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The radiation of Haliotrema (Monogenea: Dactylogyridae: Ancyrocephalinae): molecular evidence and explanation inferred from LSU rDNA sequences

Published online by Cambridge University Press:  09 January 2006

X. Y. WU ,
X. Q. ZHU ,
M. Q. XIE  and
A. X. LI
X. Y. WU
Affiliation:
School of Life Sciences, Sun Yat-sen University, 135 Xingang West Street, Haizhu District, Guangzhou 510275, Guangdong Province, The People's Republic of China
X. Q. ZHU
Affiliation:
Laboratory of Parasitology, College of Veterinary Medicine, South China Agricultural University, 483 Wushan Street, Tianhe District, Guangzhou 510642, Guangdong Province, The People's Republic of China
M. Q. XIE
Affiliation:
School of Life Sciences, Sun Yat-sen University, 135 Xingang West Street, Haizhu District, Guangzhou 510275, Guangdong Province, The People's Republic of China
A. X. LI
Affiliation:
School of Life Sciences, Sun Yat-sen University, 135 Xingang West Street, Haizhu District, Guangzhou 510275, Guangdong Province, The People's Republic of China
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Abstract

The D1-D2 domains of LSU rDNA were used to reconstruct the phylogenetic relationships within the Ancyrocephalinae (Monogenea: Dactylogyridae) utilizing maximum-parsimony (MP), maximum-likelihood (ML), minimum evolution (ME) and neighbour-joining (NJ) methods. A total of 32 monogenean taxa were examined in the present study, including 9 Haliotrema species and 13 other species representing the Ancyrocephalinae, 4 Thaparocleidus species representing the Ancylodiscoididae, and 6 species representing the Diplectanidae which were used as multiple outgroups. All 4 analyses (i.e. MP, ML, ME and NJ) inferred the same interrelationship pattern: (Diplectanidae, (Ancylodiscoididae, Dactylogyridae)) with high bootstrap support. However, 9 Haliotrema species were dispersed to form 4 clades together with species from other genera, indicating the apparent non-monophyly of Haliotrema. Three major groups were defined based on reconstructed phylogenetic trees to explain the radiation of Haliotrema species. The morphology of the reproductive organ, particularly the male copulatory organ (MCO), was discussed to further understand the formation of each group. (1) Results of the present study indicated an intimate relationship among Metahaliotrema (2 species), Protogyrodactylus (4 species) and Haliotrema (2 of 9 species), and notably, all these species share vagina-absence. (2) Based on the present molecular analyses and the morphological characters of the MCO, we propose to transfer H. spirotubiforum and the undetermined Haliotrema sp. ZHDDb to Euryhaliotrema as new combinations. (3) We propose to erect a new genus to accommodate the Haliotrema species with horn-like shaped MCO. Taxonomic implications of the present molecular phylogenetic analyses are discussed. A wider range of taxa and more DNA markers displaying various evolutionary rates should be used to estimate phylogenetic relationships among species within the Ancyrocephalinae and Ancylodiscoididae in further studies.

Keywords

AncyrocephalinaeAncylodiscoididaeDactylogyridaeHaliotremaLSU rDNAphylogeny
Type
Research Article
Information
Parasitology , Volume 132 , Issue 5 , May 2006 , pp. 659 - 668
Copyright
2006 Cambridge University Press

