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Organisms Diversity & Evolution

, Volume 17, Issue 3, pp 653–678 | Cite as

Polycladida phylogeny and evolution: integrating evidence from 28S rDNA and morphology

  • Juliana BahiaEmail author
  • Vinicius Padula
  • Michael Schrödl
Original Article

Abstract

Polyclad flatworms have a troubled classification history, with two contradicting systems in use. They both rely on a ventral adhesive structure to define the suborders Acotylea and Cotylea, but superfamilies were defined according to eyespot arrangement (Prudhoe’s system) or prostatic vesicle characters (Faubel’s system). Molecular data available cover a very limited part of the known polyclad family diversity and have not allowed testing morphology-based classification systems on Polycladida yet. We thus sampled a suitable marker, partial 28S ribosomal DNA (rDNA), from Polycladida (19 families and 32 genera), generating 136 new sequences and the first comprehensive genetic dataset on polyclads. Our maximum likelihood (ML) analyses recovered Polycladida, but the traditional suborders were not monophyletic, as the supposedly acotyleans Cestoplana and Theama were nested within Cotylea; we suggest that these genera should be included in Cotylea. The partial 28S rDNA trees were generally well supported and robust but in conflict with both Faubel’s and Prudhoe’s superfamilies. Therefore, we compiled morphological and anatomical characters for all taxa used and examined their distribution on our molecular tree. Combining morphological and molecular evidence, we redefined polyclad superfamilies. Acotylea contain tentaculated and atentaculated groups and is now divided in three superfamilies. The suborder Cotylea can be divided in five superfamilies. In general, there is a trait of anteriorization of sensory structures, from the plesiomorphic acotylean body plan to the cotylean gross morphology. Traditionally used characters, such as prostatic vesicle, eyespot distribution, and type of pharynx, are all homoplastic and likely have misled polyclad systematics so far.

Keywords

Platyhelminthes Marine flatworms Cotylea Acotylea Molecular phylogenetics Morphology 

Notes

Acknowledgements

We are thankful to colleagues that helped in the collection and providing material studied here: Prof. Dr. Juan Lucas Cervera and MSc. Patricia Perez (Universidad de Cádiz, Spain), Ariane Dimitris (USA), Prof. Dr. Peter Wirtz, Dr. Judith Brown, Dr. Yuri Deart, Dr. Bastian Brenzinger, Prof. Dr. Fernanda Cavalcanti, and Prof. Dr. Emilio Lanna (Universidade Federal da Bahia, Brazil). Our thanks extend to Arnaldo Campos Perez (Hospital Universitário Clementino Fraga Filho, Universidade Federal do Rio de Janeiro, Brazil) and Dr. Isabel Berning (ZSM, Germany) for the help in the laboratory work and MSc. Isabella Stöger for both the laboratory and analysis help. We thank Prof. Dr. Ulf Jondelius (Swedish Natural History Museum) and the SYNTHESIS program for the access to the Polycladida collection of the SNHM. We also thank an anonymous referee and the Editor Prof. Dr. Andreas Wanninger for their helpful critic and comments. The first and second authors are CNPq (Brazil) and DAAD (Germany) fellowship holders. Lab work was supported by the Deutsche Forschungsgemeinschaft (DFG; to MS).

Supplementary material

13127_2017_327_MOESM1_ESM.jpg (685 kb)
Supplementary Figure 1 Polycladida 28S rDNA phylogram (RAxML, numbers refer to bootstrap support values). (JPEG 684 kb)
13127_2017_327_MOESM2_ESM.jpg (521 kb)
Supplementary Figure 2 Acotylea 28S rDNA phylogram (RAxML, numbers refer to bootstrap support values). (JPEG 520 kb)
13127_2017_327_MOESM3_ESM.jpg (863 kb)
Supplementary Figure 3 Cotylea 28S rDNA phylogram (RAxML, numbers refer to bootstrap support values). (JPEG 862 kb)

