Abstract
A phylogenetic analysis of Polycladida based on two partial mitochondrial genes (cox1 and 16S) is provided. The analysis includes 30 polyclad terminals that represent species from the two taxa which traditionally divide the groups Cotylea and Acotylea. Our phylogenetic analyses produced a well-supported hypothesis that confirms the monophyly of Polycladida, as well as Acotylea and Cotylea. Within Acotylea, there are two lineages not highly supported: on one hand, Leptoplanoidea (excluding Hoploplana elisabelloi) and one Stylochoidea member (Pseudostylochus intermedius) (classification sensu Faubel, 1983, 1984), and on the other hand, Stylochoidea members together with Discocelis tigrina and H. elisabelloi. The genera Stylochus and Imogine are not monophyletic. Within Cotylea, Pseudocerotidae and Euryleptidae are monophyletic, though not highly supported, while Prosthiostomidae is not. Euryleptoidea is paraphyletic. The genera Pseudobiceros and Pseudoceros are monophyletic and highly supported. Our results suggest that, within Acotylea, the prostatoid organs of Discocelis may have been derived from a prostatic vesicle. The genus Hoploplana could be included in Stylochoidea. Within Cotylea, the common ancestor of Euryleptidae and Pseudocerotidae might have been an aposematic animal with tentacles.
Similar content being viewed by others
References
Aguado, M. T., Grande, C., Gerth, M., Bleidorn, C., & Noreña, C. (2016). Characterization of the complete mitochondrial genomes from Polycladida (Platyhelminthes) using next-generation sequencing. Gene, 575, 199–205.
Allen, J. D., Klompen, A. M. L., Alpert, E. J., & Reft, A. J. (2017). Obligate planktotrophy in the Götte’s larva of Stylochus ellipticus (Platyhelminthes). Invertebrate Reproduction & Development, 61, 110–118.
Ax, P. (1995). Das System der Metazoa I. Ein Lehrbuch der phylogenetische Systematik. Stuttgart: Gustac Fischer Verlag 228 pp.
Ax, P. (1996). Multicellular animals: a new approach to the phylogenetic order in nature. Berlin: Springer 225 pp.
Bahia, J., Padula, V., & Schrödl, M. (2017). Polycladida phylogeny and evolution: integrating evidence from 28S rDNA and morphology. Organisms Diversity and Evolution, 17, 653–678. https://doi.org/10.1007/s13127-017-0327-5.
Bock, S. (1913) Studien über Polycladen. Zoologiska Bidrag Uppsala 2, 29–344.
Brusa, F., & Damborenea, C. (2011). Polycladida Acotylea from Patagonia. Redescription of Crassiplana albatrossi (Pseudostylochidae), lectotype designation and first record of Notocomplana palta (Notoplanidae). Zootaxa, 2903, 29–38.
Campos, A., Cummings, M. P., Reyes, J. L., & Laclette, J. P. (1998). Phylogenetic relationships of Platyhelminthes based on 18S ribosomal gene sequences. Molecular Phylogenetics and Evolution, 10, 1–10.
Cannon, L. R. G. (1986). Turbellaria of the world. A guide to families and genera. Brisbane: Queensland Museum 136 pp.
Doignon, G., Tom Artois, T., & Deheyn, D. (2003). Discoplana malagasensis sp. nov., a new turbellarian (Platyhelminthes: Polycladida: Leptoplanidae) symbiotic in an ophiuroid (Echinodermata), with a cladistic analysis of the Discoplana/Euplana species. Zoological Science, 20, 357–369.
Egger, E., Lapraz, F., Tomiczek, B., Müller, S., Dessimoz, C., Girstmair, J., Skunca, N., Rawlinson, K. A., Cameron, C. B., Beli, E., Todaro, M. A., Gammoudi, M., Noreña, C., & Telford, M. J. (2015). A transcriptomic-phylogenomic analysis of the evolutionary relationships of flatworms. Current Biology, 25, 1347–1353.
