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Host specificity versus plasticity: testing the morphology-based taxonomy of the endoparasitic copepod family Splanchnotrophidae with COI barcoding

Published online by Cambridge University Press:  13 September 2016

Roland F. Anton ,
Dirk Schories ,
Nerida G. Wilson ,
Maya Wolf ,
Marcos Abad  and
Michael Schrödl
Roland F. Anton*
Affiliation:
Mollusca Department, SNSB- Bavarian State Collection of Zoology Munich, Münchhausenstraße 21, D-81247 München, Germany
Dirk Schories
Affiliation:
Instituto de Ciencias Marinas y Limnológicas, Universidad Austral de Chile, Valdivia, Chile
Nerida G. Wilson
Affiliation:
Molecular Systematics Unit, Western Australian Museum, Welshpool, WA 6106, Australia School of Animal Biology, University of Western Australia, Crawley, WA 6009, Australia
Maya Wolf
Affiliation:
Department of Biology, University of Oregon/Oregon Institute of Marine Biology, Charleston, OR 97420, USA
Marcos Abad
Affiliation:
Estación de Bioloxía Mariña da Graña, Universidade de Santiago de Compostela, Rúa da Ribeira, 1 (A Graña), 15590, Ferrol, Spain
Michael Schrödl
Affiliation:
Mollusca Department, SNSB- Bavarian State Collection of Zoology Munich, Münchhausenstraße 21, D-81247 München, Germany Department Biology II, BioZentrum, Ludwig-Maximilians-Universität München, Großhaderner Str. 2, 82152 Planegg-Martinsried, Germany GeoBioCenter LMU, München, Germany
*
Correspondence should be addressed to: R.F. Anton Mollusca Department, SNSB–Bavarian State Collection of Zoology Munich, Münchhausenstraße 21, D-81247 München, Germany email: [email protected]
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Abstract

The Splanchnotrophidae is a family of highly modified endoparasitic copepods known to infest nudibranch or sacoglossan sea slug hosts. Most splanchnotrophid species appear to be specific to a single host, but some were reported from up to nine different host species. However, splanchnotrophid taxonomy thus far is based on external morphology, and taxonomic descriptions are, mostly, old and lack detail. They are usually based on few specimens, with intraspecific variability rarely reported. The present study used molecular data for the first time to test (1) the current taxonomic hypotheses, (2) the apparently strict host specificity of the genus Ismaila and (3) the low host specificity of the genus Splanchnotrophus with regard to the potential presence of cryptic species. Phylogenetic analyses herein used sequences of the barcoding region of the cytochrome oxidase I (COI) gene from 40 specimens representing 13 species of five genera. Species delimitation approaches include distance and barcoding gap analyses, haplotype networks and diagnostic nucleotides. Molecular results are largely compatible with the commonly accepted, morphology-based taxonomy of the Splanchnotrophidae. Strict host specificity could be confirmed for two Ismaila species. COI analyses also supported the idea that Splanchnotrophus angulatus is host-promiscuous. In Ismaila, morphology seems more suitable than barcoding to display speciation events via host switches in a recent Chilean radiation. In Splanchnotrophus, some genetic structure suggests ongoing diversification, which should be investigated further given the inadequate morphology-based taxonomy. The present study thus supports the presence of two different life history strategies in splanchnotrophids, which should be explored integratively.

Keywords

species delimitationmolecular phylogenyDNA taxonomyspeciationCopepodasea slugsparasite
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Issue 2 , March 2018 , pp. 231 - 243
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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References