References

  1. Aguado, M. T., Grande, C., Gerth, M., Bleidorn, C., & Noreña, C. (2015). Characterization of the complete mitochondrial genomes from Polycladida (Platyhelminthes) using next-generation sequencing. Gene, 575, 199–205.CrossRefPubMedGoogle Scholar
  2. Ang, H. P., & Newman, L. J. (1998). Warning colouration in pseudocerotid flatworms (Platyhelminthes, Polycladida). A preliminary study. Hydrobiologia, 383, 29–33.CrossRefGoogle Scholar
  3. Ax, P. (1995). Das System der Metazoa I. Stuttgart: Gustav Fischer.Google Scholar
  4. Bahia, J. (2015). First records of polyclads (Platyhelminthes, Polycladida) associated with Nodipecten nodosus (Linnaeus 1758) aquaculture. Marine Biodiversity, 1–5. doi: 10.1007/s12526-015-0425-6.
  5. Bahia, J., & Schrödl, M. (2016). Pseudobiceros wirtzi sp. nov. (Polycladida: Cotylea) new species from Senegal with revision of valid species of the genus. Zootaxa, 4097(1), 101–117.CrossRefPubMedGoogle Scholar
  6. Bahia, J., Padula, V., Correia, M.D. & Sovierzoski, H.H. (2015). First records of the order Polycladida (Platyhelminthes, Rhabditophora) from reef ecosystems of Alagoas State, north-eastern Brazil, with the description of Thysanozoon alagoensis sp. nov. Journal of the Marine Biological Association of the United Kingdom, 1–14.Google Scholar
  7. Blanchard, E. (1847) Recherches sur l’organisation des vers. Annales des sciences naturelles Zoologie ser 3(7), 87–128, (8) 119–149, 271–275, tab 8, 9 and fig. 1.Google Scholar
  8. Bock, S. (1913). Studien über Polycladen. Zoologiska Bijdrag fran Uppsala, 2, 31–344.Google Scholar
  9. Bock, S. (1922). Two new cotylean genera of polyclads from Japan and remarks on some other cotyleans. Arkiv för Zoologi, 14(13), 1–31.Google Scholar
  10. Bock, S. (1923). Boninia, a new polyclad genus from the Pacific. Nova Acta Regiae Societatis Scientiarum Upsaliensis, 4(6), 1–32.Google Scholar
  11. Bolaños, D. M., Quiroga, S. Y., & Litvaitis, M. K. (2007). Five new species of cotylean flatworms (Platyhelminthes: Polycladida) from the wider Caribbean. Zootaxa, 1650, 1–23.Google Scholar
  12. Bulnes, N. V., & Torres, Y. (2014). Pseudoceros astrorum, a new species of Polycladida (Cotylea, Pseudocerotidae) from northeastern Brazil. Zootaxa, 3881(1), 94–100.CrossRefPubMedGoogle Scholar
  13. Bulnes, N. V., Faubel, A., & Ponce de León, R. (2003). New species of Stylochocestidae and Cryptocelidae (Platyhelminthes, Polycladida: Acotylea) from the Atlantic coast of Uruguay. Mitteilungen Hamburbischen Zoologischen Museum und Institute, 100, 59–72.Google Scholar
  14. Bulnes, N. V., Faubel, A., & Park, J. K. (2005). Two new marine species from South Korea with remarks on the family Stylochidae (Acotylea, Polycladida, Platyhelminthes). Journal of Natural History, 39(23), 2089–2107.CrossRefGoogle Scholar
  15. 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), 1–10.CrossRefPubMedGoogle Scholar
  16. Chiaje, D., (1822) Memorie sulla storia e notomia degli animali senza vertebre dell regno di Napoli. 109 p.Google Scholar
  17. Corrêa, D. D. (1958). A new Polyclad from Brazil. Boletim do Instituto Oceanográfico de São Paulo, 7(1–2), 81–84.Google Scholar
  18. Curini-Galletti, M., Campus, P., & Delogu, V. (2008). Theama mediterranea sp. nov. (Platyhelminthes, Polycladida), the first interstitial polyclad from the Mediterranean. Italian Journal of Zoology, 75(1), 77–83.CrossRefGoogle Scholar
