A Comprehensive Molecular Phylogeny of Dalytyphloplanida (Platyhelminthes: Rhabdocoela) Reveals Multiple Escapes from the Marine Environment and Origins of Symbiotic Relationships

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Van Steenkiste, Niels ^a,e   Tessens, Bart ^a   Willems, Wim ^a   Backeljau, Thierry ^b,c   Jondelius, Ulf ^d   Artois, Tom ^a  

^a HASSELT UNIVERSITY   (Belgium)

^b UNIVERSITY OF ANTWERP   (Belgium)

^c ROYAL BELGIAN INSTITUTE OF NATURAL SCIENCES   (Belgium)

^d SWEDISH MUSEUM OF NATURAL HISTORY   (Sweden)

^e PACIFIC BIOLOGICAL STATION   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

28S RIBOSOME DNA; DNA 18S; RIBOSOME DNA; UNCLASSIFIED DRUG;

ARTICLE; CLADISTICS; CONTROLLED STUDY; DALYELLIIDAE; DALYTYPHLOPLANIDA; DNA SEQUENCE; FRESHWATER ENVIRONMENT; HELMINTH; MARINE ENVIRONMENT; MOLECULAR PHYLOGENY; NONHUMAN; PLATYHELMINTH; SPECIES DIVERSITY; SPECIES HABITAT; SPECIES INVASION; SYMBIOSIS; TEMNOCEPHALIDA; TYPHLOPLANIDAE;

ANIMALS; ENVIRONMENT; EVOLUTION, MOLECULAR; FEMALE; MALE; PHYLOGENY; PLATYHELMINTHS; RNA, RIBOSOMAL, 18S; RNA, RIBOSOMAL, 28S; SYMBIOSIS;

DALYELLIIDAE; PLATYHELMINTHES; RHABDOCOELA; TEMNOCEPHALIDA; TYPHLOPLANIDAE; TYPHLOPLANOIDA;

EID: 84875410333     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059917     Document Type: Article

References (82)

