Evolutionary history of the Tricladida and the platyhelminthes: An up-to-date phylogenetic and systematic account

International Journal of Developmental Biology

Volumn 56, Issue 1-3, 2012, Pages 5-17

  Riutort, Marta ^a   Álvarez Presas, Marta ^a   Lázaro, Eva ^a   Solà, Eduard ^a   Paps, Jordi ^b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Metazoa; Molecular phylogeny; Platyhelminthes; Systematic; Tricladida

Indexed keywords

ANNELID WORM; ARTICLE; CLASSIFICATION; DNA BARCODING; EVOLUTION; FAMILIA; FRESHWATER SPECIES; GENE EXPRESSION; GENETIC VARIABILITY; GENUS; HOX GENE; METAZOON; MOLECULAR PHYLOGENY; MOLLUSC; NONHUMAN; ORDO; PHYLOGENY; PHYLOGEOGRAPHY; PHYLUM; PLATYHELMINTH; PRIORITY JOURNAL; REGENERATION; SOUTHERN EUROPE; SPECIES; SPECIES DISTRIBUTION; TRICLADIDA; TURBELLARIA;

ANIMALS; BIOLOGICAL EVOLUTION; PHYLOGENY; PLATYHELMINTHS;

ANNELIDA; CATENULIDA; DUGESIA (TURBELLARIAN); LOPHOTROCHOZOA; METAZOA; MOLLUSCA; PLATYHELMINTHES; SCHMIDTEA; TRICLADIDA; TURBELLARIA;

EID: 84859143153     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.113441mr     Document Type: Article

References (92)

1. ABOUHEIF, E., ZARDOYA, R. and MEYER, A. (1998). Limitations of metazoan 18S rRNA sequence data: implications for reconstructing a phylogeny of the animal kingdom and inferring the reality of the Cambrian explosion. J Mol Evol 47: 394-405.
2. ÁLVAREZ-PRESAS, M., BAGUÑÀ, J. and RIUTORT, M. (2008). Molecular phylogeny of land and freshwater planarians (Tricladida, Platyhelminthes): From freshwater to land and back. Mol Phylogenet Evol 47: 555-568.
3. ÁLVAREZ-PRESAS, M., CARBAYO, F., ROZAS, J. and RIUTORT, M. (2011). Land planarians (Platyhelminthes) as a model organism for fine-scale phylogeographic studies: understanding patterns of biodiversity in the Brazilian Atlantic Forest hotspot. J Evolution Biol 24: 887-896.
4. ANDERSON, F.E., CORDOBA, A.J. and THOLLESSON, M. (2004). Bilaterian phylogeny based on analyses of a region of the sodium-potassium ATPase beta-subunit gene. J Mol Evol 58: 252-68.
5. BAGUÑÀ, J., CARRANZA, S., PALA, M., RIBERA, C., GIRIBET, G., ARNEDO, M.A., RIBAS, M. and RIUTORT, M. (1999). From morphology and karyology to molecules. New methods for taxonomical identification of asexual populations of freshwater planarians. A tribute to Professor Mario Benazzi. Ital. J. Zool. 66: 207-214.
6. BAGUÑÀ, J., CARRANZA, S., PAPS, J., RUIZ-TRILLO, I. and RIUTORT, M. (2001). Molecular taxonomy and phylogeny of Tricladida. In Interrelationships of the Platyhelminthes (Eds. D.T.J. Littlewood and R.D. Bray). Taylor and Francis, London, England, pp: 49-56.
7. BAGUÑÀ, J. and RIUTORT, M. (2004). Molecular phylogeny of the Platyhelminthes. Can. J. Zool, no. 82: 168-193.
8. BALL, I.R. (1981). The phyletic status of the Paludicola. Hydrobiologia 84: 7-12.
9. BALL, I.R. (1977). On the phylogenetic classi¢cation of aquatic planarians. Acta Zool. Fenn. 154: 21-35.
10. BALL, I.R. (1974). A contribution to the phylogeny and biogeography of the freshwater Triclads (Platyhelminthes: Turbellaria). Biology of the Turbellaria, (Eds. N.W. Riser and M.P. Morse). McGraw-Hill, NY.
