Abstract
A survey of the endohelminth fauna of Indo-West Pacific Lutjanidae (Perciformes) revealed the presence of the species Siphoderina manilensis (Velasquez, 1961) Miller & Cribb, 2008 and S. marina (Hafeezullah & Siddiqi, 1970) Miller & Cribb, 2008 in seven Lutjanus spp. from sites off the Great Barrier Reef, the Maldives, New Caledonia and Ningaloo Reef, Western Australia. A combination of morphological and ribosomal DNA analyses of these cryptogonimids prompted the transfer of these taxa to a new genus, Euryakaina n. g., as E. manilensis n. comb. and E. marina n. comb., based on comparative analysis with other cryptogonimid taxa. Euryakaina n. g. is distinguished from all other cryptogonimid genera by the combination of a fusiform body, the few relatively small, widely spaced oral spines (sometimes absent), a highly lobed ovary, opposite to slightly oblique testes, vitelline follicles that extend from the anterior margin of the testes to slightly posterior to the intestinal bifurcation, and an excretory vesicle that bifurcates dorsal to the ovary and reunites briefly slightly posterior to the intestinal bifurcation. Morphometric analysis of these taxa alone suggests they should be reduced to synonymy, but DNA sequence analyses and ecological niche partitioning provide evidence that they form a cryptic species complex in sympatric lutjanids in the Indo-West Pacific. The secondary structure of the ITS2 rDNA for species of Euryakaina was also modelled and analysed for the presences of compensatory base changes (CBCs) or hemi-CBCs in order to explore the usefulness of these changes as a tool to help elucidate the taxonomy of this complex system. We also report what we interpret here as intraspecific variation in the ITS2 rDNA between individuals of E. manilensis from Lutjanus vitta recovered off the Great Barrier Reef and New Caledonia.
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Bickford, D., Lohman, D. J., Sodhi, N. S., Ng, P. K. L., Meier, R., Winker, K., Ingram, K. K., & Das, I. (2007). Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution, 22, 148–155.
Byun, Y., & Han, K. (2006). Pseudoviewer: web application and web service for visualizing RNA pseudoknots and secondary structures. Nucleic Acids Research, 34, W416–W422.
Coleman, A. W. (2003). ITS2 is a double-edged tool for eukaryote evolutionary comparisons. Trends in Genetics, 19, 370–375.
Coleman, A. W. (2007). Pan-eukaryote ITS2 homologies revealed by RNA secondary structures. Nucleic Acids Research, 35, 3322–3329.
Coleman, A. W. (2009). Is there a molecular key to the level of “biological species” in eukaryotes? A DNA guide. Molecular Phylogenetics and Evolution, 50, 197–203.
Cribb, T. H., & Bray, R. A. (2010). Gut wash, body soak, blender and heat fixation: approaches to the effective collection, fixation and preservation of tematodes of fishes. Systematic Parasitology, 76, 1–7.
Cribb, T. H., Pichelin, S., Dufour, V., Bray, R. A., Chauvet, C., Faliex, E., Galzin, R., Lo, C. M., Lo-Yat, A., Morand, S., Rigby, M. C., & Sasal, P. (2000). Parasites of recruiting coral reef fish larvae in New Caledonia. International Journal for Parasitology, 30, 1445–1451.
Dawson, M. N., & Jacobs, D. K. (2001). Molecular evidence for cryptic species of Aurelia aurita (Cnidaria, Scyphozoa). Biological Bulletin, 200, 92–96.
Derycke, S., Fonseca, G., Vierstraete, A., Vanfleteren, J., Vincx, M., & Moens, T. (2008). Disentangling taxonomy within the Rhabditis (Pellioditis) marina (Nematoda, Rhabditidae) species complex using molecular and morphological tools. Zoological Journal of the Linnean Society, 152, 1–15.
Durio, W. O., & Manter, H. W. (1969). Some digenetic trematodes of marine fishes of New Caledonia. III. Acanthocolpidae, Haploporidae, Gyliauchenidae, and Cryptogonimidae. Journal of Parasitology, 55, 293–300.
Geml, J., Laursen, A., O’Neill, K., Nusbaum, H. C., & Taylor, D. L. (2006). Beringian origins and cryptic speciation events in the fly agaric (Amanita muscaria). Molecular Ecology, 15, 225–239.
Grillo, V., Jackson, F., Cabaret, J., & Gilleard, J. S. (2007). Population genetic analysis of the ovine parasitic nematode Teladorsagia circumcincta and evidence for a cryptic species. International Journal for Parasitology, 37, 435–447.
Guindon, S., & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704.
Gutell, R. R., Larsen, N., & Woese, C. R. (1994). Lessons from an evolving rRNA: 16S and 23S rRNA structures from a comparative perspective. Microbiological Reviews, 58, 10–26.
Hafeezullah, M., & Siddiqi, A. H. (1970). Digenetic trematodes of marine fishes of India. Part I. Bucephalidae and Cryptogonimidae. Indian Journal of Helminthology, 22, 1–22.
Hammer, O., Harper, D. A. T., & Ryan, P. D. (2001). PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4, 1–9.