  19. de Blainville, D. (1828). Dictionnaire des Sciences naturelles. p. 204–218.Google Scholar
  20. de Quatrefages, A. (1845). Études sur les types inférieurs de l’embranchement des annelés: mémoire sur quelques planairées marines appartenant aux genres Tricelis (Ehr.), Polycelis (Ehr.), Prosthiostomum (Nob.), Proceros (Nob.), Eolidiceros (Nob.), et Stylochus (Ehr). Annales des Sciences Naturelles, (3) Zool 4, 129–184.Google Scholar
  21. Du Bois-Reymond Marcus, E. (1957). On Turbellaria. Anais da Academia Brasileira de Ciências, 29(1), 153–191.Google Scholar
  22. Du Bois-Reymond Marcus, E. (1965). Drei neue neotropische Turbellaria. Sitzungsberichte der Gesellshaft naturforschender Freunde zu Berlin, 5, 129–135.Google Scholar
  23. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5), 1792–1797.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Egger, B., Gschwentner, R., & Rieger, R. (2007). Free-living flatworms under the knife: past and present. Development Genes and Evolution, 217, 89–104.CrossRefPubMedGoogle Scholar
  25. Egger, B., 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, 1–7.CrossRefGoogle Scholar
  26. Ehlers, U. (1985). Das phylogenetische system der Platyhelminthes. Stuttgart: Gustav Fischer Verlag 317 pp.Google Scholar
  27. Ehlers, U. (1986). Comments on a phylogenetic system of the Platyhelminthes. Hydrobiologia, 132, 1–12.CrossRefGoogle Scholar
  28. Ehrenberg, C.G. (1831). Phytozoa Turbellaria africana et asiatica. In: Hemprich und Ehrenberg “Symbolae physicae.”Google Scholar
  29. Faubel, A. (1983). The Polycladida, Turbellaria; proposal and establishment of a new system. Part I. The Acotylea. Mitteilungen Hamburbischen Zoologischen Museum und Institute, 80, 17–121.Google Scholar
  30. Faubel, A. (1984). The Polycladida, Turbellaria proposal and establishment of a new system part II. The Cotylea. Mitteilungen Hamburbischen Zoologischen Museum und Institute, 81, 189–259.Google Scholar
  31. Girard, C. F. (1853). Descriptions of new nemerteans and planarians from the coast of the Carolinas. Proceedings of the Academy of Natural Sciences of Philadelphia, 6, 365–367.Google Scholar
  32. Grube, A.E. (1840). Actinien, Echinodermen und Würmer des adriatischen und Mittelmeers, nach eigenen Sammlungenbeschrieben. Königsberg, 92pp.Google Scholar
  33. Halanych, K. M. (2016). How our views of animal phylogeny was reshaped by molecular approaches: lessons learned. Organisms Diversity & Evolution. doi: 10.1007/s13127-016-0264-8.Google Scholar
  34. 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
  35. Haswell, W. A. (1907). Observations on Australian polyclads. Transactions of the Linnean Society of London, Zoology, 9(2), 465–485.CrossRefGoogle Scholar
  36. Hyman, L. H. (1939a). Acoel and Polyclad Turbellaria from Bermuda and the Sargassum. Bulletin of the Bingham Oceanographic Collection, 7(1), 1–35.Google Scholar
  37. Hyman, L. H. (1939b). Some polyclads of the New England coast, especially of the woods hole region. Biological Bulletin, 76(2), 127–152.CrossRefGoogle Scholar
  38. Hyman, L. H. (1939c). Polyclad worms collected on the presidential cruise of 1938. Smithsonian Miscellaneous Collections, 38(17), 1–12.Google Scholar
  39. Hyman, L. H. (1951). The invertebrates: Vol. II. Platyhelminthes and Rhynchocoela; the acelomate Bilateria. New York: McGraw-Hill 572 pp.Google Scholar