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References

REFERENCES

Beverley-Burton, M. and Klassen, G. J. ( 1990). New approaches to the systematics of the Ancyrocephalid Monogenea from Nearcric freshwater fishes. Journal of Parasitology 76, 1–12.Google Scholar
Beverley-Burton, M. and Suriano, D. M. ( 1981). Onchocleidus ferox (Mueller, 1934) and O. similis Mueller, 1936 (Monogenea: Ancyrocephalinae) from Lepomis gibbosus L. (Pisces: Centrarchidae) in Ontario, Canada: anatomy, systematic position and possible evolution. Canadian Journal of Zoology 59, 1161–1171.Google Scholar
Boeger, W. A. and Kritsky, D. C. ( 1997). Coevolution of the Monogenoidea (Platyhelminthes) based on a revised hypothesis of parasite phylogeny. International Journal for Parasitology 27, 1495–1511. DOI: 10.1016/S0020-7519(97)00140-9.CrossRefGoogle Scholar
Boeger, W. A. and Kritsky, D. C. ( 2001). Phylogenetic relationship of the Monogenoidea. In Interrelationships of the Platyhelminthes ( ed. Littlewood, D. T. J. and Bray, R. A.), pp. 92–102. Taylor and Francis, London.
Boeger, W. A., Kritsky, D. C. and Pie, M. R. ( 2003). Context of diversification of the viviparous Gyrodactylidae (Platyhelminthes, Monogenoidea). Zoologica Scripta 32, 437–448. DOI: 10.1046/j.1463-6409.2003.00130.x.CrossRefGoogle Scholar
Bychowsky, B. E. ( 1957). [Monogenetic Trematodes. Their Systematics and Phylogeny]Moscow-Leningrad: Izdatel'stvo Akademiya Nauk SSSR. (In Russian.)
Bychowsky, B. E. and Nagibina, L. F. ( 1978). Revision of Ancyrocephalinae Bychowsky, 1937. Parazitologicheskii Sbornik 28, 5–15.Google Scholar
Chisholm, L. A., Morgan, J. A. T., Adlard, R. D. and Whittington, I. D. ( 2001). Phylogenetic analysis of the Monocotylidae (Monogenea) inferred from 28S rDNA sequences. International Journal for Parasitology 31, 1253–1263. PII: S0020-7519(01)00223-5.CrossRefGoogle Scholar
Euzet, L. and Suriano, D. M. ( 1977). Ligophorus n.g. (Monogenea: Ancyrocephalidae) parasite des Mugilidae (Téléostéens) en Méditerranée. Bulletin of the American Museum of Natural History 329, 799–822.Google Scholar
Gussev, A. V. ( 1961). [The new subfamily of monogenean parasites (Monogenoidea).] Doklady Akademii Nauk 139, 1480–1482. (In Russian.)Google Scholar
Gussev, A. V. ( 1978). Monogenoidea of freshwater fishes. Principles of systematics, analysis of world fauna and its evolution. Parazitologicheskii Sbornik 28, 96–198. (In Russian.)Google Scholar
Gussev, A. V. ( 1985). Identification of Freshwater Fish Parasites. 2. Metazoan Parasites (Part 1). Nauka Publishers, Leningrad.
Jovelin, R. and Justine J.-L. ( 2001). Phylogenetic relationships within the polyopisthocotylean monogeneans (Platyhelminthes) inferred from partial 28S rDNA sequences. International Journal for Parasitology 31, 393–401. PII: S0020-7519(01)00114-X.CrossRefGoogle Scholar
Justine, J.-L., Jovelin, R., Neifar, R., Mollaret, I., Lim, L. H. S., Hendrix, S. S. and Euzet, L. ( 2002). Phylogenetic positions of the Bothitrematidae and Neocalceostomatidae (Monoopisthocotylean Monogeneans) inferred from 28S rDNA sequences. Comparative Parasitology 69, 20–25.CrossRefGoogle Scholar
Klassen, G. J. ( 1994 a). Phylogeny of Haliotrema species (Monogenea: Ancyrocephalidae) from boxfishes (Tetraodontiformes: Ostraciidae): are Haliotrema species from boxfishes monophyletic? Journal of Parasitology 80, 596–610.Google Scholar
Klassen, G. J. ( 1994 b). On the monophyly of Haliotrema species (Monogenea: Ancyrocephalidae) from boxfishes (Tetraodontiformes: Ostraciidae): relationships within the Bodiani group. Journal of Parasitology 80, 611–619.Google Scholar
