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Molecular examination of kalyptorhynch diversity (Platyhelminthes: Rhabdocoela), including descriptions of five meiofaunal species from the north-eastern Pacific Ocean

Published online by Cambridge University Press:  10 January 2014

Rebecca J. Rundell*
Affiliation:
Department of Zoology, Biodiversity Research Centre, University of British Columbia, Canadian Institute for Advanced Research, Program in Integrated Microbial Diversity, Vancouver, British Columbia, V6T 1Z4Canada Department of Environmental and Forest Biology, State University of New York, College of Environmental Science and Forestry, Syracuse, New York 13210, USA
Brian S. Leander
Affiliation:
Department of Zoology, Biodiversity Research Centre, University of British Columbia, Canadian Institute for Advanced Research, Program in Integrated Microbial Diversity, Vancouver, British Columbia, V6T 1Z4Canada
*
Correspondence should be addressed to: R.J. Rundell, Department of Environmental and Forest Biology, State University of New York, College of Environmental Science and Forestry, Syracuse, New York 13210, USA email: [email protected]

Abstract

The spaces between sand grains are home to a myriad of microscopic marine eukaryotes, including kalyptorhynch rhabdocoels equipped with an eversible proboscis that enables them to capture microscopic prey living in these environments. The structure of the kalyptorhynch proboscis separates the two major subclades within the group: the Schizorhynchia (bifurcated proboscis) and the Eukalyptorhynchia (unbranched proboscis). A survey of meiofaunal metazoans in the Pacific north-west led to the discovery of three new schizorhynch species (Undicola tofinoensis gen. nov., sp. nov., Schizorhinos vancouverensis gen. nov., sp. nov. and Linguabana tulai gen. nov., sp. nov.) and two new eukalyptorhynch species (Thinodactylaina tlaoquiahtensis gen. nov., sp. nov. and Rostracilla nuuchahnulthensis gen. nov., sp. nov.). This survey also recovered the putative cosmopolitan eukalyptorhynch (Polycystididae) Gyratrix hermaphroditus Ehrenberg, 1831. We performed molecular phylogenetic analyses on 18S rDNA sequences from all five novel isolates and from all available kalyptorhynch species in GenBank. The molecular data supported the monophyly of the Eukalyptorhynchia and Schizorhynchia and helped demonstrate the boundaries between different species within the Kalyptorhynchia.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