  40. Hyman, L. H. (1953). The polyclad flatworms of the Pacific coast of North America. Bulletin of the American Museum of Natural History, 100(2), 265–392.Google Scholar
  41. Hyman, L. H. (1955). Some Polyclad flatworms from the West Indies and Florida. Proceedings of the United States National Museum, 104(3341), 115–150.CrossRefGoogle Scholar
  42. Janssen, T., Vizoso, D., Schulte, G., Littlewood, D. T. J., Waeschenbach, A., & Schärer, L. (2015). The first multi-gene phylogeny of the Macrostomorpha sheds light on the evolution of sexual and asexual reproduction in basal Platyhelminthes. Molecular Phylogenetics and Evolution, 92, 82–107.CrossRefPubMedGoogle Scholar
  43. Kato, K. (1934). Polyclad turbellarians from the neighborhood of the Mitsui Institute of Marine Biology. Japanese Journal of Zoology, 6, 123–129.Google Scholar
  44. Kato, K. (1938). Polyclads from Amakusa, southern Japan. Japanese Journal of Zoology, 7, 559–576.Google Scholar
  45. 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. (2012). Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28(12), 1647–1649.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Ladurner, P., Schärer, L., Salvenmoser, W., & Rieger, R. M. (2005). A new model organism among the lower Bilateria and the use of digital microscopy in taxonomy of meiobenthic Platyhelminthes: Macrostomum lignano n. sp. (Rhabditophora, Macrostomorpha). Journal of Zoological and Systematic Evolution Research, 43, 114–126.CrossRefGoogle Scholar
  47. Laidlaw, F. F. (1902). The marine Turbellaria, with an account of the anatomy of some of the species. The Fauna and Geography of the Maldive and Laccadive Archipelagoes, 1(3), 282–312.Google Scholar
  48. Laidlaw, F. F. (1903a). Notes on some marine Turbellaria from Torres Straits and the Pacific, with a description of new species. Memoirs and Proceedings of the Manchester Literary and Philosophical Society, 47(5), 1–12.Google Scholar
  49. Laidlaw, F.F. (1903b) On a collection of Turbellaria Polycladida from the straits of Malacca (Skeat Expedition, 1889–1900). Proceedings of the Zoological Society of London, 1903, 301–318.Google Scholar
  50. Laidlaw, F. F. (1903c). IV. Suggestions for a revision of the classification of the Polyclad Turbellaria. Manchester Memoirs, 48(4), 1–16.Google Scholar
  51. Lang, A. (1884) Die Polycladen (Seeplanarien) des Golfes von Neapel und der angrenzenden Meeresabschnitte. Eine Monographie. Fauna Flora Golfes v. Neapel, Leipzig, 11, ix+668pp.Google Scholar
  52. Laumer, C. E., & Giribet, G. (2014). Inclusive taxon sampling suggests a single, stepwise origin of ectolecithality in Platyhelminthes. Biological Journal of the Linnean Society, 111, 570–588.CrossRefGoogle Scholar
  53. Laumer, C. E., Hejnol, A., & Giribet, G. (2015). Nuclear genomic signals of the ‘microturbellarian’ roots of platyhelminth evolutionary innovation. eLife, 4(e05503), 1–31.Google Scholar
  54. 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.CrossRefGoogle Scholar
  55. Litvaitis, M. K., & Newman, L. J. (2001). A molecular framework for the phylogeny of the Pseudocerotidae (Platyhelminthes, Polycladida). Hydrobiologia, 444, 177–182.CrossRefGoogle Scholar