11. BENAZZI, M. (1982). Speciation events evidenced in Turbellaria. In Mechanisms of Speciation (Ed. C. Barigozzi, Alan R. Liss). New York, pp. 307-344.
12. BENAZZI, M. (1957). Cariologia di Dugesia lugubris (0. Schmidt) (Tricladida, Paludicola). Cariologia 10: 276-303.
13. BENAZZI, M., BAGUÑÀ, J., BALLESTER, R., PUCCINELLI, I. and DEL PAPA, R. (1975). Further contribution to the taxonomy of the Dugesia lugubris-polychroa group- with description of Dugesia mediterranea n.sp. (Tricladida, Paludicola). Boll. Zool. 42: 81-89.
14. BENAZZI, M. and BENAZZI-LENTATI, G. (1976). Animal Cytogenetics. Vol. I Platyhehninthes, Gebruder Borntraeger, Berlin.
15. BOURLAT, S.J., NIELSEN, C., ECONOMOU, A.D. and TELFORD, M.J. (2008). Testing the new animal phylogeny: A phylum level molecular analysis of the animal kingdom. Mol Phylogenet Evol 49: 23-31.
16. CARBAYO, F., LEAL-ZANCHET, A.M. and VIEIRA, E.M. (2002). Terrestrial flatworm (Platyhelminthes: Tricladida: Terricola) diversity versus man-induced disturbance in an ombrophilous forest in southern Brazil. Biodiversity and Conservation 11: 1091-1104.
17. CARRANZA, S., BAGUÑÀ, J. and RIUTORT, M. (1997). Are the Platyhelminthes a monophyletic primitive group? An assessment using 18S rDNA sequences. Mol Biol Evol 14: 485-497.
18. CARRANZA, S., LITTLEWOOD, D.T.J., CLOUGH, K.A., RUIZ-TRILLO, I., BAGUÑÀ, J. and RIUTORT, M. (1998). A robust molecular phylogeny of the Tricladida (Platyhelminthes: Seriata) with a discussion on morphological synapomorphies P Roy Soc B-Biol Sci 265: 631-640.
19. CARRANZA, S., BAGUÑÀ, J. and RIUTORT, M. (1999). Origin and Evolution of Paralogous rRNA Gene Clusters Within the Flatworm Family Dugesiidae (Platyhelminthes, Tricladida). J Mol Evol. 49: 250-259.
20. CAVALIER-SMITH, T. (1998). A revised six-kingdom system of life. Biol Rev 73: 203.
21. CHARBAGIBARBIROU, K., ÁLVAREZ-PRESAS, M., VILA, M., GAMMOUDI, M., TEKAYA, S. and RIUTORT, M. (2011). Marine triclads (Platyhelminthes, Tricladida, Maricola). a preliminary molecular approach to their phylogeny. Cah. Biol. Mar. 52: 303-311.
22. DE BEAUCHAMP, P. (1961). Classe des Turbellariés. In Traité de Zoologie (Ed. P. Grassé), Masson et Cie, Paris. pp. 35-212.
23. DE VRIES, E.J. (1984). On the species of the Dugesia gonocephala group (Platyhelminthes, Turbellaria, Tricladida) from Greece. Bijdragen tot de Dierkunde 54: 101-126.
24. DE VRIES, E.J. and SLUYS, R. (1991). Phylogenetic relationships of the genus Dugesia (Platyhelminthes, Tricladida, Paludicola). J Zool (Lond) 223: 103-116.
25. DIESING, K.M. (1850). Systema Helminthum, Vindobonae.
26. DINDAL, D.L. (1970). Feeding behaivor of a terrestrial turbellarian Bipalium adventitium. Am. Midl. Nat. 83: 635-637.