Hebert, P. D. N., Penton, E. H., Burns, J. M., Janzen, D. H., & Hallwachs, W. (2004). Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America, 101, 14812–14817.
Held, C., & Wägele, J.-W. (2005). Cryptic speciation in the giant Antarctic isopod Glyptonotus antarcticus (Isopoda: Valvifera: Chaetiliidae). Scientia Marina, 69, 175–181.
Jousson, O., Bartoli, P., & Pawlowski, J. (2000). Cryptic speciation among intestinal parasites (Trematoda: Digenea) infecting sympatric host fishes (Sparidae). Journal of Evolutionary Biology, 13, 778–785.
Jousson, O., & Bartoli, P. (2002). Species diversity among the genus Monorchis (Digenea: Monorchiidae) parasitic in marine teleosts: Molecular, morphological and morphometrical studies with a description of Monorchis blennii n. sp. Parasitology Research, 88, 230–241.
Justine, J.-L. (2007). Fish parasites: Platyhelminthes (Monogenea, Digenea, Cestoda) and nematodes, reported from off New Caledonia. In: Payri, C. E. & Richer de Forges, B. (Eds) Compendium of marine species of New Caledonia. Noumea: Institut de Recherche pour le Développement, pp. 183–198.
Kardousha, M. M. (2003). Redescription of ten species of digenetic trematodes from marine fishes of the Emirati coasts of the Arabian Gulf. Arab Gulf Journal of Scientific Research, 21, 217–226.
Keller, A., Schleicher, T., Schultz, J., Müller, T., Dandekar, T., & Wolf, M. (2009). 5.8S–28S rRNA interaction and HMM-based ITS2 annotation. Gene, 430, 50–57.
Koetschan, C., Förster, F., Keller, A., Schleicher, T., Ruderisch, B., Schwarz, R., Müller, T., Wolf, M., & Schultz, J. (2010). The ITS2 Database III - sequences and structures for phylogeny. Nucleic Acids Research, 38, D275–D279.
Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., & Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947–2948.
Leonard, J. L. (2006). Sexual selection: lessons from hermaphrodite mating systems. Integrative and Comparative Biology, 46, 349–367.
Maddison, D. R., & Maddison, W. P. (2005). MacClade 4: Analysis of phylogeny and character evolution. Version 4.08. Sunderland, Massachusetts: Sinauer Associates.
Maddison, W. P., & Maddison, D. R. (2009). Mesquite: a modular system for evolutionary analysis. Version 2.72 http://mesquiteproject.org.
Manter, H. W. (1963). Studies on digenetic trematodes of fishes of Fiji. III. Families Acanthocolpidae, Fellodistomatidae, and Cryptogonimidae. Journal of Parasitology, 49, 443–450.
Meegaskumbura, M., Bossuyt, F., Pethiyagoda, R., Manamendra-Arachchi, K., Bahir, M., Milinkovitch, M. C., & Schneider, C. J. (2002). Sri Lanka: an amphibian hot spot. Science, 298, 379.
Miller, T. L., & Cribb, T. H. (2005). A new genus and species of cryptogonimid from Lutjanus spp. (Pisces: Lutjanidae) on the Great Barrier Reef and New Caledonia. Journal of Parasitology, 91, 922–924.
Miller, T. L., & Cribb, T. H. (2007a). Phylogenetic relationships of some common Indo-Pacific snappers (Perciformes: Lutjanidae) based on mitochondrial DNA sequences, with comments on the taxonomic position of the Caesioninae. Molecular Phylogenetics and Evolution, 44, 450–460.
Miller, T. L., & Cribb, T. H. (2007b). Coevolution of Retrovarium n. gen. (Digenea: Cryptogonimidae) in Lutjanidae and Haemulidae (Perciformes) in the Indo-West Pacific. International Journal for Parasitology, 37, 1023–1045.
Miller, T. L., & Cribb, T. H. (2007c). Two new cryptogonimid genera (Digenea: Cryptogonimidae) from Lutjanus bohar (Perciformes: Lutjanidae): analyses of multiple ribosomal DNA regions reveals wide geographic distribution and presence of cryptic species. Acta Parasitologica, 52, 104–113.
Miller, T. L., & Cribb, T. H. (2007d). Two new cryptogonimid genera Beluesca n. gen. and Chelediadema n. gen. (Digenea: Cryptogonimidae) from Tropical Indo-West Pacific Haemulidae (Perciformes). Zootaxa, 1543, 45–60.
Miller, T. L., & Cribb, T. H. (2008a). Family Cryptogonimidae Ward, 1917. In: Bray, R. A., Gibson, D. I., & Jones, A. (Eds) Keys to the Trematoda. Vol. 3. Wallingford: CAB International, pp. 51–112.
Miller, T. L., & Cribb, T. H. (2008b). Eight new species of Siphoderina Manter, 1934 (Digenea, Cryptogonimidae) infecting Lutjanidae and Haemulidae (Perciformes) off Australia. Acta Parasitologica, 53, 344–364.