1. Willems WR, Wallberg A, Jondelius U, Littlewood DTJ, Backeljau T, et al. (2006) Filling a gap in the phylogeny of flatworms: relationships within the Rhabdocoela (Platyhelminthes), inferred from 18S ribosomal DNA sequences. Zool Scr 35: 1-17.
2. Jondelius U, Thollesson M, (1993) Phylogeny of the Rhabdocoela (Platyhelminthes): a working hypothesis. Can J Zool 71: 298-308.
3. Willems WR (2005) The phylogeny of the 'Typhloplanoida' (Platyhelminthes) inferred from 18S ribosomal DNA sequences. Ph.D. Dissertation, Limburgs Universitair Centrum, Diepenbeek, 67 p. + 7 appendices.
4. Schockaert ER, Hooge M, Sluys R, Schilling S, Tyler S, et al. (2008) Global diversity of free-living flatworms (Platyhelminthes, "Turbellaria") in freshwater. Hydrobiologia 595: 41-48.
5. Schockaert ER (1996) Turbellarians. In: Hall GS, editor. Methods for the examination of organismal diversity in soils and sediments. Wallinford: CAB International. pp. 221-226.
6. Townshend JL, (1963) A modification and evaluation of the apparatus for the Oostenbrink direct cottonwool filter extraction method. Nematologica 9: 106-110.
7. Littlewood DTJ, Rohde K, Clough KA, (1999a) The interrelationships of all major groups of Platyhelminthes: phylogenetic evidence from morphology and molecules. Biol J Linn Soc Lond 66: 75-114.
8. Littlewood DTJ, Rohde K, Bray RA, Herniou EA, (1999b) Phylogeny of the Platyhelminthes and the evolution of parasitism. Biol J Linn Soc Lond 68: 257-287.
9. Norén M, Jondelius U, (2002) The phylogenetic position of the Prolecithophora (Rhabditophora, 'Platyhelminthes'). Zool Scr 31: 403-414.
10. Littlewood DTJ, Curini-Galletti M, Herniou EA, (2000) The interrelationships of Proseriata (Platyhelminthes: Serata) tested with molecules and morphology. Mol Phylogenet Evol 16: 449-466.
11. Staden R, (1996) The Staden sequence analysis package. Mol Biotechnol 5: 233-241.
12. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
13. Katoh K, Toh H, (2008a) Improved accuracy of multiple ncRNA alignment by incorporating structural information into MAFFT-based framework. BMC Bioinformatics 9: 212.
14. Katoh K, Toh H, (2008b) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9: 286-298.
15. Misof B, Misof K, (2009) A Monte Carlo approach successfully identifies randomness in multiple sequence alignments: a more objective means of data exclusion. Syst Biol 58: 21-34.
16. Xia X, Lemey P (2009) Assessing substitution saturation with DAMBE. In: Lemey P, Salemi M, Vandamme A-M, editors. The phylogenetic handbook: a practical approach to DNA and protein phylogeny, 2nd edition. Cambridge University Press. pp. 615-630.
17. Posada D, (2008) jModeltest: phylogenetic model averaging. Mol Biol Evol 25: 1253-1256.
18. Stamatakis A (2006) Phylogenetic models of rate heterogeneity: A high performance computing perspective. Proceedings of 20th IEEE/ACM International parallel and distributed processing symposium, High performance computational biology workshop (Proceedings on CD. Rhodos, Greece 2006.
19. Stamatakis A, (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
20. Sukumaran J, Holder MT, (2010) DendroPy: A Python library for phylogenetic computing. Bioinformatics 26: 1569-1571.
21. Ronquist F, Huelsenbeck JP, (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
22. Kumar S, Skjæveland Å, Orr RJS, Enger P, Ruden T, et al. (2009) AIR: A batch-oriented web program package for construction of supermatrices ready for phylogenomic analyses. BMC Bioinformatics 10: 357.
23. Rambaut A (2009) Figtree v1.3.1. Available: http://tree.bio.ed.ac.uk. Accessed 2011 Aug.
24. Alfaro ME, Zoller S, Lutzoni F, (2003) Bayes or bootstrap? A simulation study comparing the performance of Bayesian Markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Mol Biol Evol 20: 255-266.
25. Shimodaira H, (2002) An approximately unbiased test of phylogenetic tree selection. Syst Biol 51: 492-508.
26. Schmidt HA, Strimmer K, Vingron M, von Haeseler A, (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502-504.
27. Shimodaira H, Hasegawa M, (2001) CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17: 1246-1247.
28. Pagel M, Meade A, Barker D, (2004) Bayesian estimation of ancestral character states on phylogenies. Syst Biol 53: 673-684.
29. Rambaut A, Drummond AJ (2009) Tracer v1.5. Available: http://tree.bio.ed.ac.uk. Accessed 2011 Aug.
30. Barbeitos MS, Romano SL, Lasker HR, (2010) Repeated loss of coloniality and symbiosis in scleractinian corals. Proc Natl Acad Sci USA 107: 11877-11882.
