Exploring the potential of small RNA subunit and ITS sequences for resolving phylogenetic relationships within the phylum Ctenophora

Zoology

Volumn 118, Issue 2, 2015, Pages 102-114

  Simion, Paul ^a   Bekkouche, Nicolas ^a,b   Jager, Muriel ^a   Quéinnec, Eric ^a   Manuel, Michaël ^a  

^a Département de Biologie   (France)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

18S rRNA; Ctenophora; Doublet model; ITS

Indexed keywords

RIBOSOMAL SPACER DNA; RIBOSOME DNA;

ANIMAL; CLASSIFICATION; CTENOPHORA; GENETICS; MOLECULAR GENETICS; PHYLOGENY;

ANIMALS; CTENOPHORA; DNA, RIBOSOMAL; DNA, RIBOSOMAL SPACER; MOLECULAR SEQUENCE DATA; PHYLOGENY;

EID: 84930725645     PISSN: 09442006     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.zool.2014.06.004     Document Type: Article

References (79)

1. Abouheif E., Zardoya R., Meyer A. 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. 1998, 47:394-405.
2. Alié A., Leclère L., Jager M., Dayraud C., Chang P., Le Guyader H., Quéinnec E., Manuel M. Somatic stem cells express Piwi and Vasa genes in an adult ctenophore: ancient association of germline genes with stemness. Dev. Biol. 2011, 350:183-197.
3. Borchiellini C., Manuel M., Alivon E., Boury-Esnault N., Vacelet J., Le Parco Y. Sponge paraphyly and the origin of Metazoa. J. Evol. Biol. 2001, 14:171-179.
4. Borisenko I., Ereskovsky A.V. Tentacular apparatus ultrastructure in the larva of Bolinopsis infundibulum (Lobata: Ctenophora): tentacular apparatus ultrastructure in Ctenophora. Acta Zool. 2013, 94:193-202.
5. Carré C., Carré D. Haeckelia bimaculata sp. nov., une nouvelle espéce méditerranéenne de cténophore (Cyddipida Haeckeliidae) pourvue de cnidocystes et de pseudocolloblastes. Comptes Rendus Acad. Sci. 1989, 308(Series III):321-327.
6. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 2000, 17:540-552.
7. Cavalier-Smith T., Allsopp M., Chao E.E., Boury-Esnault N., Vacelet J. Sponge phylogeny, animal monophyly, and the origin of the nervous system: 18S rRNA evidence. Can. J. Zool. 1996, 74:2031-2045.
8. Chow S., Ueno Y., Toyokawa M., Oohara I., Takeyama H. Preliminary analysis of length and GC content variation in the ribosomal first internal transcribed spacer (ITS1) of marine animals. Mar. Biotechnol. 2008, 11:301-306.
9. Chun C. Die Ctenophoren des Golfes von Neapel und der angrenzenden Meeres-Abschnitte: eine Monographie 1880, W. Engelmann, Leipzig.
10. Collins A.G. Evaluating multiple alternative hypotheses for the origin of Bilateria: an analysis of 18S rRNA molecular evidence. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:15458-15463.
11. Collins A.G. Phylogeny of Medusozoa and the evolution of cnidarian life cycles. J. Evol. Biol. 2002, 15:418-432.
12. Collins A.G., Schuchert P., Marques A.C., Jankowski T., Medina M., Schierwater B. Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models. Syst. Biol. 2006, 55:97-115.
13. Costello J.H., Bayha K.M., Mianzan H.W., Shiganova T.A., Purcell J.E. Transitions of Mnemiopsis leidyi (Ctenophora: Lobata) from a native to an exotic species: a review. Hydrobiologia 2012, 690:21-46.
14. Darriba D., Taboada G.L., Doallo R., Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Method 2012, 9:772. 10.1038/nmeth.2109.
15. Dayraud C., Alié A., Jager M., Chang P., Le Guyader H., Manuel M., Quéinnec E. Independent specialisation of myosin II paralogues in muscle vs. non-muscle functions during early animal evolution: a ctenophore perspective. BMC Evol. Biol. 2012, 12:107. 10.1186/1471-2148-12-107.
16. Dohrmann M., Wörheide G. Novel scenarios of early animal evolution - is it time to rewrite textbooks?. Integr. Comp. Biol. 2013, 53:503-511.
17. Doyle J.J., Doyle J.L. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 1987, 19:11-15.