  56. Litvaitis, M. K., & Rhode, K. (1999). A molecular test of Platyhelminth phylogeny: inferences from partial 28S rDNA sequences. Invertebrate Biology, 118(1), 42–56.CrossRefGoogle Scholar
  57. Litvaitis, M. K., Bolaños, D. M., & Quiroga, S. Y. (2010). When names are wrong and colours deceive: unraveling the Pseudoceros bicolor species complex (Turbellaria: Polycladida). Journal of Natural History, 44, 829–845.CrossRefGoogle Scholar
  58. Marcus, E. (1947). Turbelários marinhos do Brasil. Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, Zoologia, 12, 99–206.Google Scholar
  59. Marcus, E. (1949). Turbellaria brasileiros (7). Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, Zoologia, 14, 7–155.Google Scholar
  60. Marcus, E. (1950). Turbellaria brasileiros (8). Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, Zoologia, 15, 69–190.Google Scholar
  61. Marcus, E. (1952). Turbellaria brasileiros (10). Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, Zoologia, 17, 5–186.Google Scholar
  62. Marcus, E., & Marcus, E. (1951). Contributions to the natural history of Brazilian Turbellaria. Comunicaciones Zoologicas del Museu de Historia Natural de Montevideo, 63(3), 1–25.Google Scholar
  63. Marcus, E., & Marcus, E. (1966). Systematische Übersicht der Polycladen. Zoologische Beitrage, 21, 320–343.Google Scholar
  64. Marcus, E., & Marcus, E. (1968). Polycladida from Curaçao and faunistically related regions. Studies on the Fauna of Curaçao and other Caribbean Islands, 101, 1–133.Google Scholar
  65. Meixner, A. (1907). Polykladen von der Somalikuest, nebst einer Revision der Stylochinen. Zeitschrift fur wissenschaftliche Zoologie, 88, 385–498.Google Scholar
  66. Montagu, G. (1815). Description of several new or rare animals principally marine, discovered on the south coast of Devonshire. Transactions of the Linnean Society of London, 11, 25–26.Google Scholar
  67. Müller, O. F. (1773). Vermium terrestrium et fluviatilium, seu animalium infusoriorum, helminthicorum et testaceorum, non marinorum, succincta historia. Vol. primi pars altera. Havniae et Lipsiae, 4, 52–72.Google Scholar
  68. Newman, L. J., & Cannon, L. R. G. (1994). Pseudoceros and Pseudobiceros (Platyhelminthes, Polycladida, Pseudocertotidae) from eastern Australia and Papua New Guinea. Memoirs of the Queensland Museum, 37(1), 205–266.Google Scholar
  69. Newman, L. J., & Cannon, L. R. G. (1995). Colour pattern variation in the tropical flatworm, Pseudoceros (Platyhelminthes: Polycladida), with descriptions of three new species. The Raffles Bulletin of Zoology, 43(2), 435–446.Google Scholar
  70. Newman, L. J., & Cannon, L. R. G. (1996). New genera of pseudocerotid flatworms (Platyhelminthes; Polycladida) from Australian and Papua New Guinean coral reefs. Journal of Natural History, 30(10), 1425–1441.CrossRefGoogle Scholar
  71. Newman, L. J., & Cannon, L. R. G. (2000). A new genus of euryleptid flatworm (Platyhelminthes, Polycladida) from the Indo-Pacific. Journal of Natural History, 34(2), 191–205.CrossRefGoogle Scholar
  72. Newman, L., & Cannon, L. (2003). Marine flatworms: the world of polyclads. Collingwood: Csiro 97pp.Google Scholar
  73. Palombi, A. (1928). Report on the Turbellaria (Cambridge Expedition Suez Canal 1924). Transactions of the Zoological Society of London, 22, 579–631.CrossRefGoogle Scholar
  74. Pearse, A. S., & Wharton, G. W. (1938). The oyster “leech,” Stylochus inimicus Palombi, associated with oysters on the coasts of Florida. Ecological Monographies, 8(4), 605–656.CrossRefGoogle Scholar
