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A preliminary phylogenetic analysis of the Capsalidae (Platyhelminthes: Monogenea: Monopisthocotylea) inferred from large subunit rDNA sequences

Published online by Cambridge University Press:  06 May 2004

I. D. WHITTINGTON
Affiliation:
Monogenean Research Laboratory, Parasitology Section, The South Australian Museum, North Terrace, Adelaide, South Australia 5000, Australia Marine Parasitology Laboratory, Environmental Biology, School of Earth and Environmental Sciences, The University of Adelaide, North Terrace, Adelaide, South Australia 5005, Australia
M. R. DEVENEY
Affiliation:
PIRSA Aquaculture, Primary Industry and Resources South Australia, GPO Box 1625, Adelaide, South Australia 5001, Australia
J. A. T. MORGAN
Affiliation:
Department of Microbiology and Parasitology, The University of Queensland, Brisbane, Queensland 4072, Australia Present address: Department of Plant and Microbial Biology, University of California Berkeley, CA 94720-3102, USA.
L. A. CHISHOLM
Affiliation:
Marine Parasitology Laboratory, Environmental Biology, School of Earth and Environmental Sciences, The University of Adelaide, North Terrace, Adelaide, South Australia 5005, Australia
R. D. ADLARD
Affiliation:
Department of Microbiology and Parasitology, The University of Queensland, Brisbane, Queensland 4072, Australia Biodiversity Program, Queensland Museum, PO Box 3300, South Brisbane, Queensland 4101, Australia

Abstract

Phylogenetic relationships within the Capsalidae (Monogenea) were examined using large subunit ribosomal DNA sequences from 17 capsalid species (representing 7 genera, 5 subfamilies), 2 outgroup taxa (Monocotylidae) plus Udonella caligorum (Udonellidae). Trees were constructed using maximum likelihood, minimum evolution and maximum parsimony algorithms. An initial tree, generated from sequences 315 bases long, suggests that Capsalinae, Encotyllabinae, Entobdellinae and Trochopodinae are monophyletic, but that Benedeniinae is paraphyletic. Analyses indicate that Neobenedenia, currently in the Benedeniinae, should perhaps be placed in a separate subfamily. An additional analysis was made which omitted 3 capsalid taxa (for which only short sequences were available) and all outgroup taxa because of alignment difficulties. Sequence length increased to 693 bases and good branch support was achieved. The Benedeniinae was again paraphyletic. Higher-level classification of the Capsalidae, evolution of the Entobdellinae and issues of species identity in Neobenedenia are discussed.

