Skip to main content
Log in

Cryptic species of Euryakaina n. g. (Digenea: Cryptogonimidae) from sympatric lutjanids in the Indo-West Pacific

  • Published:
Systematic Parasitology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • 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.

    Article  Google Scholar 

  • Byun, Y., & Han, K. (2006). Pseudoviewer: web application and web service for visualizing RNA pseudoknots and secondary structures. Nucleic Acids Research, 34, W416–W422.

    Article  CAS  PubMed  Google Scholar 

  • Coleman, A. W. (2003). ITS2 is a double-edged tool for eukaryote evolutionary comparisons. Trends in Genetics, 19, 370–375.

    Article  CAS  PubMed  Google Scholar 

  • Coleman, A. W. (2007). Pan-eukaryote ITS2 homologies revealed by RNA secondary structures. Nucleic Acids Research, 35, 3322–3329.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Dawson, M. N., & Jacobs, D. K. (2001). Molecular evidence for cryptic species of Aurelia aurita (Cnidaria, Scyphozoa). Biological Bulletin, 200, 92–96.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Guindon, S., & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704.

    Article  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Held, C., & Wägele, J.-W. (2005). Cryptic speciation in the giant Antarctic isopod Glyptonotus antarcticus (Isopoda: Valvifera: Chaetiliidae). Scientia Marina, 69, 175–181.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Leonard, J. L. (2006). Sexual selection: lessons from hermaphrodite mating systems. Integrative and Comparative Biology, 46, 349–367.

    Article  Google Scholar 

  • Maddison, D. R., & Maddison, W. P. (2005). MacClade 4: Analysis of phylogeny and character evolution. Version 4.08. Sunderland, Massachusetts: Sinauer Associates.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Müller, T., Philippi, N., Dandekar, T., Schultz, J., & Wolf, M. (2007). Distinguishing species. RNA, 13, 1469–1472.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Pfenninger, M., & Schwenk, K. (2007). Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evolutionary Biology, 7, 121.

    Article  PubMed  Google Scholar 

  • Posada, D. (2008). jModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution, 25, 1253–1256.

    Article  CAS  PubMed  Google Scholar 

  • Ronquist, F., & Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • Wolf, M., Selig, C., Müller, T., Philippi, N., Dandekar, T., & Schultz, J. (2007). Placozoa: at least two. Biologia, 62, 641–645.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Terrence L. Miller.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11230-010-9266-7

Keywords

Navigation