  75. Poche, F. (1926). Das System der Platodaria. Archiv für Naturgeschichte Abteilung A, 91, 1–458.Google Scholar
  76. Prudhoe, S. (1978). Some polyclad turbellarians new to the fauna of the Australian coasts. Records of the Australian Museum, 31(14), 586–604.CrossRefGoogle Scholar
  77. Prudhoe, S. (1985). A monograph on Polyclad Turbellaria. London: British Museum of Natural History and Oxford University Press 259 pp.Google Scholar
  78. Quiroga, S. Y., Bolaños, D. M., & Litvaitis, M. K. (2006). First description of deep-sea polyclad flatworms from the North Pacific: Anocellidus n. Gen. profundus n. sp. (Anocelidae, n. Fam.) and Oligocladus voightae n. sp. (Euryleptidae). Zootaxa, 1317, 1–19.Google Scholar
  79. Quiroga, S. Y., Bonilla, E. C., Bolaños, D. M., Carbayo, F., Litvaitis, M. K., & Brown, F. D. (2015). Evolution of flatworms central nervous systems: insights from polyclads. Genetics and Molecular Biology, 38(3), 233–248.CrossRefPubMedPubMedCentralGoogle Scholar
  80. Rawlinson, K. A. (2008). Biodiversity of coastal polyclad flatworm assemblages in the wider Caribbean. Marine Biology, 153, 769–778.CrossRefGoogle Scholar
  81. Rawlinson, K. A., & Litvaitis, M. K. (2008). Cotylea (Polycladida): a cladistics analysis of morphology. Invertebrate Biology, 127(2), 121–138.CrossRefGoogle Scholar
  82. 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(8), 1–6.CrossRefGoogle Scholar
  83. Rawlinson, K. A., Bolaños, D. M., Liana, M. K., & Litvaitis, M. K. (2008). Reproduction, development and parental care in two direct-developing flatworms (Platyhelminthes: Polycladida: Acotylea). Journal of Natural History, 42(33–34), 2173–2192.CrossRefGoogle Scholar
  84. 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.CrossRefGoogle Scholar
  85. Risso, A. (1818). Sur quelques gasteropodes nouveaux, nudibranches et testibranches observes dans la mer de Nice. Journal de Physique Chimie et Histoire Naturelle, 87, 368–376.Google Scholar
  86. Ritson-Williams, R., Yotsu-Yamashita, M., & Paul, V. J. (2006). Ecological functions of tetrodotoxin in a deadly polyclad flatworm. PNAS, 103(9), 3176–3179.CrossRefPubMedPubMedCentralGoogle Scholar
  87. Schmmarda, L.K. (1859). Neue Turbellarien, Rotatorien und Anneliden beobachtet und gesammelt auf einer Reise um die Erde 1853 bis 1857. In: Neue Wirbellose thiere I. 1–66, 15pl.Google Scholar
  88. Schultze, M. (1851). Beiträge zur Naturgeschichte der Turbellarien. Greifswald. 78 p.Google Scholar
  89. Schupp, P., Steubeb, K., Meyerb, C., & Proksch, P. (2001). Anti-proliferative effects of new staurosporine derivatives isolated from a marine ascidian and its predatory flatworm. Cancer Letters, 174, 165–172.CrossRefPubMedGoogle Scholar
  90. Shimodaira, H. (2002). An approximately unbiased test of phylogenetic tree selection. Systematic Biology, 51, 492–508.CrossRefPubMedGoogle Scholar
  91. Shimodaira, H., & Hasegawa, M. (2001). CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics, 17, 1246–1247.CrossRefPubMedGoogle Scholar
  92. Sluys, R., Faubel, A., Rajagopal, S., & van der Velde, G. (2005). A new and alien species of “oyster leech” (Platyhelminthes, Polycladida, Stylochidae) from the brackish North Sea Canal, the Netherlands. Helgoland Marine Research, 59, 310–314.CrossRefGoogle Scholar