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References

REFERENCES

Artois, T.J. and Schockaert, E.R. (2000) Interstitial fauna of the Galapagos: Typhlopolycystidinae (Platyhelminthes Polycystididae). Tropical Zoology 13, 141158.Google Scholar
Artois, T.J. and Schockaert, E.R. (2003) Primary homology assessment in the male atrial system of the Polycystididae (Platyhelminthes: Eukalyptorhynchia). Zoologischer Anzeiger 242, 179190.Google Scholar
Artois, T.J. and Schockaert, E.R. (2005a) Primary homology assessment of structures in the female atrial system among species of the Polycystididae (Rhabditophora, Eukalyptorhynchia). Invertebrate Biology 124, 109118.CrossRefGoogle Scholar
Artois, T.J. and Schockaert, E.R. (2005b) World database of Proseriata and Kalyptorhynchia. Available at: http://www.marinespecies.org/rhabditophora (accessed 3 October 2013).Google Scholar
Artois, T.J. and Tessens, B.S. (2008) Polycystididae (Rhabditophora: Rhabdocoela: Kalyptorhynchia) from the Indian Ocean, with the description of twelve new species. Zootaxa 1849, 127.Google Scholar
Ax, P. (1959) Zur Systematik, Ökologie und Tiergeographie der Turbellarienfauna in den ponto-kaspischen Brackwassergebieten. Zoologische Jahrbucher-Abteilung für Systematik, Oekologie und Geographie der Tiere 87, 43184.Google Scholar
Ax, P. and Heller, R. (1970) Neue Neorhabdocoela (Turbellaria) vom Sandstrand der Nordsee-Insel Sylt. Mikrofauna Meeresbodens 2, 146.Google Scholar
Boaden, P.J.S. (1963) The interstitial fauna of some North Wales beaches. Journal of the Marine Biological Association of the United Kingdom 43, 7996.CrossRefGoogle Scholar
Brusca, R.C. and Brusca, G.J. (2003) Invertebrates. Sunderland, MA: Sinauer Associates.Google Scholar
Cannon, L.R.G. (1986) Turbellaria of the World. A guide to families and genera. Brisbane: Queensland Museum.Google Scholar
Curini-Galletti, M. and Puccinelli, I. (1990) The Gyratrix hermaphroditus species complex (Platyhelminthes: Kalyptorhynchia) in the Darwin area (Northern Territory, Australia). Transactions of the American Microscopical Society 109, 368379.CrossRefGoogle Scholar
Curini-Galletti, M. and Puccinelli, I. (1994) The Gyratrix hermaphroditus species-complex (Platyhelminthes Kalyptorhynchia) in marine tropical areas: first data from the Caribbean. Belgian Journal of Zoology 124, 157166.Google Scholar
Curini-Galletti, M. and Puccinelli, I. (1998) The Gyratrix hermaphroditus species complex (Kalyptorhynchia: Polycystididae) in marine habitats of eastern Australia. Hydrobiologia 383, 287298.Google Scholar
Dean, H.K. (1977) Two new Kalyptorhynchia (Turbellaria) from the coast of northern New England, USA. Zoologica Scripta 6, 265274.Google Scholar
Dean, H.K. (1980) Parathylacorhynchus reidi gen. et sp. n., a Schizorhynchid (Turbellaria, Kalyptorhynchia) from the coast of Maine, USA. Zoologica Scripta 9, 59.Google Scholar
DeVocht, A. (1991) Anatomy and ultrastructure of the proboscis in Mesorhynchus terminostylis (Platyhelminthes, Rhabdocoela). Hydrobiologia 227, 291298.Google Scholar
Doe, D.A. (1974) Two new Proschizorhynchus species from the coast of Massachusetts, USA (Turbellaria, Kalyptorhynchia). Zoologica Scripta 3, 101110.Google Scholar
Ehrenberg, C.G. (1831) Animalia Evertebrata exclusis insectis recensuit. Series prima cum tabularum decade prima. In Hemprich, F.G. and Ehrenberg, C.G. (eds) Symbolae Physicae 2. Phytozoa Turbellaria, pp. 115.Google Scholar
Giere, O. (2009) Meiobenthology, 2nd edition. Berlin: Springer..Google Scholar
Giribet, G., Carranza, S., Baguna, J., Riutort, M. and Ribera, C. (1996) First molecular evidence for the existence of a Tardigrada + Arthropoda clade. Molecular Biology and Evolution 13, 7684.Google Scholar
Graff, L. von (1905) Marine Turbellarien Orotavas und der Küsten Europas. Zeitschrift für Wissenschaftliche Zoologie 83, 68154.Google Scholar
Guindon, S. and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696704.CrossRefGoogle ScholarPubMed
Heitkamp, U. (1978) Speziationsprozesse bei Gyratrix hermaphroditus Ehrenberg, 1831 (Turbellaria, Kalyptorhynchia). Zoomorphologie 90, 227251.Google Scholar
Hochberg, R. (2004) Smithsoniarhynches, a new genus of interstitial Gnathorhynchidae (Platyhelminthes: Kalyptorhynchia) from Mosquito Lagoon and Indian River Lagoon, Florida. Journal of the Marine Biological Association of the United Kingdom 84, 11431149.Google Scholar