27. DUNN, C.W., HEJNOL, A., MATUS, D.Q., PANG, K., BROWNE, W.E., SMITH, S.A., SEAVER, E., ROUSE, G.W., OBST, M., EDGECOMBE, G.D., SORENSEN, M.V., HADDOCK, S.H.D., SCHMIDT-RHAESA, A., OKUSU, A., KRISTENSEN, R.M., WHEELER, W.C., MARTINDALE, M.Q. and GIRIBET, G. (2008). Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452: 745-749.
28. EHLERS, U. (1985). Das Phylogenetische System der Plathelminthes. G. Fischer. Stuttgart and New York.
29. EHRENBERG, C.G. (1831). Animalia evertebrata exdusis Insectis in Symbolae physicae (Ed. Fredericus Guilelmus Hemprich and Christianus Godofredus Ehrenberg). Symbolae physicae. Volume 4, series prima cum tabularum decade prima. Berolini.
30. FALLENI, A., LUCCHESI, P., GHEZZANI, C., MCDONALD, J.C. and JONES, H.D. (2009). The female gonad in two species of Microplana (Platyhelminthes, Tricladida, Rhynchodemidae): Ultrastructural and cytochemical investigations. J Morphol. 270: 1042-1054.
31. FIELD, K.G., OLSEN, G.J., LANE, D.J., GIOVANNONI, S.J., GHISELIN, M.T., RAFF, E.C., PACE, N.R. and RAFF, R.A. (1988) Molecular phylogeny of the animal kingdom. Science 239: 748-753.
32. GAREY, J.R. (2002). The Lesser-Known Protostome Taxa: An Introduction and a Tribute to Robert P. Higgins. Int. Comp. Biol. 42: 611-618.
33. GEGENBAUR, C. (1859). Grundzuge der vergleichenden Anatomie. W. Engelmann, Leipzig, Germany.
34. GEGENBAUR, C., JEFFREY BELL, F. and RAY LANKESTER, E. (1878). Elements of Comparative Anatomy, MacMillan and Co, London.
35. GIRIBET, G., DISTEL, D.L., POLZ, M., STERRER, W. and WHEELER, W.C. (2000). Triploblastic relationships with emphasis on the acoelomates and the position of Gnathostomulida, Cycliophora, Plathelminthes, and Chaetognatha: a combined approach of 18S rDNA sequences and morphology. Syst Biol 49: 539-62.
36. GRAFF, L.V. (1882). Monographie der Turbellarien. I. Rhabdocoela.
37. HAECKEL, E. (1866). Generelle Morphologie der Organismen. Allgemeine Grundzüge der organischen Formen-Wissenschaft, mecanisch begründet durch die von Charles Darwin reformirte Descendenz-Theorie. 2 vols. Verlag von Georg Reimer, Berlin.
38. HAECKEL, E. (1876). The History of Creation (6th New English Edition 1914). D. Appelton and Company, New York.
39. HALANYCH, K.M. (2004). The new view of animal phylogeny. Annual Review of Ecology, Evolution, and Systematics 35: 229-256.
40. HALLEZ, P. (1894). Catalogue des Rhabdocoelides, Triclades and Polyclades du Nord de la France. 2nd ed. edn, L. Daniel, Lille (France).
41. HASZPRUNAR, G. (1996a). The Mollusca: coelomate turbellarians or mesenchymate annelids? In Origin an Evolutionary Radiation of the Mollusca. (Ed. J. Taylor, Oxford University Press, Oxford, pp. 1-28.
42. HASZPRUNAR, G. (1996b). Plathelminthes and Plathelminthomorpha - paraphyletic taxa. J Zool Syst Evol Res 34: 41-48.
43. HEJNOL, A., OBST, M., STAMATAKIS, A., OTT, M., ROUSE, G.W., EDGECOMBE, G.D., MARTINEZ, P., BAGUÑÀ, J., BAILLY, X., JONDELIUS, U., WIENS, M., MÜLLER, W.E.G., SEAVER, E., WHEELER, W.C., MARTINDALE, M.Q., GIRIBET, G. and DUNN, C.W. (2009). Assessing the root of bilaterian animals with scalable phylogenomic methods. P Roy Soc B-Biol Sci 276: 4261-4270.