Kritsky, D. C. and Boeger, W. A. ( 1989). The phylogenetic status of the Ancyrocephalidae Bychowsky, 1937 (Monogenea: Dactylogyridea). Journal of Parasitology 75, 207–211.CrossRefGoogle Scholar
Kritsky, D. C. and Boeger, W. A. ( 2002). Neotropical Monogenoidea. 41. New and previously described species of Dactylogyridae (Platyhelminthes) from the gills of marine and freshwater perciform fishes (Teleostei) with proposal of a new genus and a hypothesis on phylogeny. Zoosystema 24, 7–40.Google Scholar
Kritsky, D. C. and Stephens, F. ( 2001). Haliotrema abaddon n. sp. (Monogenoidea: Dactylogyridae) from the gills of wild and maricultured West Australian dhufish Glaucosoma hebraicum (Teleostei: Glaucosomatidae), in Australia. Journal of Parasitology 87, 749–754.Google Scholar
Kumar, S., Tamura, K. and Nei, M. ( 2004). MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.CrossRefGoogle Scholar
Le Brun, N., Lambert, A. and Justine, J.-L. ( 1986). Oncomiracidium, morphogenèse du hapteur et ultrastructure du spermatozoide de Pseudodactylogyrus anguillae (Yin et Sproston, 1948) Gussev, 1965 (Monogenea, Monopisthocotylea, Pseudodactylogyridae n. fam.). Annales de Parasitologie Humaine et Comparée 61, 273–284.CrossRefGoogle Scholar
Lim, L. H. S. ( 1998). Diversity of monogeneans in Southeast Asia. International Journal for Parasitology 28, 1495–1515.CrossRefGoogle Scholar
Lim, L. H. S., Timofeeva, T. A. and Gibson, D. I. ( 2001). Dactylogyridean monogeneans of the siluriform fishes of the Old World. Systematic Parasitology 50, 159–197.CrossRefGoogle Scholar
Littlewood, D. T. J., Rohde, K. and Clough, K. A. ( 1998). The phylogenetic position of Udonella (Platyhelminthes). International Journal for Parasitology 28, 1241–1250. PII: S0020-7519(98)00108-8.CrossRefGoogle Scholar
Meinilä, M., Kuusela, J., Ziętars, M. S. and Lumme, J. ( 2004). Initial steps of speciation by geographic isolation and host switch in salmonid pathogen Gyrodactylus salaris (Monogenea: Gyrodactylidae). International Journal for Parasitology 34, 515–526. DOI: 10.1016/j.ijpara.2003.12.002.CrossRefGoogle Scholar
Mollaret, I., Jamieson, B. G. M. and Justine, J.-L. ( 2000 a). Phylogeny of the Monopisthocotylea and Polyopisthocotylea (Platyhelminthes) inferred from 28S rDNA sequences. International Journal for Parasitology 30, 171–185. PII: S0020-7519(99)00197-6.Google Scholar
Mollaret, I., Jamieson, B. G. M., Adlard, R. D., Hugall, A., Lecointre, G., Chombard, C. and 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, 433–438.CrossRefGoogle Scholar
Mollaret, I., Lim, L. H. S. and Justine, J.-L. ( 2000 b). Phylogenetic position of the monogeneans Sundanonchus, Thaparocleidus, and Cichlidogyrus inferred from 28S rDNA sequences. International Journal for Parasitology 30, 659–662. PII: S0020-7519(00)00039-4.Google Scholar
Ogawa, K. ( 1986). Pseudodactylogyroides gen. n. (Monogenea: Ancyrocephalidae, Pseudodactylogyrinae sub. n.), with a re-description of P. apogonis (Yamaguti, 1940) comb. n. Zoological Science 3, 181–185.Google Scholar
Olson, P. D. and Littlewood, D. T. J. ( 2002). Phylogenetics of the Monogenea – evidence from a medley of molecules. International Journal for Parasitology 32, 233–244. PII: S0020-7519(01)00328-9.CrossRefGoogle Scholar
Pariselle, A. and Euzet, L. ( 1995). Scutogyrus gen. n. (Monogenea, Ancyrocephalidae) for Cichlidogyrus longicornis minus Dossou, 1982, C. l. longicornis, and C. l. gravivaginus Paperna and Thurston, 1969, with description of three new species parasitic on African Cichlids. Journal of the Helminthology Society of Washington 62, 188–205.Google Scholar