Joffe, B.I. and Kornakova, E.E. (2001) Flatworm phylogeneticist: between molecular hammer and morphological anvil. In Littlewood, D.T.J. and Bray, R.A. (eds) Interrelationships of the Platyhelminthes. London and New York: Taylor & Francis, pp. 279291.Google Scholar
Joffe, B.I., Selivanova, R.V. and Kornakova, E.E. (1997) Notentera ivanovi n. gen., n. sp. (Turbellaria, Platyhelminthes), a new parasitic turbellarian. Parasitologya (St Petersburg) 31, 126131.Google Scholar
Jörger, K.M., Norenburg, J.L., Wilson, N.G. and Schrodl, M. (2012) Barcoding against a paradox? Combined molecular species delineations reveal multiple cryptic lineages in elusive meiofaunal sea slugs. BMC Evolutionary Biology 12, 245.CrossRefGoogle ScholarPubMed
Karling, T.G. (1931) Untersuchungen über Kalyptorhynchia (Turbellaria Rhabdocoela) aus dem brackwasser des finnischen meerbusens. Acta Zoologica Fennica 11, 167.Google Scholar
Karling, T.G. (1956) Morphologisch-histologische Untersuchungen an den männlichen Atrialorganen der Kalyptorhynchia (Turbellaria). Arkiv für Zoologi 9, 187279.Google Scholar
Karling, T.G. (1961) Zur Morphologie, Entstehungsweise und Funktion des Spaltrüssels der Turbellaria Schizorhynchia. Arkiv fur Zoologi 13, 253286.Google Scholar
Karling, T.G. (1981) Typhlorhynchus nanus Laidlaw, a kalyptorhynch turbellarian without proboscis (Platyhelminthes). Annales Zoologici Fennici 18, 169177.Google Scholar
Karling, T.G. (1983a) Structural and systematic studies on Turbellaria Schizorhynchia (Platyhelminthes). Zoologica Scripta 12, 7789.Google Scholar
Karling, T.G. (1983b) Phylogeny of Paragnathorhynchus Meixner and Aculeorhynchus Schilke (Turbellaria, Kalyptorhynchia). Zoologica Scripta 12, 7376.Google Scholar
Karling, T.G. (1989) New taxa of Kalyptorhynchia (Platyhelminthes) from the N. American Pacific coast. Zoologica Scripta 18, 1932.Google Scholar
Karling, T.G. (1995) Two new species of Kalyptorhynchia (Platyhelminthes) from the N. American Atlantic coast. Belgian Journal of Zoology 125, 395402.Google Scholar
Karling, T.G. and Schockaert, E.R. (1977) Anatomy and systematics of some Polycystididae (Turbellaria, Kalyptorhynchia) from the Pacific and S. Atlantic. Zoologica Scripta 6, 519.Google Scholar
Kölliker, A. (1845) Lineola, Choraima, Polycystis, neue wurmgattungen und neue arten von Nemertes. Verhandlungen der Schweizrischen Naturforschenden Gesellschaft II (29 Juli), 86105.Google Scholar
L'Hardy, J.P. (1963) Turbellaries Schizorhynchidae des sables de Roscoff. I. Les Genres Carcharodorhynchus, Schizochilus et Schizorhynchoides. Cahiers de Biologie Marine 4, 459472.Google Scholar
Littlewood, D.T.J. and Olson, P.D. (2001) Small subunit rDNA and the Platyhelminthes: signal noise, conflict and compromise. In Littlewood, D.T.J. and Bray, R.A. (eds) Interrelationships of the Platyhelminthes. London and New York: Taylor & Francis, pp. 262278.Google Scholar
Littlewood, D.T.J., Rohde, K. and Clough, K.A. (1999a) The interrelationships of all major groups of Platyhelminthes: phylogenetic evidence from morphology and molecules. Biological Journal of the Linnean Society 66, 75114.Google Scholar
Littlewood, D.T.J., Rohde, K., Bray, R.A. and Herniou, E.A. (1999b) Phylogeny of the Platyhelminthes and the evolution of parasitism. Biological Journal of the Linnean Society 68, 257287.Google Scholar
MacArthur, R.H. (1972) Geographical ecology. Patterns in the distribution of species. Princeton, NJ: Princeton University Press.Google Scholar
Maddison, D.R. and Maddison, W.P. (2001) MacClade 4: analysis of phylogeny and character evolution. Sunderland, MA: Sinauer Associates, Inc.Google Scholar
Marcus, E. (1949) Turbellaria Brasileiros (7). Boletins da Faculdade de filosofia, ciências e letras, Universidade de São Paulo (Zoologia) 14, 7155.Google Scholar
Martens, P.M. and Schockaert, E.R. (1986) The importance of turbellarians in the marine meiobenthos: a review. Hydrobiologia 132, 295303.Google Scholar
Mayr, E. (1963) Animal species and evolution. Cambridge, MA: Belknap Press.Google Scholar
Meixner, J. (1925) Beitrag zur Morphologie und zum System der Turbellaria-Rhabdocoela. I. Die Kalyptorhynchia. Zeitschrift für Morphologie und Okologie der Tiere 3, 255343.Google Scholar
Meixner, J. (1928) Aberrante Kalyptorhynchia (Turbellaria Rhabdocoela) aus dem Sande der Kieler Bucht. I. Zoologischer Anzeiger 77, 229253.Google Scholar
Metschnikoff, E. (1865) Zur Naturgeschichte der Rhabdocolen. Archiv für Naturgeschichte 31, 174181.Google Scholar