44. HYMAN, L.H. (1951). The Invertebrates: Platyhelminthes and Rhynchocoela the acoelomate Bilateria, McGraw-Hill, London and New York.
45. HYMAN, L.H. (1940).The invertebrates: Protozoa through Ctenophora. Vol 1. New York.
46. HYMAN, L.H. (1937). Studies on the morphology, Taxonomy, and distribution of North American Triclad Turbellaria. VIII. Some cave Planarians of the United States. Transactions of the American Microscopical Society 56: 457-477.
47. JONDELIUS, U., RUIZ-TRILLO, I., BAGUÑÀ, J. and RIUTORT, M. (2002). The Nemertodermatida are basal bilaterians and not members of the Platyhelminthes. Zool Scr 31: 201-215.
48. JONES, H.D. and BOAG, B. (1996). The distribution of New Zealand and Australian terrestrial flatworms (Platyhelminthes: Turbellaria: Tricladida:Terricola) in the British Isles the Scotish survey and Megalab worms. J. Nat. Hist. 30: 955-975.
49. KARLING, T.G. (1974). On the anatomy and affinities of the Turbellarian orders. In Biology of the Tureballaria. McGraw-Hill., NewYork: 1-16.
50. KENK, R. (1975). Fresh-water triclads (Turbellaria) of North America. VII. The genus Macrocotyla. Trans Am Microsc Soc 94: 324-339.
51. KENK, R. (1974). Index of the genera and species of the freshwater Triclads (Turbellaria) of the World. Smithsonian Contrib. Zool. 183: 1-90.
52. KENK, R. (1930). Beiträge zum System der Probursalier (Tricladida Paludicola). III. Zool. Anz. 89: 289-302.
53. LAZARO, E.M., SLUYS, R., PALA, M., STOCCHINO, G.A., BAGUÑÀ, J. and RIUTORT, M. (2009). Molecular barcoding and phylogeography of sexual and asexual freshwater planarians of the genus Dugesia in the Western Mediterranean (Platyhelminthes, Tricladida, Dugesiidae). Mol Phylogenet Evol 52: 835-845.
54. LAZARO, E., HARRATH, A.H., STOCCHINO, G., PALA, M., BAGUNA, J. and RIUTORT, M. (2011). Schmidtea mediterranea phylogeography: an old species surviving on a few Mediterranean islands? BMC Evol Biol 11: 274.
55. LITTLEWOOD, D.T.J. and OLSON, P.D. (2001). Small subunit rDNA and the Platyhelminthes: signal, noise and compromise. In The interrelationships of the Platyhelminthes (Ed. D.T.J.a.B. Littlewood R.D.) Taylor and Francis, London, England. pp: 262-278.
56. LITTLEWOOD, D.T.J., ROHDE, K., BRAY, R.A. and HERNIOU, E.A. (1999a). Phylogeny of the Platyhelminthes and the evolution of parasitism. Biol J Linn Soc 68 1-2: 257-287.
57. LITTLEWOOD, D.T.J., ROHDE, K. and CLOUGH, K.A. (1999b). The interrelationships of all major groups of Platyhelminthes: phylogenetic evidence from morphology and molecules. Biol J Linn Soc 66: 75-114.
58. MALLATT, J. and WINCHELL, C.J. (2002). Testing the new animal phylogeny: first use of combined large-subunit and small-subunit rRNA gene sequences to classify the protostomes. Mol Biol Evol 19: 289-301.
59. MALLATT, J., CRAIG, C.W. and YODER, M.J. (2010) Nearly complete rRNA genes assembled from across the metazoan animals: Effects of more taxa, a structure-based alignment, and paired-sites evolutionary models on phylogeny reconstruction. Mol Phylogenet Evol 55: 1-17.