REFERENCES

Abad, M., Díaz-Agras, G. and Urgorri, V. (2011) Anatomical description and biology of the Splanchnotrophid Splanchnotrophus gracilis Hancock & Norman, 1863 found parasitizing the Doridacean Nudibranch Trapania tartanella Ihering, 1886 at the Ría de Ferrol (Galicia, NW Iberian Peninsula). Thalassas 27, 49–60.Google Scholar
Anton, R.F., Schories, D., Joerger, K.M., Kaligis, F. and Schrödl, M. (2015) Description of four new endoparasitic species of the family Splanchnotrophidae (Copepoda, Poecilostomatoida) from nudibranch and sacoglossan gastropod hosts. Marine Biodiversity 46, 183–195.CrossRefGoogle Scholar
Anton, R.F. and Schrödl, M. (2013a) The gastropod – crustacean connection: towards the phylogeny and evolution of the parasitic copepod family Splanchnotrophidae. Zoological Journal of the Linnean Society 167, 501–530.CrossRefGoogle Scholar
Anton, R.F. and Schrödl, M. (2013b) The “inner values” of an endoparasitic copepod – computer-based 3D-reconstruction of Ismaila aliena . Spixiana 36, 183–199.Google Scholar
Anton, R.F., Stevenson, A. and Schwabe, E. (2013) Description of a new abyssal copepod associated with the echinoid Sperosoma grimaldii Koehler, 1897. Spixiana 36, 201–210.Google Scholar
Bassett-Smith, P.W. (1903) On new parasitic Copepoda from Zanzibar and East Africa, collected by Mr. Cyril Crossland, B. A., B. Sc. Proceedings of the Zoological Society London 73, 104–107.CrossRefGoogle Scholar
Blanco-Berical, L., Cornils, A., Copley, N. and Bucklin, A. (2014) DNA barcoding of marine copepods: assessment of analytical approaches to species identification. PLOS Currents Tree of Life 6. doi: 10.1371/currents.tol.cdf1378b74881f74887e74883b74801d74856b43791626d43791622.CrossRefGoogle Scholar
Canu, E. (1891) Sur quelques Copépodes parasites, observés dans le Boulonnais. Comptes Rendus Hebdomadaire des Séances de ĺAcademie des Sciences, Paris 113, 435–437.Google Scholar
Carmona, L., Lei, B.R., Pola, M., Gosliner, T.M., Valdés, Á and Cervera, J.L. (2014) Untangling the Spurilla neapolitana (Delle Chiaje, 1841) species complex: a review of the genus Spurilla Bergh, 1864 (Mollusca: Nudibranchia: Aeolidiidae). Zoological Journal of the Linnean Society 170, 132–154.CrossRefGoogle Scholar
Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.CrossRefGoogle ScholarPubMed
Clement, M., Posada, D. and Crandall, K.A. (2009) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.CrossRefGoogle Scholar
Delamare Deboutteville, C. (1950) Contribution a la conaissance des Copepodes genre Splanchnotrophus Hancock & Norman parasites de mollusques. Vie et Milieu 1, 74–80.Google Scholar
Folmer, O., Black, W., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google ScholarPubMed
Gotto, R.V. (1979) The association of copepods with marine invertebrates. Advances in Marine Biology 16, 1–109.CrossRefGoogle Scholar
Gotto, R.V. (2004) Commensal and parasitic copepods associated with marine invertebrates. Shrewsbury: Field Studies Council.Google Scholar
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Haumayr, U. and Schrödl, M. (2003) Revision of the endoparasitic copepod genus Ismaila Bergh, 1867, with description of eight new species. Spixiana 26, 1–33.Google Scholar
Hecht, E. (1895) Contributions a ĺétude des Nudibranches. Mémoires de la Société Zoologique de France 8, 539–711.Google Scholar
Ho, J.S. (2001) Why do symbiotic copepods matter? Hydrobiologia 453/454, 1–7.CrossRefGoogle Scholar
Huson, D.H. and Bryant, D. (2006) Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23, 254–267.CrossRefGoogle ScholarPubMed
Huys, R. (2001) Splanchnotrophid systematics, a case of polyphyly and taxonomic myopia. Journal of Crustacean Biology 21, 106–156.CrossRefGoogle Scholar
Jensen, K.R. (1990) Splanchnotrophus elysiae n. sp. (Copepoda; Splanchnotrophidae) found parasitizing in the sacoglossan opisthobranch Elysia australis (Quoy and Gaymard, 1832). In Proceedings of the Third International Marine Biological Workshop: The Marine Flora and Fauna of Albany, Western Australia – Western Australia Museum, Perth, Volume 1, pp. 291–296.Google Scholar
Jörger, K., Neusser, T.P., Brenzinger, B. and Schrödl, M. (2014) Exploring the diversity of mesopsammic gastropods: How to collect, identify, and delimitate small and elusive sea slugs? American Malacological Bulletin 32, 290–307.CrossRefGoogle Scholar
Jörger, K. and Schrödl, M. (2014) How to use CAOS software for taxonomy? A quick guide to extract diagnostic nucleotides or amino acids for species descriptions. Spixiana 37, 21–26.Google Scholar