  93. Sòla, E., Álvarez-Presa, M., Frías-López, C., Littlewood, D. T. J., Rozas, J., & Riutort, M. (2015). Evolutionary analysis of mitogenomes from parasitic and free-living flatworms. PloS One, 10(3), 1–20.CrossRefGoogle Scholar
  94. Sonnenberg, R., Nolte, A. W., & Tautz, D. (2007). An evaluation of LSU rDNA D1-D2 sequences for their use in species identification. Frontiers in Zoology, 4, 6–18.CrossRefPubMedPubMedCentralGoogle Scholar
  95. Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22(21), 2688–2690.CrossRefPubMedGoogle Scholar
  96. Steinböck, O., & Reisinger, E. (1924). On Prorhynchus putealis Haswell, with a description of a new species of the genus. Quarterly Journal of Microscopical Science, 68, 443–451.Google Scholar
  97. Stimpson, W. (1857). Prodromus descriptionis animalium evertebratorum, quae in Expeditione ad Oceanum Pacificum Septentrionalem a Republica Federata missa, Johanne Rodgers Duce, observavit et descripsit. Pars I, Turbellaria Dendrocoela. Proceedings of the Academy of Science of Philadelphia, 9, 19–31.Google Scholar
  98. Stummer-Traunfels, R. (1933). Polycladida (continued). pp. 3485–3596. In Bronn, H.G. (ed.), Klassen und Ordnungen des Tier-Reichs IV. (Vermes). (Leipzig).Google Scholar
  99. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10), 2731–2739.CrossRefPubMedPubMedCentralGoogle Scholar
  100. Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.CrossRefPubMedPubMedCentralGoogle Scholar
  101. Telford, M. J., Herniou, E., Russell, R. B., & Littlewood, T. J. (2000). Changes in mitochondrial genetic codes as phylogenetic characters: two examples from the flatworms. PNAS, 97(21), 11359–11364.CrossRefPubMedPubMedCentralGoogle Scholar
  102. Telford, M. J., Budd, G. E., & Phillippe, H. (2015). Phylogenomic insights into animal evolution. Current Biology, 25, 876–887.CrossRefGoogle Scholar
  103. Tyler S, Schilling S, Hooge M, and Bush L.F. (comp.) (2006–2016) Turbellarian taxonomic database. Version 1.7 http://turbellaria.umaine.edu.
  104. Verrill, A.E. (1882). Notice of the remarkable marine fauna occupying the outer banks off the southern coast of New England, No. 7, and of some additions to the fauna of Vineyard Sound. American Journal of Science, 24, 360 pages.Google Scholar
  105. Verrill, A. E. (1900). Additions to the Turbellaria, Nemertina, and Annelida of the Bermudas. Transactions of the Connecticut Academy of Arts and Science, 10, 595–670.CrossRefGoogle Scholar
  106. Verrill, A. E. (1901). Additions to the fauna of the Bermudas from the Yale Expedition of 1901, with notes on other species. Transactions of the Connecticut Academy of Arts and Sciences, 11, 15–62.Google Scholar
  107. Woodworth, W. M. (1898). Some planarians from great barrier reef of Australia. Bulletin of the Museum of Comparative Zoology of Harvard College, 32(4), 61–67 1 table.Google Scholar

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© Gesellschaft für Biologische Systematik 2017

Authors and Affiliations

  1. 1.SNSB-Zoologische Staatssammlung MünchenMunichGermany
  2. 2.GeoBioCenter LMU and Biozentrum of the Ludwig-Maximilians Universität MünchenMunichGermany
  3. 3.Department of Marine BiotecnologyInstituto de Estudos do Mar Almirante Paulo Moreira (IEAPM)Arraial do CaboBrazil

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