60. MEDINA, M., COLLINS, A.G., SILBERMAN, J.D. and SOGIN, M.L. (2001). Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA. P Natl Acad Sci USA. 98: 9707-12.
61. MITCHELL, R.W. (1968). New species of Sphalloplana (Turbellaria; Paludicola) from the caves of Texas and a reexamination of the genus Speophila and the family Kenkiidae. Ann. Spéléol. 23: 597-620.
62. MÜLLER, O.F. (1776). Zoologiae danicae prodromus, seu Animalium Daniae et Norvegiae indigenarum characteres, nomina, et synonyma imprimis popularium, Havniae.
63. NIELSEN, C. (2010). After all: Xenoturbella is an acoelomorph!. Evol Dev 12: 241-243.
64. NOREN, M. and JONDELIUS, U. (2002). The phylogenetic position of the Prolecithophora (Rhabditophora,?Platyhelminthes?). Zool Scr 31: 403-414.
65. PAPS, J., BAGUÑÀ, J. and RIUTORT, M. (2009a). Bilaterian Phylogeny: A Broad Sampling of 13 Nuclear Genes Provides a New Lophotrochozoa Phylogeny and Supports a Paraphyletic Basal Acoelomorpha. Mol Biol Evol 26: 2397-2406.
66. PAPS, J., BAGUÑÀ, J. and RIUTORT, M. (2009b). Lophotrochozoa internal phylogeny: new insights from an up-to-date analysis of nuclear ribosomal genes. P Roy Soc B-Biol Sci 276: 1245-1254.
67. PHILIPPE, H., BRINKMANN, H., COPLEY, R.R., MOROZ, L.L., NAKANO, H., POUSTKA, A.J., WALLBERG, A., PETERSON, K.J. and TELFORD, M.J. (2011). Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 470: 255-258.
68. REYNOLDSON, T.B. and BELLAMY, L.S. (1970). The status of Dugesia lugubris and D. polychroa (Turbellaria, Tricladida) in Britain. J Zool Lond. 162: 157-177.
69. RIUTORT, M., FIELD, K.G., TURBEVILLE, J.M., RAFF, R.R. and BAGUÑÀ, J. (1992) Enzyme electrophoresis, 18S rRNA sequences, and levels of phylogenetic resolution among several species of freshwater planarians (Platyhelminthes, Tricladida, Paludicola). Can. J. Zool 70: 1425-1439.
70. ROHDE, K. (1990) Phylogeny of platyhelminthes, with special reference to parasitic groups. Int J Parasito.l 20: 979-1007.
71. RUIZ-TRILLO, I., PAPS, J., LOUKOTA, M., RIBERA, C., JONDELIUS, U., BAGUÑÀ, J. and RIUTORT, M. (2002). A phylogenetic analysis of myosin heavy chain type II sequences corroborates that Acoela and Nemertodermatida are basal bilaterians. P Natl Acad Sci USA. 99: 11246-51.
72. RUIZTRILLO, I., RIUTORT, M., LITTLEWOOD, D.T.J., HERNIOU, E.A. and BAGUÑÀ, J. (1999). Acoel flatworms: earliest extant bilaterian Metazoans, not members of Platyhelminthes. Science 283: 1919-23.
73. RUPPERT, E.E., FOX, R. and BARNES, R.D. (2003). Invertebrate Zoology: A Functional Evolutionary Approach. Seventh Edition, Brooks/Cole Thompson Learning, Belmont, California.
74. SLUYS, R. (2001). Towards a phylogenetic classification and characterization of dugesiid genera (Platyhelminthes, Tricladida, Dugesiidae): a morphological perspective. In The interrelationships of the Platyhelminthes (Ed. D.T.J.a.B. Littlewood R.D.) Taylor and Francis, London, England. pp: 57-73.