Jörger, K.M., Stöger, I., Kano, Y., Fukuda, H., Knebelsberger, T. and Schrödl, M. (2010) On the origin of Acochlidia and other enigmatic euthyneuran gastropods, with implications for the systematics of Heterobranchia. BMC Evolutionary Biology 10, 323. doi: 310.1186/1471-2148-1110-1323.CrossRefGoogle ScholarPubMed
Layton, K.K., Martel, A.L. and Hebert, P.D. (2014) Patterns of DNA barcode variation in Canadian marine molluscs. PloS ONE 9, e95003.CrossRefGoogle ScholarPubMed
Meier, R., Shiyang, K., Vaidya, G. and Ng, P.L.K. (2006) DNA barcoding and taxonomy in Diptera: a tale of high intraspecific variability and low identification success. Systematic Biology 55, 715–728.Google ScholarPubMed
Miralles, A., Vasconcelos, R., Perera, A., Harris, D.J. and Carranza, S. (2011) An integrative taxonomic revision of the Cape Verdean skinks (Squamata, Scincidae). Zoologica Scripta 40, 16–44.CrossRefGoogle Scholar
Monod, T. and Dollfus, R.-P. (1932) Les Copépodes parasites de mollusques. Annales de Parasitologie humaine et comparée 10, 129–204.CrossRefGoogle Scholar
O'Donoghue, C.H. (1924) Report on Opisthobranchiata from the Abrolhos Islands, Western Australia, with description of a new parasitic copepod. Journal of the Linnean Society (Zoology) XXXV, 521–579.Google Scholar
Padula, V., Araújo, A.K., Mathews-Cascon, H. and Schrödl, M. (2014) Is the Mediterranean nudibranch Cratena peregrina (Gmelin, 1791) present on the Brazilian coast? Integrative species delimitation and description of Cratena minor n. sp. Journal of Molluscan Studies 80, 575–584.CrossRefGoogle Scholar
Puillandre, N., Lambert, A., Brouillet, S. and Achaz, G. (2011) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology. doi: 10.1111/j.1365-294X.2011.05239.x.Google ScholarPubMed
Puillandre, N., Modica, M.V., Zhang, Y., Sirovich, L., Boisselier, M.-C., Craud, C., Holford, M. and Samadi, S. (2012) Large-scale species delimitation method for hyperdiverse groups. Molecular Ecology 21, 2671–2691.CrossRefGoogle ScholarPubMed
Ronquist, F. and Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Salmen, A., Kaligis, F., Mamangkey, G.F. and Schrödl, M. (2008) Arthurius bunakenensis, a new tropical Indo-Pacific species of endoparasitic copepods from a sacoglossan opisthobranch host. Spixiana 31, 199–205.Google Scholar
Sarkar, I.N., Planet, P.J. and DeSalle, R. (2008) CAOS software for use in character-based DNA barcoding. Molecular Ecology Resources 8, 1256–1259.CrossRefGoogle ScholarPubMed
Schrödl, M. (1997) Aspects of Chilean nudibranch biology: effects of splanchnotrophid copepod parasitism on Flabellina sp.1 (Mollusca, Nudibranchia). Opisthobranch Newsletter 23, 45–48.Google Scholar
Schrödl, M. (2003) Sea slugs of southern South America. Hackenheim: ConchBooks.Google Scholar
Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30.CrossRefGoogle ScholarPubMed
Talavera, G. and Castresana, J. (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequences alignments. Systematic Biology 56, 564–577.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Uyeno, D. and Nagasawa, K. (2012) Four new species of splanchnotrophid copepods (Poecilostomatoida) parasitic on doridacean nudibranchs (Gastropoda, Opisthobranchia) from Japan, with proposition of one new genus. ZooKeys 247, 1–29.CrossRefGoogle Scholar
Weis, A. and Melzer, R.R. (2012) How did seaspiders recolonize the Chilean fjords after glaciation? DNA barcoding of Pycnogonida, with remarks on phylogeography of Achelia assimilis (Haswell, 1885). Systematics and Biodiversity 10, 361–374.CrossRefGoogle Scholar
Xia, X. and Lemey, P. (2009) Assessing substitution saturation with DAMBE. In Lemey, P., Salemi, M. and Vandamme, A.-M. (eds) The phylogenetic handbook: a practical approach to DNA and protein phylogeny, 2nd edition. Cambridge: Cambridge University Press, pp. 615–630.Google Scholar
Xia, X., Xie, Z., Salemi, M., Chen, L. and Wang, Y. (2003) An index of substitution saturation and its application. Molecular Phylogenetics and Evolution 26, 1–7.Google ScholarPubMed
Yoshikoshi, K. (1975) On the structure and function of the alimentary canal of Tigriopus japonicus (Copepoda; Hapacticoida) – I. Histological structure. Bulletin of the Japanese Society of Scientific Fisheries 41, 929–935.CrossRefGoogle Scholar
Zhang, J., Kapli, P., Pavlidis, P. and Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 2869–2876.CrossRefGoogle ScholarPubMed