Faubel, A. (1983). The Polycladida, Turbellaria. Proposal and establishment of a new system. Part I. The Acotylea. Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut, 80, 17–121.
Faubel, A. (1984). The Polycladida, Turbellaria. Proposal and establishment of a new system. Part II. The Cotylea. Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut, 81, 189–259.
Folmer, O., Back, M., Hoeh, W., Lutz, R., & 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.
Gammoudi, M., Noreña, C., Tekaya, S., Prantl, V., & Egger, B. (2012). Insemination and embryonic development of some mediterranean polyclad flatworms. Invertebrates, Reproductive & Development, 56, 272–286.
Girard, C. (1854). Researches upon nemerteans and planarians: I, embryonic development of Planocera elliptica. Journal of the Academy of Natural Sciences of Philadelphia, 2, 307–325.
Golombek A, Tobergte S, Struck TH. (2015). Elucidating the phylogenetic position of Gnathostomulida and first mitochondrial genomes of Gnathostomulida, Gastrotricha and Polycladida(Platyhelminthes). Molecular Phylogenetics and Evolution, 86: 49-63. https://doi.org/10.1016/j.ympev.2015.02.013.
Jennings, K. A., & Newman, L. J. (1996). Two new stylochid flatworms (Platyhelminthes: Polycladida) from the Southern Great Barrier Reef, Australia. Raffles Bulletin of Zoology, 44(1), 135–142.
Katoh, K., Misawa, K., Kuma, K., & Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30, 3059–3066.
Kück, P., & Longo, G. C. (2014). FASconCAT-G: extensive functions for multiple sequence alignment preparations concerning phylogenetic studies. Frontiers in Zoology, 11, 1–8.
Lanfear, R., Calcott, B., Kainer, D., Mayer, C., & Stamatakis, A. (2014). Selecting optimal partitioning schemes for phylogenomic datasets. BMC Evolutionary Biology, 14, 82.
Lang, A. (1884). Die Polycladen (Seeplanarien) des Golfes von Neapel und der angrenzenden Meeresabschnitte. Eine Monographie. Fauna und Flora des Golfes von Neapel und der angrenzenden Meeresabschnitte. Zoologische Station in Neapel. W. Engelmann, Leipzig. Fauna Flora Golfes Neapel 11:ix+688 pp.
Lapraz, F., Rawlinson, K. A., Girstmair, J., Tomiczek, B., Berger, J., Jékely, G., Telford, M. J., & Egger, B. (2013). Put a tiger in your tank: the polyclad flatworm Maritigrella crozieri as a proposed model for evo-devo. EvoDevo, 4, 29.
Laumer, C. E., Bekkouche, N., Kerbl, A., Goetz, F., Neves, R. C., Sørensen, M. C., Kristensen, R. M., Hejnol, A., Dunn, C. W., Giribet, G., & Worsaae, K. (2015). Spiralian phylogeny informs the evolution of microscopic lineages. Current Biology, 25, 2000–2006.
Laumer, CE & Giribet, G. (2014). Inclusive taxon sampling suggests a single, stepwise origin of ectolecithality in Platyhelminthes. Biological Journal of the Linnean Society, 111(3), 570–588. https://doi.org/10.1111/bij.12236.
Littlewood, D. T. J., Rohde, K., & Clough, K. A. (1999). The interrelationships of all major groups of Platyhelminthes: phylogenetic evidence from morphology and molecules. Biological Journal of the Linnean Society, 66, 75–114.
Litvaitis, M. K., & Newman, L. J. (2001). A molecular framework for the phylogeny of the Pseudocerotidae (Platyhelminthes, Polycladida). Hydrobiologia, 444(1–3), 177–182.
Litvaitis, M. K., & Rhode, K. (1999). A molecular test of Platyhelminth phylogeny: inferences from partial 28S rDNA sequences. Invertebrate Biology, 118(1), 42–56.
Litvaitis, M. K., Bolaños, D. M., & Quiroga, S. Y. (2010). When names are wrong and colours deceive: unravelling the Pseudoceros bicolor species complex (Turbellaria: Polycladida). Journal of Natural History, 44(13–14), 829–845.
