Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2021-03-23
Page range: 451–500
Abstract views: 163
PDF downloaded: 68

Taxonomy and phylogeny of Koinocystididae (Platyhelminthes, Kalyptorhynchia), with the description of three new genera and twelve new species

Universidad de Oriente, Biology & Geography Department, Ave. Patricio Lumumba s/n, CP 90500, Santiago de Cuba, Cuba. Hasselt University, Centre for Environmental Sciences, Research Group Zoology: Biodiversity and Toxicology, Universitaire Campus Gebouw D, B-3590 Diepenbeek, Belgium
Hasselt University, Centre for Environmental Sciences, Research Group Zoology: Biodiversity and Toxicology, Universitaire Campus Gebouw D, B-3590 Diepenbeek, Belgium
Centro Oriental de Ecosistemas y Biodoversidad (BIOECO). Museo Tomás Romay, Calle Enramadas 601, CP 90100, Santiago de Cuba, Cuba.
Hasselt University, Centre for Environmental Sciences, Research Group Zoology: Biodiversity and Toxicology, Universitaire Campus Gebouw D, B-3590 Diepenbeek, Belgium
Hasselt University, Centre for Environmental Sciences, Research Group Zoology: Biodiversity and Toxicology, Universitaire Campus Gebouw D, B-3590 Diepenbeek, Belgium Royal Zoological Society of Antwerp, Centre for Research & Conservation, Koningin Astridplein 20-26, B-2018 Antwerp, Belgium.
University of British Columbia, Departments of Botany and Zoology, 6270 University Blvd., Vancouver, BC, V6T 1Z4 Canada.
University of British Columbia, Departments of Botany and Zoology, 6270 University Blvd., Vancouver, BC, V6T 1Z4 Canada.
Hasselt University, Centre for Environmental Sciences, Research Group Zoology: Biodiversity and Toxicology, Universitaire Campus Gebouw D, B-3590 Diepenbeek, Belgium
Hasselt University, Centre for Environmental Sciences, Research Group Zoology: Biodiversity and Toxicology, Universitaire Campus Gebouw D, B-3590 Diepenbeek, Belgium
Hasselt University, Centre for Environmental Sciences, Research Group Zoology: Biodiversity and Toxicology, Universitaire Campus Gebouw D, B-3590 Diepenbeek, Belgium
Hasselt University, Centre for Environmental Sciences, Research Group Zoology: Biodiversity and Toxicology, Universitaire Campus Gebouw D, B-3590 Diepenbeek, Belgium
Platyhelminthes Kalyptorhynchia microturbellarian Rhabdocoela systematics phylogeny

Abstract

The taxon Koinocystididae is the third most species-rich family within Eukalyptorhynchia. However, its diversity and phylogeny have been largely neglected in former studies. We introduce three new genera and twelve new species of Koinocystididae including Simplexcystis asymmetrica gen. n. sp. n., Galapagetula cubensis sp. n., eight species of Reinhardorhynchus gen. n. and two species of Itaipusa. This raises the total number of species within Koinocystididae from 51 to 63. We also report on new distribution records for six known species: I. divae (Cuba, Panama and New Caledonia), I. karlingi (Sardinia and Lanzarote), Reinhardorhynchus riegeri comb. n. (Cuba), R. ruffinjonesi comb. n. (Cuba and Panama), Utelga heinckei (Cuba and Lanzarote), and U. pseudoheinckei (Sardinia). Simplexcystis asymmetrica gen. n. sp. n. is characterised by a male duct running eccentrically through the copulatory bulb, lack of any hard structures in the male system, lack of a bursa, and the fact that the epithelia of the female, the male, and part of the common atrium are covered by a brush border. Galapagetula cubensis sp. n. has a caudal gonopore, a divisa-type copulatory bulb with an unarmed penis papilla, and a female duct without a sphincter. The new species of Itaipusa and Reinhardorhynchus gen. n. differ from their congeners in the detailed structure of the copulatory bulb and especially the hard structures associated with it. In a molecular phylogenetic analysis based on all available 18S and 28S rDNA sequences of koinocystidids, we found support for the monophyly of the family and the genus Utelga Marcus, 1949. The genus Itaipusa is not monophyletic in that I. sinensis forms a clade with Rhinolasius dillonicus, while other species of Itaipusa that have a copulatory bulb armed with hooks form a clade together with Sekerana stolzi. As the type species of Itaipusa (I. divae) is in neither of these clades, we erected a new genus for I. sinensis (Koinogladius gen. n.) and one for species of Itaipusa having a hook-bearing copulatory bulb (Reinhardorhynchus gen. n.), respectively. Whether the remaining species of Itaipusa form a monophylum remains uncertain.