Type
Research Article
Copyright
2004 Cambridge University Press

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References

REFERENCES

BAUER, O. N. & HOFFMAN, G. L. (1976). Helminth range extension by translocation of fish. In Wildlife Diseases (ed. Page, L. A. ), pp. 163172. Plenum, New York.CrossRef
BOEGER, W. A. & KRITSKY, D. C. (1997). Coevolution of the Monogenoidea (Platyhelminthes) based on a revised hypothesis of parasite phylogeny. International Journal for Parasitology 27, 14951511.CrossRefGoogle Scholar
BYCHOWSKY, B. E. (1957). Monogenetic Trematodes, their Systematics and Phylogeny. Izdatel'suo Akademiya Nauk SSSR, Moscow. [In Russian: English translation edited by Hargis, W. J. Jr., 1961.]
CHISHOLM, L. A., WHITTINGTON, I. D., MORGAN, J. A. T. & ADLARD, R. D. (2001 a). The Calicotyle conundrum: do molecules reveal more than morphology? Systematic Parasitology 49, 8187.Google Scholar
CHISHOLM, L. A., MORGAN, J. A. T., ADLARD, R. D. & WHITTINGTON, I. D. (2001 b). Phylogenetic analysis of the Monocotylidae (Monogenea) inferred from 28S rDNA sequences. International Journal for Parasitology 31, 12531263.Google Scholar
DEVENEY, M. R., CHISHOLM, L. A. & WHITTINGTON, I. D. (2001). First published record of the pathogenic monogenean parasite Neobenedenia melleni (Capsalidae) from Australia. Diseases of Aquatic Organisms 46, 7982.CrossRefGoogle Scholar
EGOROVA, T. P. (1989). A taxonomic analysis of the subfamily Capsalinae (Monogenoidea: Capsalidae). In Parazitologicheskie Issledovaniya: sbornik nauchnykh trudov. Dal'nevostochnoe otdelenie (ed. Lebedev, B. I.), pp. 4654. Akademiya Nauk SSSR, Vladivostok. [In Russian.]
EGOROVA, T. P. (1994 a). A taxonomic review of the subfamily Trochopodinae (Monogenoidea: Capsalidae). Parazitologiya 28, 8191. [In Russian.]Google Scholar
EGOROVA, T. P. (1994 b). About a new genus, Megalobenedenia (Capsalidae: Trochopodinae). Parazitologiya 28, 7678. [In Russian.]Google Scholar
EGOROVA, T. P. (1997). A taxonomic review of the subfamily Benedeniinae (Monogenoidea: Capsalidae). Parazitologiya 31, 438451. [In Russian.]Google Scholar
EGOROVA, T. P. (1999). Systematics of the subfamily Entobdellinae (Monogenoidea: Capsalidae). Parazitologiya 33, 420425. [In Russian.]Google Scholar
EGOROVA, T. P. (2000 a). New monogeneans of the genus Dionchus (Capsalidae: Dionchinae). Parazitologiya 34, 252258. [In Russian.]Google Scholar
EGOROVA, T. P. (2000 b). Occurrence of monogeneans of the subfamily Capsalinae (Capsalidae) – parasites of marine fishes. Parazitologiya 34, 111117. [In Russian.]Google Scholar
EGOROVA, T. P. (2000 c). Recent composition of the subfamily Encotyllabinae (Monogenea: Capsalidae). Parazitologiya 34, 295301. [In Russian.]Google Scholar
HASSOUNA, N., MICHOT, B. & BACHELLERIE, J. P. (1984). The complete nucleotide sequence of mouse 28S rRNA gene. Implications for the process of size increase of the large subunit rRNA in higher eukaryotes. Nucleic Acids Research 12, 35633583.Google Scholar
HORTON, M. A. & WHITTINGTON, I. D. (1994). A new species of Metabenedeniella (Monogenea: Capsalidae) from the dorsal fin of Diagramma pictum (Perciformes: Haemulidae) from the Great Barrier Reef, Australia with a revision of the genus. Journal of Parasitology 80, 9981007.CrossRefGoogle Scholar
HUELSENBECK, J. P. & CRANDALL, K. A. (1997). Phylogeny estimation and hypothesis testing using maximum likelihood. Annual Review of Ecological Systematics 28, 437466.CrossRefGoogle Scholar
KEARN, G. C. (1963). The egg, oncomiracidium and larval development of Entobdella soleae, a monogenean skin parasite of the common sole. Parasitology 53, 435447.CrossRefGoogle Scholar
KEARN, G. C. (1998). Parasitism and the Platyhelminths. Chapman & Hall, London.
KHALIL, L. F. & ABDUL-SALAM, J. F. (1988). The subfamily Encotyllabinae (Monogenea: Capsalidae) with the description of Alloencotyllabe caranxi n. g., n. sp. and Encotyllabe kuwaitensis n. sp. Systematic Parasitology 11, 139150.Google Scholar
KLASSEN, G. J., BEVERLEY-BURTON, M. & LOCKE, A. (1989). A revision of Entobdella Blainville (Monogenea: Capsalidae) with particular reference to E. hippoglossi and E. squamula: the use of ratios in taxonomy and key to species. Canadian Journal of Zoology 67, 18691876.Google Scholar
KRITSKY, D. C. & FENNESSY, C. J. (1999). Calicobenedenia polyprioni n. gen., n. sp. (Monogenoidea: Capsalidae) from the external surfaces of wreckfish, Polyprion americanus (Teleostei: Polyprionidae), in the North Atlantic. Journal of Parasitology 85, 192195.Google Scholar