Marquina, D., Osca, D., Rodríguez, J., Fernández-Despiau, E., & Noreña, C. (2014a). State of knowledge of the Acotylea (Polycladida, Platyhelminthes) from the Mediterranean coasts of Spain: new records and new species. Zootaxa, 3780(1), 108–134.
Marquina, D., Fernández-Álvarez, F. Á., & Noreña, C. (2014b). Five new records and one new species of Polycladida (Platyhelminthes) for the Cantabrian coast (North Atlantic) of the Iberian Peninsula. Journal of the Marine Biological Association of the United Kingdom, 95(2), 311–322.
Marquina, D., Aguado, M. T., & Noreña, C. (2015). New records of Cotylea (Polycladida, Platyhelminthes) and one new species from Lizard Island (Australia), with remarks on the distribution of the Pseudoceros Lang, 1884 and Pseudobiceros Faubel, 1984 species of the Indo-Pacific marine region. Zootaxa, 4019(1), 354–377.
Newman, L., & Cannon, L. R. G. (1994). Pseudoceros and Pseudobiceros (Platyhelminthes, Polycladida, Pseudocerotidae) form eastern Australia and Papua New Guinea. Memoirs of the Queensland Museum, 37(1), 205–266.
Newman, L. J., Norenberg, J. L., & Reed, S. (2000). Taxonomic and biological observations on the tiger flatworm, Maritigrella crozieri (Hyman, 1939), new combination (Platyhelminthes, Polycladida, Euryleptidae) from Florida waters. Journal of Natural History, 34, 799–808.
Nguyen, L.-T., Schmidt, H. A., von Haeseler, A., & Minh, B. Q. (2015). IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274. https://doi.org/10.1093/molbev/msu300.
Noreña, C., Marquina, D., Pérez, J., & Almón, B. (2014). First records of Cotylea (Polycladida, Platyhelminthes) for the Atlantic coast of the Iberian peninsula. ZooKeys, 404, 1–22.
Noreña, C., Rodríguez, J., Pérez, J., & Almón, B. (2015). New Acotylea (Polycladida, Platyhelminthes) from the east coast of the North Atlantic Ocean with special mention of the Iberian littoral. Zootaxa, 4039(1), 157–172.
Palumbi, S. R. (1996). Nucleic acids II: the polymerase chain reaction. In D. M. Hillis, C. Moritz, & B. K. Mable (Eds.), Molecular systematics (2nd ed., pp. 205–247). Massachusetts: Sinauer.
Patzner, R. A., Hofricher, R., Schmidt-Rhaesa, A., Faubel, A., & Noreña, C. (2004). Plathelminthes: Einführung. In R. Hofrichter (Ed.), Das Mittelmeer (Vol. 20, pp. 654–668). Berlin: Spektrum Akademischer Verlag Heidelberg.
Prudhoe, S. (1985). A monograph on polyclad Turbellaria. Oxford: Oxford University Press 253 pp.
Rawlinson, K. A. (2010). Embryonic and post-embryonic development of the polyclad flatworm Maritigrella crozieri: implications for the evolution of spiralian life history traits. Frontiers in Zoology, 7, 12. https://doi.org/10.1186/1742-9994-7-12.
Rawlinson, K. A. (2014). The diversity, development and evolution of polyclad flatworm larvae. EvoDevo, 5, 1–12.
Rawlinson, K. A., & Litvaitis, M. K. (2008). Cotylea (Polycladida): a cladistic analysis of morphology. Invertebrate Biology, 127(2), 121–138.
Rawlinson, K. A., & Stella, J. S. (2012). Discovery of the corallivorous polyclad flatworm, Amakusaplana acroporae, on the Great Barrier Reef, Australia: the first report from the wild. PloS One, 7, e42240.
Rawlinson, K. A., Gillis, J. A., Billings, R. E., & Borneman, E. H. (2011). Taxonomy and life history of the Acropora-eating flatworm Amakusaplana acroporae nov. sp. (Polycladida: Prosthiostomidae). Coral Reefs, 30(3), 693–705.