Plaisance, L. and Kritsky, D. C. ( 2004). Dactylogyridae (Platyhelminthes: Monogenea) parasitizing butterfly fishes (Teleostei: Chaetodontidae) from the coral reefs of Palau, Moorea, Wallis, New Caledonia, and Australia: species of Euryhaliotrematoides n. gen. and Aliatrema n. gen. Journal of Parasitology 90, 328–341.Google Scholar
Plaisance, L., Bouamer, S. and Morand, S. ( 2004). Description and redescription of Haliotrema species (Monogenoidea: Poloyonchoinea: Dactylogyridae) parasitizing butterfly fishes (Teleostei: Chaetodontidae) in the Indo-West Pacific Ocean. Parasitology Research 93, 72–78. DOI: 10.1007/s00436-004-1094-8.CrossRefGoogle Scholar
Posada, D. and Crandall, K. A. ( 1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle Scholar
Price, C. E. ( 1967). Two new subfamilies of monogenetic trematodes. Quarterly Journal of the Florida Academy of Sciences 29, 199–201.Google Scholar
Simková, A., Plaisance, L., Matĕjusová, I., Morand, S. and Verneau, O. ( 2003). Phylogenetic relationships of the Dactylogyridae Bychowsky, 1933 (Monogenea: Dactylogyridea): the need for the systematic revision of the Ancyrocephalinae Bychowsky, 1937. Systematic Parasitology 54, 1–11.CrossRefGoogle Scholar
Suriano, D. M. and Beverley-Burton, M. ( 1981). Urocleidus aculeatus (Van Cleave and Miller, 1932) (Monogenea: Ancyrocephalinae) from Stizostedion vitreum (Mitchill) (Pisces: Percidae) in eastern North America: anatomy and systematic position. Canadian Journal of Zoology 59, 240–245.CrossRefGoogle Scholar
Swofford, D. L. ( 2001). PAUP*: Phylogenetic Analysis using Parsimony (and Other Methods). Sinauer Associates, Sunderland, MA.
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. ( 1997). The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24, 4876–4882.CrossRefGoogle Scholar
Whittington, I. D., Deveney, M. R., Morgan, J. A., Chisholm, L. A. and Adlard, R. D. ( 2004). A preliminary phylogenetic analysis of the Capsalidae (Platyhelminthes: Monogenea: Monopisthocotylea) inferred from large subunit rDNA sequences. Parasitology 128, 511–519. DOI: 10.1017/S0031182004004901.CrossRefGoogle Scholar
Wu, B. H., Long, S., Wang, W. J. et al. ( 2000). Fauna Sinica: Platyhelminthes: Monogenea. Science Press, Beijing. (In Chinese.)
Wu, X. Y., Li, A. X., Zhu, X. Q. and Xie, M. Q. ( 2005 a). Description of Pseudorhabdosynochus seabassi sp. n. (Monogenea: Diplectanidae) from Lates calcarifer and revision of the phylogenetic position of Diplectanum grouperi (Monogenea: Diplectanidae) based on rDNA sequence data. Folia Parasitologica 52, 231–240.Google Scholar
Wu, X. Y., Chilton, N. B., Zhu, X. Q., Xie, M. Q. and Li, A. X. ( 2005 b). Molecular and morphological evidence indicates that Pseudorhabdosynochus lantauensis (Monogenea: Diplectanidae) represents two species. Parasitology 130, 669–677. DOI: 10.1017/S0031182004007152.CrossRefGoogle Scholar
Yamaguti, S. ( 1963). Systema helminthum. Vol. 4. Monogenea and Aspidocotylea. Interscience Publication, New York.
Young, P. C. ( 1968). Ten new species of Haliotrema (Monogenoidea: Dactylogyridae) from Australian fish and a revision of the genus. Journal of Zoology 154, 41–75.CrossRefGoogle Scholar
Zhang, J. Y., Qiu, Z. Z. and Ding, X. J. ( 1999). Parasites and Parasitic Diseases of Fishes. Science Press, Beijing. (In Chinese.)
Zhang, J. Y., Yang, T. B. and Liu, L. ( 2001). Monogeneans of Chinese Marine Fishes. Agriculture Press, Beijing. (In Chinese.)
Ziętara, M. S. and Lumme, J. ( 2002). Speciation by host switch and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea, Gyrodactylidae). Evolution 56, 2445–2458.CrossRefGoogle Scholar