Miller, T. L., Downie, A. J., & Cribb, T. H. (2009a). Morphological disparity despite genetic similarity; new species of Lobosorchis Miller & Cribb, 2005 (Digenea: Cryptogonimidae) from the Great Barrier Reef and the Maldives. Zootaxa, 1992, 37–52.
Miller, T. L., Bray, R. A., Goiran, C., Justine, J.-L., & Cribb, T. H. (2009b). Adlardia novaecaledoniae n. g., n. sp. (Digenea: Cryptogonimidae) from the fork-tailed threadfin bream Nemipterus furcosus (Val.) (Perciformes: Nemipteridae) off New Caledonia. Systematic Parasitology, 73, 151–160.
Miller, T. L., & Cribb, T. H. (2009c). Gynichthys diakidnus n. g., n. sp. (Digenea: Cryptogonimidae) from the grunt Plectorhinchus gibbosus (Lacépède, 1802) (Perciformes: Haemulidae) off the Great Barrier Reef, Australia. Systematic Parasitology, 74, 103–112.
Morgan, J. A. T., & Blair, D. (1998). Trematode and monogenean rRNA ITS2 secondary structures support a four-domain model. Journal of Molecular Evolution, 47, 406–419.
Müller, T., Philippi, N., Dandekar, T., Schultz, J., & Wolf, M. (2007). Distinguishing species. RNA, 13, 1469–1472.
Nolan, M. J., & Cribb, T. H. (2005). The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Advances in Parasitology, 60, 101–163.
Pfenninger, M., & Schwenk, K. (2007). Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evolutionary Biology, 7, 121.
Posada, D. (2008). jModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution, 25, 1253–1256.
Ronquist, F., & Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
Schultz, J., Maisel, S., Gerlach, D., Müller, T., & Wolf, M. (2005). A common core of secondary structure of the internal transcribed spacer 2 (ITS2) throughout the Eukaryota. RNA, 11, 361–364.
Seibel, P. N., Müller, T., Dandekar, T., & Wolf, M. (2008). Synchronous visual analysis and editing of RNA sequence and secondary structure alignments using 4SALE. BMC Research Notes, 1, 91.
Swofford, D. L. (2003). PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Sunderland, Massachusetts: Sinauer Associates.
Velasquez, C. C. (1961). Cryptogonimidae (Digenea: Trematoda) from Philippine food fishes. Journal of Parasitology, 47, 914–918.
Velasquez, C. C. (1975). Digenetic trematodes of Philippine fishes. University of the Philippines Press, Quezon, 140 pp.
Wolf, M., Friedrich, J., Dandekar, T., & Müller, T. (2005). CBCAnalyzer: inferring phylogenies based on compensatory base changes in RNA secondary structures. In Silico Biology, 5, 0027.
Wolf, M., Selig, C., Müller, T., Philippi, N., Dandekar, T., & Schultz, J. (2007). Placozoa: at least two. Biologia, 62, 641–645.
Wörheide, G., Epp, L. S., & Macis, L. (2008). Deep genetic divergence among Indo-Pacific populations of the coral reef sponge Leucetta chagosensis (Leucettidae): founder effects, vicariance, or both? BMC Evolutionary Biology, 8, doi:10.1186/1471-2148-8-24.
Yamaguti, S. (1970). Digenetic trematodes of Hawaiian fishes. Tokyo: Keigaku Publishing Company, 436 pp.
Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research, 31, 3406–3415.
Acknowledgements
This study was funded by, and is a contribution from, the Australian node of the CReefs global research initiative (grant number: 209/29), a partnership between the Australian Biological Resource Study (ABRS), BHP Billiton, the Great Barrier Reef Foundation, the Census of Marine Life and the Australian Institute of Marine Science (AIMS). The CReefs Australia Project is generously sponsored by BHP Billiton in partnership with The Great Barrier Reef Foundation, the Australian Institute of Marine Science, the Australian Biological Resources Study and the Alfred P. Sloan Foundation. CReefs is a field program of the Census of Marine Life. We thank Dr Matthew Nolan, Mieke Burger and Dr Nicole Gunter for assistance with the fieldwork undertaken on the Great Barrier Reef and for help in collecting the teleost specimens used in this study. We gratefully thank the staff of the Lizard Island research station for their support and hospitality. We also thank Dr Robert Konecny and Julia Lorber for helping to organise the trip to the Maldives and for their assistance in the field. We are grateful to the Research Service and International Relations Office of the University of Vienna for assistance in financing the trip to Rasdhoo Atoll, Maldives. Dr Reinhard Kikinger kindly gave us access to his laboratory at the Kuramathi Biological Field Station to conduct fish necropsies and extended his generous hospitality to us during our stay. In New Caledonia, František Moravec, Eva Řehulkova, Jean-Pierre Debenay and Aude Sigura participated to the fishing expeditions and parasitological survey.
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Miller, T.L., Adlard, R.D., Bray, R.A. et al. Cryptic species of Euryakaina n. g. (Digenea: Cryptogonimidae) from sympatric lutjanids in the Indo-West Pacific. Syst Parasitol 77, 185–204 (2010). https://doi.org/10.1007/s11230-010-9266-7
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DOI: https://doi.org/10.1007/s11230-010-9266-7