cestoidea): Evolution and classification. Advances in Parasitology, 19, 139–206.
Mackiewicz, J. S. (1982). Caryophyllidea (Cestoidea): Perspectives. Parasitology, 84, 397–417.
Mackiewicz, J. S. (1994). Order Caryophyllidea van Beneden in Carus, 1863. In L. F. Khalil, A. Jones, & R. A. Bray (Eds.), Keys to the cestode parasites of vertebrates (pp. 21–43). Wallingford: CAB International.
Mackiewicz, J. S. (2003). Caryophyllidea (Cestoidea): Molecules, morphology and evolution. Acta Parasitologica, 48, 143–154.
Mariaux, J. (1998). A molecular phylogeny of the Eucestoda. Journal of Parasitology, 84, 114–124.
Olson, P. D., & Caira, J. N. (1999). Evolution of the major lineages of tapeworms (Platyhelminthes: Cestoidea) inferred from 18S ribosomal DNA and elongation factor-1-α. Journal of Parasitology, 85, 1134–1159.
Olson, P. D., Littlewood, D. T. J., Bray, R. A., & Mariaux, J. (2001). Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Molecular Phylogenetics and Evolution, 19, 443–467.
Olson, P. D., Scholz, T., Poddubnaya, L. G., & Littlewood, D. T. J. (2008). On the derived position of Archigetes and the early evolution of the tapeworms (Platyhelminthes: Cestoda). Journal of Parasitology (in press).
Olson, P. D., & Tkach, V. V. (2005). Advances and trends in the molecular systematics of the parasitic Platyhelminthes. Advances in Parasitology, 60, 165–243.
Page, R. D. M. (1996). TREEVIEW: An application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences, 12, 357–358.
Poddubnaya, L., Mackiewicz, J. S., & Kuperman, B. I. (2003). Ultrastructure of Archigetes sieboldi (Cestoda: Caryophyllidea): Relationship between progenesis, development and evolution. Folia Parasitologica, 50, 275–292.
Rego, A. A. (1994). Order Proteocephalidea Mola, 1928. In L. F. Khalil, A. Jones, & R. A. Bray (Eds.), Keys to the cestode parasites of vertebrates (pp. 257–293). Wallingford: CAB International.
Rego, A. A., de Chambrier, A., Hanzelová, V., Hoberg, E., Scholz, T., Weekes, P., & Zehnder, M. (1998) .Preliminary phylogenetic analysis of subfamilies of the Proteocephalidea (Eucestoda). Systematic Parasitology, 40, 1–9.
Stunkard, H. W. (1967). Platyhelminth parasites of invertebrates. Journal of Parasitology, 53, 673–682.
Škeříková, A., Hypša, V., & Scholz, T. (2001). Phylogenetic analysis of European species of Proteocephalus (Cestoda: Proteocephalidea): Compatibility of molecular and morphological data, and parasite-host coevolution. International Journal for Parasitology, 31, 1121–1128.
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.
Wiley, E. O., Siegel-Causey, D., Brooks, D. R., & Funk, V. A. (1991). The compleat cladist: a primer of phylogenetic procedures (158 pp). Lawrence, Kansas: University of Kansas.
Zehnder, M. P., & Mariaux, J. (1999). Molecular systematic analysis of the order Proteocephalidea (Eucestoda) based on mitochondrial and nuclear rDNA sequences. International Journal for Parasitology, 29, 1841–1852.
Acknowledgements
The authors are indebted to Eric P. Hoberg and Patricia Pilitt, US National Parasite Collection, Beltsville, USA, Agustín Jiménez-Ruiz, H.W. Manter Laboratory, University of Nebraska State Museum, Lincoln, USA, and Ian Whittington and David Stemmer, South Australian Museum, Adelaide, Australia for providing type- and voucher specimens for this study, and Blanka Škoríková, Institute of Parasitology, for help with preparation of figures. Invaluable suggestions of three anonymous referees have helped considerably in improving the present paper and are greatly appreciated, as is the thorough editing of the manuscript by D.I. Gibson. M.O. is grateful for the financial support to the European Commission (Research Infrastructure Action via the SYNTHESYS Project: AT-TAF-411, HU-TAF-300, GB-TAF-1135, DK-TAF-2354). This study was supported by the Scientific Grant Agency of Slovakia (VEGA, project No. 2/7192/27), Czech Science Foundation (GA ČR, project 524/08/0885), research projects of the Institute of Parasitology (Z60220518, LC 522), SYNTHESYS Programme of the EU (GE-TAF-127, FR-TAF-1139), and the Grant Agency of the Slovak Republic (AVVP, project No. 51-062205).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Oros, M., Hanzelová, V., Scholz, T. et al. Phylogenetic relationships of the monozoic tapeworms (Eucestoda: Caryophyllidea) inferred from morphological characters. Syst Parasitol 70, 1–14 (2008). https://doi.org/10.1007/s11230-008-9133-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11230-008-9133-y