 

References

  1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.

    https://doi.org/10.1016/S0022-2836(05)80360-2

    Attems, C.G. (1897) Beitrag zur Kenntnis der rhabdocoelen Turbellarien Helgolands. Wissenschaftliche Meeresuntersuchungen der Kommission Abteilung Kiel, 2 (1), 219–232.

    Benson, D.A., Karsch-Mizrachi, I., Clark, K., Lipman, D.J., Ostell, J. & Sayers, E.W. (2012) GenBank. Nucleic Acids Research, 40, D48–D53.

    https://doi.org/10.1093/nar/gkr1202

    Brunet, M. (1965) Turbellariés calyptorhynques de substrats meubles de la région de Marseille. Recueil des Travaux de la Station Marine d’Endoume, 39 (55), 128–218.

    Brunet, M. (1972) Koinocystididae de la région de Marseille. Zoologica Scripta, 1, 157–174.

    https://doi.org/10.1111/j.1463-6409.1972.tb00673.x

    Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17, 540–552.

    https://doi.org/10.1093/oxfordjournals.molbev.a026334

    Claus, C. (1887) Lehrbuch der Zoologie. 4. Auflage. N. G. Elwertsche Verlagsbuchhandlung, Marburg, Leipzig, 1279 pp.

    Ehlers, U. (1985) Cytoskelette bei freilebenden Plathelminthen. Verhandlungen der Deutschen Zoologischen Gesellschaft, 78, 161.

    Ehrenberg, C.G. (1831) Animalia evertebrata exclusis insectis recensuit C.G. Ehrenberg. Series prima cum Tabularum decade prima. In: Hemprich, F.G. & Ehrenberg, C.G. (Eds.), Symbolae Physicae 2. Phytozoa Turbellaria. Officina Academica, Berolina, pp. 1–15.

    Fuhrmann, O. (1904) Ein neuer Vertreter eines marinen Turbellariengenus in Süsswasser. Zoologischer Anzeiger, 27, 381–384.

    Graff, L. von (1905) Marine turbellarien Orottavas und der Küsten Europas. Zeitschrift für wissenschaftliche Zoologie, 83, 68–148.

    Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0. Systematic Biology, 59 (3), 307–321.

    https://doi.org/10.1093/sysbio/syq010

    Hoang, D.T., Chernomor, O., Haeseler, Arndt von, Minh, B.Q. & Vinh, L.S. (2013) UFBoot2: Improving the Ultrafast Bootstrap Approximation. Molecular Biology and Evolution, 35 (2), 518–522.

    https://doi.org/10.1093/molbev/msx281

    Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., Haeseler, A. von & Jermiin, L.S. (2017) ModelFinder: Fast Model Selection for Accurate Phylogenetic Estimates. Nature Methods, 14 (6), 587–589.

    https://doi.org/10.1038/nmeth.4285

    Karling, T.G. (1952a) Kalyptorhynchia (Turbellaria). Further Zoological Results of the Swedish Antarctic Expedition, 4 (9), 1–50.

    Karling, T.G. (1952b) Studien über Kalyptorhynchien (Turbellaria) IV. Einige Eukalyptorhynchia. Acta Zoologica Fennica, 69, 1–49.

    Karling, T.G. (1954) Einige marine Vertreter der Kalyptorhynchien-Familie Koinocystididae. Arkiv för Zoologi, 7, 165−183.

    Karling, T.G. (1956) Morphologisch-histologische Untersuchungen an den männlichen Atrialorganen der Kalyptorhynchia (Turbellaria). Arkiv för Zoologi, Serie 2, 9 (7), 187–279.