18. 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., Sørensen M.V., Haddock S.H.D., Schmidt-Rhaesa A., Okusu A., Kristensen R.M., Wheeler W.C., Martindale M.Q., Giribet G. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 2008, 452:745-749.
19. Erpenbeck D., Nichols S.A., Voigt O., Dohrmann M., Degnan B.M., Hooper J.N.A., Wörheide G. Phylogenetic analyses under secondary structure-specific substitution models outperform traditional approaches: case studies with diploblast LSU. J. Mol. Evol. 2007, 64:543-557.
20. Ghada B., Ahmed B.A., Messaoud M., Amel S.-H. Genetic diversity and molecular evolution of the internal transcribed spacer (ITSs) of nuclear ribosomal DNA in the Tunisian fig cultivars (Ficus carica L.; Moracea). Biochem. Syst. Ecol. 2013, 48:20-33.
21. Gillespie J.J., Yoder M.J., Wharton R.A. Predicted secondary structure for 28S and 18S rRNA from Ichneumonoidea (Insecta: Hymenoptera: Apocrita): impact on sequence alignment and phylogeny estimation. J. Mol. Evol. 2005, 61:114-137.
22. Glenner H., Hansen A.J., Sørensen M.V., Ronquist F., Huelsenbeck J.P., Willerslev E. Bayesian inference of the metazoan phylogeny: a combined molecular and morphological approach. Curr. Biol 2004, 14:1644-1649.
23. Granhag L., Majaneva S., Møller L. First recordings of the ctenophore Euplokamis sp. (Ctenophora, Cydippida) in Swedish coastal waters and molecular identification of this genus. Aquat. Inv. 2012, 7:455-463.
24. Halanych K.M. The new view of animal phylogeny. Ann. Rev. Ecol. Evol. Syst. 2004, 35:229-256.
25. Harbison G.R. On the classification and evolution of the Ctenophora. The Origins and Relationships of Lower Invertebrates 1985, 78-100. Oxford University Press, Oxford. S.C. Morris, J.D. George, R. Gibson, H.M. Platt (Eds.).
26. Hejnol A., Obst M., Stamatakis A., Ott M., Rouse G.W., Edgecombe G.D., Martinez P., Baguna J., Bailly X., Jondelius U., Wiens M., Muller W.E.G., Seaver E., Wheeler W.C., Martindale M.Q., Giribet G., Dunn C.W. Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc. R. Soc. B 2009, 276:4261-4270.
27. Hernandez-Nicaise M.L., Franc J.M. Embranchement des Cténaires. Traité de Zoologie 1994, 943-1075. Masson et Cie, Paris. P.P. Grassé (Ed.).
28. Huelsenbeck J.P., Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755.
29. Hyman L.H. Ctenophora. The Invertebrates: Protozoa Through Ctenophora 1940, 662-696. McGraw Hill, New York. L.H. Hyman (Ed.).
30. Jager M., Quéinnec E., Chiori R., Le Guyader H., Manuel M. Insights into the early evolution of SOX genes from expression analyses in a ctenophore. J. Exp. Zool. B: Mol. Dev. Evol. 2008, 310B:650-667.
31. Jager M., Chiori R., Alié A., Dayraud C., Quéinnec E., Manuel M. New insights on ctenophore neural anatomy: immunofluorescence study in Pleurobrachia pileus (Müller, 1776). J. Exp. Zool. B: Mol. Dev. Evol. 2011, 316B:171-187.
32. Kjer K.M. Use of rRNA secondary structure in phylogenetic studies to identify homologous positions: an example of alignment and data presentation from the frogs. Mol. Phyl. Evol. 1995, 4:314-330.
33. Kohn A.B., Citarella M.R., Kocot K.M., Bobkova Y.V., Halanych K.M., Moroz L.L. Rapid evolution of the compact and unusual mitochondrial genome in the ctenophore, Pleurobrachia bachei. Mol. Phyl. Evol. 2012, 63:203-207.
34. Komai, T., 1922. Studies on two aberrant ctenophores. In: Coeloplana and Gastrodes. Published by the author, Kyoto, Japan.
35. Komai T. On the structure of Ctenoplana. Kyoto Univ. Col. Sci. Mem., B 1934, 9:245-256.
36. Lang A. Die Polycladen (Seeplanarien) des Golfes von Neapel und der angrenzenden Meeresabschnitte: Eine Monographie 1884, W. Engelmann, Leipzig.
37. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