Noldt, U. and Reise, K. (1987) Morphology and ecology of the kalyptorhynch Typhlopolycystis rubra (Plathelminthes), an inmate of lugworm burrows in the Wadden Sea. Helgoländer Meeresuntersuchungen 41, 185199.Google Scholar
Posada, D. (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 12531256.Google Scholar
Puccinelli, I. and Curini-Galletti, M.C. (1987) Chromosomal evolution and speciation in marine populations of Gyratrix hermaphroditus sensulato (Platyhelminthes: Kalyptorhynchia) and in other species of the Gyratricinae. Transactions of the American Microscopical Society 106, 311320.Google Scholar
Rieger, R.M. (1974) A new group of Turbellaria–Typhloplanoida with a proboscis and its relationship to Kalyptorhynchia. In Riser, N.W. and Morse, M.P. (eds) Biology of the Turbellaria. Libbie H. Hyman Memorial Volume. New York: McGraw-Hill, pp. 2358.Google Scholar
Rieger, R.M. (1998) 100 years of research on ‘Turbellaria.’Hydrobiologia 383, 127.Google Scholar
Rieger, R.M., Tyler, S., Smith, J.P.S. III and Rieger, G.E. (1991) Platyhelminthes: Turbellaria. In Harrison, F.W. and Bogitsh, B.J. (eds). Microscopic anatomy of invertebrates, Volume 3 Platyhelminthes and Nemertinea. New York: Wiley-Liss, pp. 7140.Google Scholar
Schilke, K. (1969) Zwei neuartige Konstruktionstypen des Rüsselapparates der Kalyptorhynchia (Turbellaria). Zeitschrift für Morphologie der Tiere 65, 287314.Google Scholar
Schilke, K. (1970a) Zur Morphologie und Phylogenie der Schizorhynchia (Turbellaria, Kalyptorhynchia). Zeitschrift für Morphologie der Tiere 67, 118171.Google Scholar
Schilke, K. (1970b) Kalyptorhynchia (Turbellaria) aus dem Eulitoral der deutschen Nordseeküste. Helgoländer. Wissenschaftlische Meeresuntersuchungen 21, 143265.Google Scholar
Schockaert, E.R. (1974) On the male copulatory organ of some Polycycstididae and its importance in the systematics of the family. In Riser, N.W. and Morse, M.P. (eds) Biology of the Turbellaria. New York: McGraw-Hill, pp. 165172.Google Scholar
Schockaert, E. and Karling, T.G. (1970) Three new anatomically remarkable Turbellaria Eukalyptorhynchia from the North American Pacific coast. Arkiv für Zoologi 23, 237253.Google Scholar
Schockaert, E. and Karling, T.G. (1975) Anatomy and taxonomy of some species of Polycystididae (Turbellaria, Kalyptorhynchia) from N. Atlantic and Mediterranean coastal areas. Zoologica Scripta 4, 133143.Google Scholar
Therriault, T.W. and Kolasa, J. (1999) New species and records of microturbellarians from coastal rock pools of Jamaica, West Indies. Archiv für Hydrobiologie 144, 371381.Google Scholar
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24, 48764882.Google Scholar
Timoshkin, O.A., Zaytseva, E.P. and Gutsol, M.V. (2009) New species of microscopic psammophilous turbellarians of the genus Opisthosystis (Plathelminthes, Kalyptorhynchia) from Lake Baikal. Zoologichesky Zhurnal 88, 398413.Google Scholar
Uhlig, G. (1964) Eine einfache Methode zur Extraktion der vagilen mesopsammalen Mikrofauna. Helgoländer. Wissenschaftlische Meeresuntersuchungen 11, 178185.Google Scholar
Uyeno, T.A. and Kier, W. (2010) Morphology of the muscle articulation joint between the hooks of a flatworm (Kalyptorhynchia, Chelipana sp.). Biological Bulletin. Marine Biological Laboratory, Woods Hale 218, 169180.Google Scholar
Van Steenkiste, N., Tessens, B., Willems, W., Backeljau, T., Jondelius, U. and Artois, T. (2013) A comprehensive molecular phylogeny of Dalytyphloplanida (Platyhelminthes: Rhabdocoela) reveals multiple escapes from the marine environment and origins of symbiotic relationships. PLoS ONE 8, e59917.Google Scholar
Willems, W.R., Wallberg, A., Jondelius, U., Littlewood, D.T.J., Backeljau, T., Schockaert, E.R. and Artois, T.J. (2006a) Filling a gap in the phylogeny of flatworms: relationships within the Rhabdocoela (Platyhelminthes), inferred from 18S ribosomal DNA sequences. Zoologica Scripta 35, 117.Google Scholar
Willems, W.R., Schockaert, E.R. and Artois, T.J. (2006b) Report on the Polycystididae (Rhabdocoela, Kalyptorhynchia) from Australia, with the description of twelve new species and six new genera. Hydrobiologia 563, 329355.Google Scholar
Willems, W.R., Sandberg, M.I. and Jondelius, U. (2007) First report on Rhabdocoela (Rhabditophora) from deep parts of Skagerrak, with the description of four new species. Zootaxa 1616, 121.Google Scholar
Zwickl, D.J. (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD dissertation. The University of Texas at Austin. Available at: www.bio.utexas.edu/faculty/antisense/garli/Garli.html (accessed 3 October 2013).Google Scholar