    Karling, T.G. (1964) Über einige neue und ungenügend bekannte Turbellaria Eukalyptorhynchia. Zoologischer Anzeiger, 172, 159−183.

    Karling, T.G. (1978) Anatomy and Systematics of Marine Turbellaria from Bermuda. Zoologica Scripta, 7, 25–248.

    Karling, T.G. (1980) Revision of Koinocystididae (Turbellaria). Zoologica Scripta, 9, 241–269.

    https://doi.org/10.1111/j.1463-6409.1980.tb00666.x

    Karling, T.G., Mack-Fira, V. & Dörjes, J. (1972) First report on marine microturbellarians from Hawaii. Zoologica Scripta, 1, 251–269.

    https://doi.org/10.1111/j.1463-6409.1972.tb00575.x

    Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30 (4), 772–780.

    https://doi.org/10.1093/molbev/mst010

    Katoh, K., Rozewicki, J., Yamada, K.D. (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, 20 (4), 1160–1166.

    https://doi.org/10.1093/bib/bbx108

    Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A.A. (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28 (12), 1647–164.

    https://doi.org/10.1093/bioinformatics/bts199

    Lanfear, R., Calcott, B., Ho, S.Y.W. & Guindon, S. (2012) Partition Finder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701.

    https://doi.org/10.1093/molbev/mss020

    Lin, Y.-T., Feng, W.-T., Zhuang, J.-Y., Zhang, Y. & Wang, A.-T. (2017) Two new species of Kalyptorhynchia (Koinocystididae and Gnathorhynchidae) from China. Zootaxa, 4337 (4), 573-583.

    https://doi.org/10.11646/zootaxa.4337.4.8

    Mack-Fira, V. (1968) Turbellariés de la Mer Noire. Rapport de la Commission pour la Mer Méditerranée, 9 (2), 179–182.

    Mack-Fira, V. (1974) The turbellarian fauna of the Romanian littoral waters of the Black Sea and its annexes. In: Riser, N.W. & Morse, M.P. (Eds.), Biology of Turbellaria. McGraw-Hill, New York. pp. 248–290.

    Marcus, E. (1949) Turbellaria Brasileiros (7). Boletins da Faculdade de Filosofia Ciencias e Letras, Universidade de São Paulo Zoologia, 7 (14), 7−155.

    https://doi.org/10.11606/issn.2526-4877.bsffclzoologia.1949.129106

    Marcus, E. (1951) Turbellaria Brasileiros (9). Boletins da Faculdade de Filosofia, Ciencias e Letras, Universidade de São Paulo Zoologia, 16, 1−215.

    https://doi.org/10.11606/issn.2526-4877.bsffclzoologia.1951.125221

    Marcus, E. (1954) Turbellaria Brasileiros (11). Papéis Avulsos, 11, 419−489.

    https://doi.org/10.11606/issn.2526-4877.bsffclzoologia.1946.125301

    Meixner, J. (1924) Studien zu einer Monographie der Kalyptorhynchia und zum System der Turbellaria Rhabdocoela. Zoologischer Anzeiger, 60, 89−105.

    Meixner, J. (1925) Beitrag zur Morphologie und zum System der Turbellaria-Rhabdocoela. I. Die Kalyptorhynchia. Zeitschrift für Morphologie und Ökologie der Tiere, 3, 255–343.

    https://doi.org/10.1007/BF00408146

    Meixner, J. (1928) Der Genitalapparat der Tricladen und seine Beziehungen zu ihrer allgemeinen Morphologie, Phylogenie, Ökologie und Verbreitung. Zeitschrift für Morphologie und Ökologie der Tiere, 11 (5), 570–612.

    https://doi.org/10.1007/BF02424587

    Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop, 2010, 1–8.

    https://doi.org/10.1109/GCE.2010.5676129

    Nguyen, L.-T., Schmidt, H.A., Haeseler, A. von & Minh, B.Q. (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32 (1), 268–274.