31. Nylander JAA (2011) Burntrees v0.1.9. Perl script for manipulating MrBayes trees and parameter files. Available: http://www.abc.se/~nylander/. Accessed 2012 Mar.
32. Bollback JP, (2006) SIMMAP: Stochastic character mapping of discrete traits on phylogenies. BMC Bioinformatics 7: 88.
33. Schultz TR, Churchill GA, (1999) The role of subjectivity in reconstructing ancestral character states: a Bayesian approach to unknown rates, states and transformation asymmetries. Syst Biol 48: 651-664.
34. Salisbury BA, Kim J, (2001) Ancestral state estimation and taxon sampling density. Syst Biol 50: 557-564.
35. Zamparo D, Brooks DR, Hoberg EP, McLennan DA, (2001) Phylogenetic analysis of the Rhabdocoela (Platyhelminthes) with emphasis on the Neodermata and relatives. Zool Scr 30: 59-77.
36. Van Steenkiste N, Davison P, Artois T, (2010) Bryoplana xerophila n. g. n. sp., a new limnoterrestrial microturbellarian (Platyhelminthes, Typhloplanidae, Protoplanellinae) from epilithic mosses, with notes on its ecology. Zoolog Sci 27: 285-291.
37. Luther A, (1955) Die Dalyelliiden (Turbellaria, Neorhabdocoela). Eine Monographie. Acta Zool Fenn 87: 1-337.
38. Therriault TW, Kolasa J, (1999) New species and records of microturbellarians from coastal rock pools of Jamaica, West Indies. Archiv fur Hydrobiol 144: 371-381.
39. Ax P (2008) Plathelminthes aus Brackgewässern der Nordhalbkugel. Mainz: Akademie der Wissenschaften und der Literatur, Abhandlungen der Mathematisch-Naturwissenschaftlichen Klasse, Jhrg. 2008, Nr. 1. 696 p.
40. Karling TG, (1974) Turbellarian fauna of the Baltic proper: identification, ecology and biogeography. Fauna Fenn 27: 1-101.
41. Kolasa J, (1977) Remarks on the marine-originated Turbellaria in the freshwater fauna. Acta Zool Fenn 154: 82-87.
42. Findenegg I, (1930) Untersuchungen an einigen Arten der Familie Typhloplanidae. Zool Jahrb Abt Syst Geograph Biol Tiere 59: 73-130.
43. Ax P, (1952) Bresslauilla relicta Reisinger, ein holeuryhalines Turbellar des Meer- und Süβwassers. Faun Mitt Norddeutschl I: 18.
44. Ax P, (1957) Die Einwanderung mariner Elemente der Mikrofauna in das limnische Mesopsammal der Elbe. Verhandl Deutsch Zool Ges 1956: 428-435.
45. Rixen J-U, (1961) Kleinturbellarien aus dem Litoral der Binnengewässer Schleswig-Holsteins. Archiv fur Hydrobiol 57: 464-539.
46. Rohde K, (1997) The origins of parasitism in the Platyhelminthes: a summary interpreted on the basis of recent literature. Int J Parasitol 27: 739-746.
47. Iomini C, Ferraguti M, Justine J-L, (1999) Ultrastructure of glands in a scutariellid (Platyhelminthes) and possible phylogenetic implications. Folia Parasitol 46: 199-203.
48. Karling TG, (1956) Alexlutheria acrosiphoniae n. gen., n. sp., ein bemerkenswerter mariner Vertreter der Familie Dalyelliidae (Turbellaria). Ark Zool 10: 331-345.
49. Ehlers U (1985) Das phylogenetische System der Plathelminthes. Stuttgart: Gustav Fischer Verlag. 317 p.
50. Ehlers U, Sopott-Ehlers B, (1993) The caudal duo-gland adhesive system of Jensenia angulata (Plathelminthes, Dalyelliidae): ultrastructure and phylogenetic significance (With comments on the phylogenetic position of the Temnocephalida and the polyphyly of the Cercomeria). Microfauna Mar 8: 65-76.
51. Joffe BI, Cannon LRG, Schockaert ER, (1998) On the phylogeny of families and genera within the Temnocephalida. Hydrobiologia 383: 263-268.
52. Damborenea MC, Cannon LRG, (2001) The mosaic of the epidermal syncytia in Didymorchis sp. (Didymorchidae, Temnocephalida) from South America. Belg J Zool 31: 167-171.
53. Watson NA (2001) Insights from comparative spermatology in the 'turbellarian' Rhabdocoela. In: Littlewood DTJ, Bray RA, editors. Interrelationships of the Platyhelminthes. London: Taylor and Francis. pp. 217-230.
54. Cannon LRG (1986) The Pterastericolidae: Parasitic Turbellarians from Starfish. In: Cremin C, Dobson C, Moorehouse DE, editors. Parasite Lives. St. Lucia: University of Queensland Press. pp. 15-32.
55. Jondelius U, (1992a) New Pterastericola species (Platyhelminthes, Rhabdocoela) and a cladistic analysis of the Pterastericolidae. Zool Scr 21: 93-101.
56. Jondelius U, (1992b) Sperm morphology in the Pterastericolidae (Platyhelminthes, Rhabdocoela): phylogenetic implications. Zool Scr 21: 223-230.
57. Rohde K, Hefford C, Ellis JT, Baverstock PR, Johnson AM, et al. (1993) Contributions to the phylogeny of Platyhelminthes based on partial sequencing of 18S ribosomal DNA. Int J Parasitol 23: 705-724.