75. SLUYS, R. (1999). Global diversity of land planarians (Platyhelminthes, Tricladida, Terricola): a new indicator-taxon in Biodivers Conserv studies. Biodivers Conserv 8: 1663-1681.
76. SLUYS, R. (1990). A monograph of the Dimarcusidae (Platyhelminthes, Seriata, Tricladida). Zool Scr 19: 13-29.
77. SLUYS, R. (1989a). A monograph of the marine triclads. A. A. Balkema, Rotterdam.
78. SLUYS, R. (1989b). Phylogenetic relationships of the triclads (Platyhelminthes, Seriata, Tricladida). Bijdr. Dierkd. 59: 3-25.
79. SLUYS, R., GRANT, L. and BLAIR, D. (2007). Freshwater planarians from artesian springs in Queensland, Australia (Platyhelminthes, Tricladida, Paludicola). Contrib Zool 76: 9-19.
80. SLUYS, R. and KAWAKATSU, M. (2006). Towards a phylogenetic classification of dendrocoelid freshwater planarians (Platyhelminthes): a morphological and eclectic approach. 44: 274-284.
81. SLUYS, R., KAWAKATSU, M., RIUTORT, M. and BAGUÑÀ, J. (2009) A new higher classification of planarian flatworms (Platyhelminthes, Tricladida). J Nat Hist 43 29-30: 1763-1777.
82. SLUYS, R., KAWAKATSU, M. and WINSOR, L. (1998). The genus Dugesia in Australia, with its phylogenetic analysis and historical biogeography (Platyhelminthes, Tricladida, Dugesiidae). Zool Scr 27: 273-290.
83. SMITH J.P.S., TYLER S., RIEGER R.M. (1986). Is the Turbellaria polyphyletic?. Hydrobiologia 132: 13-21.
84. SOPOTT-EHLERS, B. (1985). The phylogenetic relationships within the Seriata (Platyhelminthes). In The origins and relationships of lower invertebrates. (Eds. S. Conway-Morris, J.D. George, R. Gibson and H.M. Platt) Clarendon Press, Oxford: 159-167.
85. SPERLING, E.A., PETERSON, K.J. and PISANI, D. (2009). Phylogenetic-Signal Dissection of Nuclear Housekeeping Genes Supports the Paraphyly of Sponges and the Monophyly of Eumetazoa. Mol Biol Evol 26: 2261-2274.
86. STEINBÖCK, O. (1925). Zur Systematik der Turbellaria metamerata, zugleich ein Beitrag zur Morphologie des Tricladen-Nervensystems. Zool. Anz. 64: 165-192.
87. SUGIURA, S. and YAMAMURA, Y. (2009). Potential impacts of the invasive flatworm Platydemus manokwari on arboreal snails. Biol.Invasions 11: 737-742.
88. SUNNUCKS, P., BLACKET, M.J., TAYLOR, J.M., SANDS, C.J., CIAVAGLIA, S.A., GARRICK, R.C., TAIT, N.N., ROWELL, D.M. and PAVLOVA, A. (2006). A tale of two flatties: different responses of two terrestrial flatworms to past environmental climatic fluctuations at Tallaganda in montane southeastern Australia. 15: 4513-4531.
89. TELFORD, M.J., LOCKYER, A.E., CARTWRIGHT-FINCH, C. and LITTLEWOOD, D.T.J. (2003). Combined large and small subunit ribosomal RNA phylogenies support a basal position of the acoelomorph flatworms. P Roy Soc B-Biol Sci 270: 1077-83.
90. TURBEVILLE, J.M. (2002). Progress in Nemertean Biology: Development and Phylogeny. Integrative and Comparative Biology 42: 692-703.
91. VALENTINE, J.W. (2004). On the Origin of Phyla. University Of Chicago Press.
92. WINSOR, L., JOHNS, P.M. and YEATES, G.W. (1998). Introduction, and ecological and systematic background, to the Terricola (Tricladida). Pedobiologia 42: 389-404.