Remane, A. (1929). Die Polycladen der Kieler Förde. Schriften Naturwiss Ver Schleswig-Holstein, 19, 73–79.
Romeis, B. (1989). Mikroskopische Technik (17 Auflage ed.). Miinchen: Verlag Oldenbourg 697 pp.
Ronquist, F., Teslenko, M., Mark, P. V. M., 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, 539–542.
Sambrook, J., Fritsch, E. F., & Maniatis, T. (1989). Molecular cloning: a laboratory manual (2nd ed.). Cold Spring Harbor: Cold Spring Harbor Laboratory Press 1626 pp.
Sato, K., Sugita, T., Kobayashi, K., Fujita, K., Fujii, T., Matsumoto, Y., Mikami, T., Nishizuka, N., Nishizuka, S., Shojima, K., Suda, M., Takahashi, G., Himeno, H., Muto, A., & Ishida, S. (2001). Localization of mitochondrial ribosomal RNA on the chromatoid bodies of marine planarian polyclad embryos. Development, Growth & Differentiation, 43, 107–114. https://doi.org/10.1046/j.1440-169X.2001.00558.x.
Teshirogi, W., Ishida, S., & Jatani, K. (1981). On the early development of some Japanese polyclads. Report of the Fukuara Marine Biological Laboratory, 9, 2–31.
Trifinopoulos, J., Nguyen, L. T., von Haeseler, A., & Minh, B. Q. (2016). W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research, 44(1), 232–235. https://doi.org/10.1093/nar/gkw256.
Tyler, S., Schilling, S., Hooge, M., & Bush, L. F. (2006-2016). Turbellarian taxonomic database, version 1.7. Available via: http://turbellaria.umaine.edu.
Acknowledgements
We are very grateful to Fernando Angel Fernández-Álvarez for kindly sending material of Imogine fafai, and Torsten H. Struck (University of Oslo) for sending material of Stylochoplana and Leptoplana collected in Helgoland, Germany. Specimens from Galicia were collected by Jacinto Perez and the Grupo de Estudo do Medio Mariño (GEMM). Material from Lizard Island was collected during the Polychaetes Workshop 2013, funded by The Lizard Island Research Foundation, permit number G12/35718.1 issued by the Great Barrier Reef Marine Park Authority to Dr. Hutchings, Australian Museum. We are very grateful to Pat Hutchings, Elena Kupriyanova, María Capa and Anna Murray for their help collecting, registering and loaning material and to Alexander Semenov for the picture of Pseudoceros paralaticlavus. We acknowledge Anna Maria Addamo (MNCN), Agostina Vertino (UNIMIB), Silvia Spezzaferri (UNIFR), Andy Wheeler (UCC) and Commander, crew and scientific party of the Moira Mound EUROFLEETS cruise aboard the Belgica R/V, funded by the European Union Seventh Framework Programme (FP7/2007-2013), under the Eurofleets grant agreement no. 228344.
Funding
This project was supported by the Museo Nacional de Ciencias Naturales (CSIC), the Spanish MEC and the Universidad Autónoma de Madrid and funded by project CGL2011-29916, PI: Cristina Grande; and CGL2015-63593-P supported by the MINECO/FEDER, UE funds, PI: M. Teresa Aguado. Christoph Bleidorn is a “Ramon y Cajal” fellow supported by the Spanish Ministry of Science and Education (MEC) (RYC-2014-15615).
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
Fig. 1
Phylogenetic hypothesis after BI analyses of combined data set. Posterior probability support values below nodes. (PDF 155 kb)
Rights and permissions
About this article
Cite this article
Aguado, M.T., Noreña, C., Alcaraz, L. et al. Phylogeny of Polycladida (Platyhelminthes) based on mtDNA data. Org Divers Evol 17, 767–778 (2017). https://doi.org/10.1007/s13127-017-0344-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13127-017-0344-4