58. Watson NA, Rohde K, Jondelius U, (1993) Ultrastructure of sperm and spermiogenesis of Pterastericola astropectinis (Platyhelminthes, Rhabdocoela, Pterastericolidae). Parasitol Res 79: 322-328.
59. Jennings JB, Phillips JI, (1978) Feeding and digestion in three entosymbiotic graffillid rhabdocoels from bivalve and gastropod molluscs. Biol Bull 155: 542-562.
60. Jennings JB, (1997) Nutritional and respiratory pathways to parasitism exemplified in the Turbellaria. Int J Parasitol 27: 679-691.
61. Cannon LRG, (1982) Endosymbiotic Umagillids (Turbellaria) from Holothurians of the Great Barrier Reef. Zool Scr 11: 173-188.
62. Doignon G, Artois T, (2006) Annotated checklist of the umagillid turbellarians infesting echinoids (Echinodermata). Belg J Zool 136: 101-106.
63. Ehlers U, (1972) Systematisch-phylogenetische Untersuchungen an der Familie Solenopharyngidae (Turbellaria, Neorhabdocoela). Mikrofauna Meeresb 11: 3-78.
64. Sopott-Ehlers B, Ehlers U, (1995) Modified sperm ultrastructure and some data on spermiogenesis in Provortex tubiferus (Plathelminthes, Rhabdocoela): phylogenetic implications for the Dalyellioida. Zoomorphology 115: 41-49.
65. Jondelius U, (1997) A new family and three new species of flatworms (Platyhelminthes) from the Darwin harbour area. In: Proceedings of the Sixth International Marine Biological Workshop. The marine flora and fauna of Darwin Harbour, Northern Territory, Australia Hanley RH, Caswell G, Megirian D, Larson HK, editors. Darwin: Museum and Art Galleries of the Northern Territory and the Australian Marine Sciences Association 1997. pp. pp.187-197.
66. Meixner J, (1926) Beitrag zur Morphologie und zum System der Turbellaria-Rhabdocoela: II. Über Typhlorhynchus nanus Laidlaw und die parasitischen Rhabdocölen nebst Nachträgen zu den Calyptorhynchia. Z Morph Okol Tiere 5: 577-624.
67. Meixner J (1938) Turbellaria (Strudelwürmer) Turbellaria I. Allgemeiner Teil. In: Grimpe G, Wagler E, editors. Die Tierwelt der Nordiska- und Ostsee 33 (4b). Leipzig: Akademische Verlaggesellschaft. pp. 1-146.
68. Marcus E, (1954) Turbellaria Brasileiros XI. Pap Avuls Zool Sec Agr Sao Paulo XI pp. 419-489.
69. Beklemischew VN, (1927) Über die Turbellarienfauna des Aralsees. Zugleich ein Beitrag zur Morphologie und zum System der Dalyelliida. Zool Jahrb Abt Syst Geograph Biol Tiere 54: 87-138.
70. Karling TG, (1986) Free-living marine Rhabdocoela (Platyhelminthes) from the N. American Pacific coast. With remarks on species from other areas. Zool Scr 15: 201-219.
71. Luther A, (1962) Die Turbellarien Ostfennoskandiens. III. Neorhabdocoela 1. Dalyellioida, Typhloplanoida: Byrsophlebidae und Trigonostomidae. Fauna Fenn 12: 1-71.
72. Luther A, (1948) Untersuchungen an Rhabdocoelen Turbellarien-VII. Über einige marine Dalyellioida-VIII. Beiträge zur Kenntnis der Typhloplanoida. Acta Zool Fenn 55: 3-122.
73. Karling TG, Mack-Fira V, Dörjes J, (1972) First report on marine microturbellarians from Hawaii. Zool Scr 1: 251-269.
74. Ehlers U, Ehlers B, (1981) Interstitielle Fauna von Galapagos-XXVII. Byrsophlebidae, Promesostomidae Brinkmanniellinae, Kytorhynchidae (Turbellaria, Typhloplanoida). Mikrofauna Meeresb 83: 1-35.
75. Rieger MR (1974) A new group of Turbellaria-Typhloplanoida with a proboscis and its relationship to Kalyptorhynchia. In: Riser NW, Morse MP, editors. Biology of the Turbellaria. Libbie H Hyman Memorial Volume. New York: Mc-Graw-Hill Company. pp. 23-62.
76. Luther A, (1946) Untersuchungen an Rhabdocoelen Turbellarien-V. Über einige Typhloplaniden. Acta Zool Fenn 46: 3-56.
77. Willems WR, Artois TJ, Vermin W, Backeljau T, Schockaert ER, (2005) Typhloplanoida (Platyhelminthes, Rhabdocoela) from New Caledonia and eastern Australia, with the description of six new taxa. N Z J Zool 32: 79-98.
78. Ax P, (1960) Turbellarien aus salzdurchtränkten Wiesenböden der deutschen Meeresküsten. Z Wiss Zool 163: 210-235.
79. Ehlers U, Sopott-Ehlers B, (1989) Interstitielle Fauna von Galapagos. XXXVIII. Haloplanella Luther und Pratoplana Ax (Typhloplanoida, Plathelminthes). Microfauna Mar 5: 189-206.
80. Hochberg R, Cannon LRG, (2002) Two new freshwater rhabdocoels, Austrodalyellia gen. nov. and Haplodidymos gen. nov. (Platyhelminthes), from Queensland, Australia. Zootaxa 44: 1-15.
81. Hochberg R, Cannon LRG, (2003) Magnetia queenslandica, a new genus and new species of typhloplanid flatworm (Platyhelminthes: Rhabdocoela) from Magnetic Island. Raffles Bull Zool 51: 1-6.
82. Norén M, Jondelius U, (1999) Phylogeny of the Prolecithophora (Platyhelminthes) inferred from 18S rDNA sequences. Cladistics 15: 103-112.