38. Lartillot N., Philippe H. CAT: un modèle phylogénétique Bayésien permettant de prendre en compte l'hétérogénéité des processus de substitution entre sites dans les alignements protéiques. Biosystema 2004, 22:97-104.
39. Lucic D., Pestoric B., Malej A., Lopez-Lopez L., Drakulovic D., Onofri V., Miloslavic M., Gangai B., Onofri I., Benovic A. Mass occurrence of the ctenophore Bolinopsis vitrea (L. Agassiz, 1860) in the nearshore southern Adriatic Sea (Kotor Bay, Montenegro). Environ. Monit. Assess. 2011, 184:4777-4785.
40. Maddison W.P., Maddison D.R. Mesquite: A Modular System for Evolutionary Analysis. Version 2.73 2010, http://mesquiteproject.org/.
41. Madin L.P., Harbison G.R. Thalassocalyce inconstans, new genus and species, an enigmatic ctenophore representing a new family and order. Bull. Mar. Sci. 1978, 28:680-687.
42. Mallatt J., Craig C.W., Yoder M.J. 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. Phyl. Evol. 2010, 55:1-17.
43. Manuel M. Early evolution of symmetry and polarity in metazoan body plans. C. R. Biol. 2009, 332:184-209.
44. 2+ regulated photoprotein: recombinant calcium-regulated photoprotein berovin. FEBS J. 2012, 279:856-870.
45. Martindale M.Q., Henry J.Q. Intracellular fate mapping in a basal metazoan, the ctenophore Mnemiopsis leidyi, reveals the origins of mesoderm and the existence of indeterminate cell lineages. Dev. Biol. 1999, 214:243-257.
46. Matsumoto G.I. Coeloplana thomsoni sp. nov., a new benthic ctenophore (Ctenophora: Platyctenida: Coeloplanidae) from Western Australia. The Seagrass Flora and Fauna of Rottnest Island, Western Australia 1999, 385-393. Western Australian Museum, Perth. D.J. Walker, F.E. Wells (Eds.).
47. Maxmen A. Comb jelly genetics suggest a radical redrawing of the tree of life. Sci. News 2013, 183:20.
48. Medlin L., Elwood H.J., Stickel S., Sogin M.L. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 1988, 71:491-499.
49. Mills C.E. Revised classification of the genus Euplokamis Chun, 1880 (Ctenophora: Cydippida: Euplokamidae n. fam.) with a description of the new species Euplokamis dunlapae. Can. J. Zool. 1987, 65:2661-2668.
50. Mills C.E. Phylum Ctenophora: list of all valid species names 2012, Electronic internet document available at http://faculty.washington.edu/cemills/Ctenolist.html. Published by the author, web page established March 1998. Last updated 15.05.12.
51. Mortensen T. The Danish ingolf-expedition. Ctenophora 1912, vol. V. Bianco Luno, Kopenhagen.
52. Nosenko T., Schreiber F., Adamska M., Adamski M., Eitel M., Hammel J., Maldonado M., Müller W.E.G., Nickel M., Schierwater B., Vacelet J., Wiens M., Wörheide G. Deep metazoan phylogeny: when different genes tell different stories. Mol. Phyl. Evol. 2013, 67:223-233.
53. Oliveira O.M.P., Mianzan H., Migotto A.E., Marques A.C. Chave de identificação dos Ctenophora da costa brasileira. Biota Neotrop. 2007, 7:341-350.
54. Ospovat M.F. On phylogeny and classification of the type Ctenophora. Zool. žurnal 1985, 647:965-974.
55. Pang K., Martindale M.Q. Ctenophores. Curr. Biol. 2008, 18:R1119-R1120.
56. Pang K., Martindale M.Q. Developmental expression of homeobox genes in the ctenophore Mnemiopsis leidyi. Dev. Genes Evol. 2008, 218:307-319.
57. Pang K., Ryan J.F., Baxevanis A.D., Martindale M.Q. Evolution of the TGF-β signaling pathway and its potential role in the ctenophore, Mnemiopsis leidyi. PLoS ONE 2011, 6:e24152. 10.1371/journal.pone.0024152.
58. Pennisi E. Nervous system may have evolved twice. Science 2013, 339:391.
59. Peterson K.J., Eernisse D.J. Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences. Evol. Dev. 2001, 3:170-205.