    https://doi.org/10.1093/molbev/msu300

    Rambaut, A. (2006–2019) FigTree: Tree Figure Drawing Tool. Computer program distributed by the author. Available from: http://tree.bio.ed.ac.uk/software/figtree/ (accessed 14 August 2020)

    Reygel, P.C., Willems, W.R. & Artois, T.J. (2011) Koinocystididae and Gnathorhynchidae (Platyhelminthes: Rhabdocoela: Kalyptorhynchia) from the Galapagos, with the description of three new species. Zootaxa, 3096 (1), 27–40.

    https://doi.org/10.11646/zootaxa.3096.1.3

    Ronquist, F., Teslenko, M., Mark, P. van der, Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2 efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61 (3), 539–542.

    https://doi.org/10.1093/sysbio/sys029

    Schockaert, E.R. (1996) Turbellarians. In: Hall, G.S. (Ed.), Methods for the Examination of Organismal Diversity in Soils and Sediments. CAB International Wallingford, pp. 211–225.

    Sekera, E. (1912) Monographie der Gruppe Olisthanellini. Sitzungsberichte der Königlichen Böhmischen Gesellschaft der Wissenschaften. Classe für Mathematik und Naturwissenschaften, 24, 1–93.

    Strand, E. (1914) Neue Namen verschiedener Tiere. Archiv für Naturgeschichte, 80, 163–164.

    Tessens, B., Janssen, T. & Artois, T. (2014) Molecular phylogeny of Kalyptorhynchia (Rhabdocoela, Platyhelminthes) inferred from ribosomal sequence data. Zoologica Scripta, 43 (5), 519–530.

    https://doi.org/10.1111/zsc.12066

    Trifinopoulos, J., Nguyen, L.-T., Haeseler, Arndt von & Minh, B.Q. (2017) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research, 44, W232–W235.

    https://doi.org/10.1093/nar/gkw256

    Tyler, S., Artois, T., Schilling, S., Hooge, M. & Bush, L.F. (Eds.) (2006–2019) World List of turbellarian worms: Acoelomorpha, Catenulida, Rhabditophora. Koinocystididae Meixner, 1924. World Register of Marine Species. Available from: http://www.marinespecies.org/aphia.php?p=taxdetails&id=142395 (accessed 28 November 2018)

    Van Steenkiste, N., Tessens, B., Willems, W., Backeljau, T., Jondelius, U. & Artois, T. (2013) Comprehensive Molecular Phylogeny of Dalytyphloplanida (Platyhelminthes: Rhabdocoela) Reveals Multiple Escapes from the Marine Environment and Origins of Symbiotic Relationships. PLoS ONE, 8 (3), e59917.

    https://doi.org/10.1371/journal.pone.0059917

    Van Steenkiste, N.W.L. & Leander, B.S. (2018) Species diversity of eukalyptorhynch flatworms (Platyhelminthes, Rhabdocoela) from the coastal margin of British Columbia: Polycystididae, Koinocystididae and Gnathorhynchidae. Marine Biology Research, 14 (9–10), 899–923.

    https://doi.org/10.1080/17451000.2019.1575514

    Van Steenkiste, N.W.L., Herbert, E.R. & Leander, B.S. (2018) Species diversity in the marine microturbellarian Astrotorhynchus bifidus sensu lato (Platyhelminthes: Rhabdocoela) from the Northeast Pacific Ocean. Molecular Phylogenetics and Evolution, 120, 259–273.

    https://doi.org/10.1016/j.ympev.2017.12.012

    Willems, W., Reygel, P., Van Steenkiste, N., Tessens, B. & Artois, T. (2017) Kalyptorhynchia (Platyhelminthes: Rhabdocoela) from KwaZulu-Natal (South Africa), with the description of six new species. Zootaxa, 4242 (3), 441–466.

    https://doi.org/10.11646/zootaxa.4242.3.2

    Willems, W.R., Sandberg, M.I. & Jondelius, U. (2007) First report on Rhabdocoela (Rhabditophora) from deep parts of Skagerrak, with the description of four new species. Zootaxa, 1616 (1), 1–21.

    https://doi.org/10.11646/zootaxa.1616.1.1