LAMOTHE-ARGUMEDO, R. (1997). Nuevo arreglo taxonomico de la subfamilia Capsalinae (Monogenea: Capsalinae) clave para los generos y dos combinaciones nuevas. Anales del Instituto de Biología, Universidad Nacional Autónoma de Mexico, Serie Zoología 68, 207223.Google Scholar
MOLLARET, I., JAMIESON, B. G. M., ADLARD, R. D., HUGALL, A., LECOINTRE, G., CHOMBARD, C. & JUSTINE, J.-L. (1997). Phylogenetic analysis of the Monogenea and their relationships with Digenea and Eucestoda inferred from 28S rDNA sequences. Molecular and Biochemical Parasitology 90, 433438.CrossRefGoogle Scholar
MOLLARET, I., JAMIESON, B. G. M. & JUSTINE, J.-L. (2000). Phylogeny of the Monopisthocotylea and Polyopisthocotylea (Platyhelminthes) inferred from 28S rDNA sequences. International Journal for Parasitology 30, 171185.CrossRefGoogle Scholar
NICHOLAS, K. B., NICHOLAS, H. B. Jr. & DEERFIELD, D. W. II (1997). Home page for GeneDoc. http://www.psc.edu/biomed/genedoc
OGAWA, K., BONDAD-REANTASO, M., FUKUDOME, M. & WAKABAYASHI, H. (1995 a). Neobenedenia girellae (Hargis, 1955) Yamaguti, 1963 (Monogenea: Capsalidae) from cultured marine fishes of Japan. Journal of Parasitology 81, 223227.Google Scholar
OGAWA, K., BONDAD-REANTASO, M. G. & WAKABAYASHI, H. (1995 b). Redescription of Benedenia epinepheli (Yamaguti, 1937) Meserve, 1938 (Monogenea: Capsalidae) from cultured and aquarium marine fishes of Japan. Canadian Journal of Fisheries and Aquatic Sciences 52, 6270.Google Scholar
OLSON, P. D. & LITTLEWOOD, D. T. J. (2002). Phylogenetics of the Monogenea – evidence from a medley of molecules. International Journal for Parasitology 32, 233244.CrossRefGoogle Scholar
PAPERNA, I. & OVERSTREET, R. M. (1981). Parasites and diseases of mullets (Muglidae). In Aquaculture of Grey Mullets (ed. Oren, O. H. ), pp. 411493. Cambridge University Press, Cambridge.
POSADA, D. & CRANDALL, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817818.CrossRefGoogle Scholar
SPROSTON, N. G. (1946). A synopsis of the monogenetic trematodes. Transactions of the Zoological Society of London 25, 185600.Google Scholar
SURIANO, D. M. & BEVERLEY-BURTON, M. (1979). Interniloculus chilensis gen. et sp. nov. (Monogenea: Capsalidae) representant d'une nouvelle sous-famille: Interniloculinae parasite des branchies de Helicolenus lengerichi Norman (Pisces: Scorpenidae) de l'Ocean Pacifique Sud. Canadian Journal of Zoology 57, 12011205.Google Scholar
SWOFFORD, D. L. (2001). PAUP* Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0b8 (PPC). Sinauer Associates, New York.
THOMPSON, J. D., GIBSON, T. J., PLEWNIAK, F., JEANMOUGIN, F. & HIGGINS, D. G. (1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24, 48764882.CrossRefGoogle Scholar
TIMOFEEVA, T. A. (1990). Phylogenetic relationships of capsalids and dionchids and the position of the latter in the system of monogeneans (Monogenea, Monopisthocotylea). Trudy Zoologicheskogo Instituta 221, 316. [In Russian.]Google Scholar
WHITTINGTON, I. D. (1994). Graham C. Kearn. An appreciation. International Journal for Parasitology 24, 481486.CrossRefGoogle Scholar
WHITTINGTON, I. D. (1996). Benedeniine (capsalid) monogeneans from Australian fishes: pathogenic species, site-specificity and camouflage. Journal of Helminthology 70, 177184.CrossRefGoogle Scholar
WHITTINGTON, I. D. & HORTON, M. A. (1996). A revision of Neobenedenia Yamaguti, 1963 (Monogenea: Capsalidae) including a redescription of N. melleni (MacCallum, 1927) Yamaguti, 1963. Journal of Natural History 30, 11131156.Google Scholar
WHITTINGTON, I. D., CORNEILLIE, S., TALBOT, C., MORGAN, J. A. T. & ADLARD, R. D. (2001 a). Infections of Seriola quinqueradiata Temminck & Schlegel and S. dumerili (Risso) in Japan by Benedenia seriolae (Monogenea) confirmed by morphology and 28S ribosomal DNA analysis. Journal of Fish Diseases 24, 421425.Google Scholar
WHITTINGTON, I. D., DEVENEY, M. R. & WYBORN, S. J. (2001 b). A revision of Benedenia Diesing, 1858 including a redescription of B. sciaenae (van Beneden, 1856) Odhner, 1905 and recognition of Menziesia Gibson, 1976 (Monogenea: Capsalidae). Journal of Natural History 35, 663777.Google Scholar
YAMAGUTI, S. (1963). Systema Helminthum. Volume IV. Monogenea and Aspidocotylea. InterScience Publishers, New York.
YAMAGUTI, S. (1965). New monogenetic trematodes from Hawaiian fishes, I. Pacific Science 19, 5595.Google Scholar