60. Pett W., Ryan J.F., Pang K., Mullikin J.C., Martindale M.Q., Baxevanis A.D., Lavrov D.V. Extreme mitochondrial evolution in the ctenophore Mnemiopsis leidyi: insight from mtDNA and the nuclear genome. Mitochondrial DNA 2011, 22:130-142.
61. Philippe H., Roure B. Difficult phylogenetic questions: more data, maybe; better methods, certainly. BMC Biol. 2011, 9:91. 10.1186/1741-7007-9-91.
62. Philippe H., Telford M.J. Large-scale sequencing and the new animal phylogeny. Trends Ecol. Evol. 2006, 21:614-620.
63. Philippe H., Derelle R., Lopez P., Pick K., Borchiellini C., Boury-Esnault N., Vacelet J., Renard E., Houliston E., Quéinnec E., Da Silva C., Wincker P., Le Guyader H., Leys S., Jackson D.J., Schreiber F., Erpenbeck D., Morgenstern B., Wörheide G., Manuel M. Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 2009, 19:706-712.
64. Philippe H., Brinkmann H., Lavrov D.V., Littlewood D.T.J., Manuel M., Wörheide G., Baurain D. Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol. 2011, 9:e1000602. 10.1371/journal.pbio.1000602.
65. Pick K.S., Philippe H., Schreiber F., Erpenbeck D., Jackson D.J., Wrede P., Wiens M., Alie A., Morgenstern B., Manuel M., Wörheide G. Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol. Biol. Evol. 2010, 27:1983-1987.
66. Podar M., Haddock S.H., Sogin M.L., Harbison G.R. A molecular phylogenetic framework for the phylum Ctenophora using 18S rRNA genes. Mol. Phyl. Evol. 2001, 21:218-230.
67. Purcell J.E. Jellyfish and ctenophore blooms coincide with human proliferations and environmental perturbations. Ann. Rev. Mar. Sci. 2012, 4:209-235.
68. Rokas A., King N., Finnerty J., Carroll S.B. Conflicting phylogenetic signals at the base of the metazoan tree. Evol. Dev. 2003, 5:346-359.
69. Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
70. Ryan J.F., Pang K., Schnitzler C.E., Nguyen A.-D., Moreland R.T., Simmons D.K., Koch B.J., Francis W.R., Havlak P., Smith S.A., Putnam N.H., Haddock S.H.D., Dunn C.W., Wolfsberg T.G., Mullikin J.C., Martindale M.Q., Baxevanis A.D. The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 2013, 342:1242592. NISC Comparative Sequencing Program. 10.1126/science.1242592.
71. Schierwater B., Eitel M., Jakob W., Osigus H.-J., Hadrys H., Dellaporta S.L., Kolokotronis S.-O., DeSalle R. Concatenated analysis sheds light on early metazoan evolution and fuels a modern "urmetazoan" hypothesis. PLoS Biology 2009, 7(1). e20. 10.1371/journal.pbio.1000020.
72. Song J.-I., Hwang S.-J., Lee S.-H., Park J.-K. New records of creeping ctenophores, genus Coeloplana (Tentaculata: Platyctenida: Coeloplanidae), from Korea. Korean J. Syst. Zool. 2011, 27:47-52.
73. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690.
74. Telford M.J., Copley R.R. Improving animal phylogenies with genomic data. Trends Genet. 2011, 27:186-195.
75. Trégouboff G., Rose M. Manuel de Planctonologie Méditerranéenne 1957, Editions du CNRS, Paris.
76. Voigt O., Erpenbeck D., Wörheide G. Molecular evolution of rDNA in early diverging Metazoa: first comparative analysis and phylogenetic application of complete SSU rRNA secondary structures in Porifera. BMC Evol. Biol. 2008, 8:69. 10.1186/1471-2148-8-69.
77. Yamada A., Martindale M.Q., Fukui A., Tochinai S. Highly conserved functions of the Brachyury gene on morphogenetic movements: insight from the early-diverging phylum Ctenophora. Dev. Biol. 2010, 339:212-222.
78. Zhao G.H., Li J., Mo X.H., Li X.Y., Lin R.Q., Zou F.C., Weng Y.B., Song H.Q., Zhu X.Q. The second transcribed spacer rDNA sequence: an effective genetic marker for inter-species phylogenetic analysis of trematodes in the order Strigeata. Parasitol. Res. 2012, 111:1467-1472.
79. Zrzavy J., Mihulka S., Kepka P., Bezdek A., Tietz D. Phylogeny of the Metazoa based on morphological and 18S ribosomal DNA evidence. Cladistics 1998, 14:249-285.