Mitochondrial genome and nuclear sequence data support Myzostomida as part of the annelid radiation

Molecular Biology and Evolution

Volumn 24, Issue 8, 2007, Pages 1690-1701

  Bleidorn, Christoph ^a   Eeckhaut, Igor ^b   Podsiadlowski, Lars ^c   Schult, Nancy ^d   McHugh, Damhnait ^d   Halanych, Kenneth M ^e   Milinkovitch, Michel C ^f   Tiedemann, Ralph ^a  

^a UNIVERSITY OF POTSDAM   (Germany)

^b UNIVERSITY OF MONS   (Belgium)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

^d Assistant Professor in the University Libraries

^e AUBURN UNIVERSITY   (United States)

^f FREE UNIVERSITY OF BRUSSELS   (Belgium)

Author keywords

Annelida; Gene order; Long branch attraction; Mitochondrial genome; Myosin II; Myzostomida

Indexed keywords

ELONGATION FACTOR 1ALPHA; MYOSIN II; RIBOSOME DNA;

ANNELID WORM; ARTICLE; CONTROLLED STUDY; ECHINODERM; GENE SEQUENCE; MITOCHONDRIAL GENE; MYZOSTOMA CIRRIFERUM; MYZOSTOMA SEYMOURCOLLEGIORUM; NONHUMAN; PHYLOGENY; SYMBIONT;

ANIMALS; ANNELIDA; BAYES THEOREM; CELL NUCLEUS; DNA, MITOCHONDRIAL; DNA, RIBOSOMAL; ECHINODERMATA; EVOLUTION, MOLECULAR; GENES, MITOCHONDRIAL; GENETIC MARKERS; GENOME; HOST-PARASITE RELATIONS; LIKELIHOOD FUNCTIONS; MYOSIN TYPE II; PEPTIDE ELONGATION FACTOR 1; PHYLOGENY; SYMBIOSIS;

ANNELIDA; ECHINODERMATA; LOPHOTROCHOZOA; MYZOSTOMIDA; SIPUNCULUS NUDUS;

EID: 34547812067     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msm086     Document Type: Article

References (87)

1. Abascal F, Zardoya R, Posada D. 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics. 21:2104-2105.
2. Afzelius BA. 1983. The spermatozoon of Myzostomum cirriferum (Annelida, Myzostomida). J. Ultrastruct Res. 83:58-68.
3. Bartolomaeus T, Purschke G, Hausen H. 2005. Polychaete phylogeny based on morphological data - a comparison of current attempts. Hydrobiologia. 535/536:341-356.
4. Bartolomaeus T, Quast B. 2005. Structure and development of nephridia in Annelida and related taxa. Hydrobiologia. 535/536:139-165.
5. Benham WB. 1896. Archiannelida, Polychaeta, Myzostomidaria. In: Farmer SF, Shipley AE, editors. The Cambridge natural history. London: Macmillan. p. 241-334.
6. Bergsten J. 2005. A review of long-branch attraction. Cladistics. 21:163-193.
7. Bleidorn C. 2005. Phylogenetic relationships and evolution of Orbiniidae (Annelida, Polychaeta) based on molecular data. Zool J Linn Soc. 144:59-73.
8. Bleidorn C, Podsiadlowski L, Bartolomaeus T. 2006. The complete mitochondrial genome of the orbiniid polychaete Orbinia latreillii (Annelida, Orbiniidae) - a novel gene order for Annelida and implications for annelid phylogeny. Gene. 370:96-103.
9. Bleidorn C, Vogt L, Bartolomaeus T. 2003. New insights into polychaete phylogeny (Annelida) inferred by 18S rDNA sequences. Mol Phylogenet Evol. 29:279-288.
10. Boore JL. 1999. Animal mitochondrial genomes. Nucleic Acids Res. 27:1767-1780.
11. Boore JL, Brown WM. 1998. Big trees from little genomes: mitochondrial gene order as a phylogenetic tool. Curr Opin Gen Dev. 8:668-674.
12. Boore JL, Staton JL. 2002. The mitochondrial genome of the sipunculid Phascolopsis gouldii supports its association with Annelida rather than Mollusca. Mol Biol Evol. 19:127-137.
13. Brusca RC, Brusca GJ. 2003. Invertebrates. Sunderland, MA: Sinauer Associates.
14. Castresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 17:540-552.
15. Eeckhaut I. 1998. Mycomyzostoma caldicola gen. et sp. n., the first extant myzostomid infesting crinoid stalks, with a nomenclatural appendix by M.J. Grygier. Spec Div. 3:89-103.
16. Eeckhaut I, Dochy B, Jangoux M. 1995. Feeding behaviour and functional morphology of the introvert and digestive system of Myzostoma cirriferum (Myzostomida). Acta Zool. 76: 307-315.
17. Eeckhaut I, Fievez M, Müller MC. 2003. Larval development of Myzostoma cirriferum (Myzostomida). J Morph. 258:269-283.
18. Eeckhaut I, Jangoux M. 1991. Fine structure of the spermatophore and intradermic penetration of sperm cells in Myzostoma cirriferum (Annelida, Myzostomida). Zoomorphology. 111:49-58.
19. Eeckhaut I, Jangoux M. 1993. Integument and epidermal sensory structures of Myzostoma cirriferum (Myzostomida). Zoomorphology. 113:33-46.
20. Eeckhaut I, Lanterbecq D. 2005. Myzostomida: A review of the phylogeny and ultrastructure. Hydrobiologia. 535/536:253-275.
21. Eeckhaut I, McHugh D, Mardulyn P, Tiedemann R, Monteyne D, Jangoux M, Milinkovitch MC. 2000. Myzostomida: a link between trochozoans and flatworms? Proc R Soc Lond. B. 267:1383-1392.
22. Fedotov D. 1929. Beiträge zur Kenntnis der Morphologie der Myzostomiden. Z. Morphol Ökol Tiere. 15:156-191.
23. Felsenstein J. 1978. Cases in which parsimony or compability methods will be positively misleading. Syst Zool. 27:401-410.
24. Fritzsch G, Schlegel M, Stadler PF. 2006. Alignments of mitochondrial genome arrangements: Applications to metazoan phylogeny. J Theor Biol. 240:511-520.
25. Giribet G, Soerensen MV, Funch P, Kristensen RM, Sterrer W. 2004. Investigations into the phylogenetic position of Micrognathozoa using four molecular loci. Cladistics. 20:1-13.
26. Graff L. 1877. Das Genus Myzostoma (F.S. Leuckhart). Leipzig: Wilhelm Engelmann.
27. Grygier MJ. 2000. Myzostomida. In: Beesley PL, Ross GJB, Glasby CJ, editors. Polychaetes and allies: the southern synthesis. Fauna of Australia, Vol 4A Polychaeta, Myzostomida, Pogonophora, Echiura, Sipuncula. Melbourne: CSIRO Publishing. p. 297-330.
28. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52:696-704.
29. Halanych KM. 2004. The new view of animal phylogeny. Ann Rev Ecol Evol Syst. 35:229-256.
30. Halanych KM, Dahlgren TG, McHugh D. 2002. Evidence that some lesser-known "phyla" are annelids. Amer Zool. 42:678-684.
31. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/ NT. Nucleic Acids Symp Ser. 41:95-98.
32. Haszprunar G. 1996. The Mollusca: coelomate turbellarians or mesenchymate annelids? In: Taylor JD, editor. Origin and evolutionary radiation of the Mollusca. Oxford: Oxford University Press. p. 3-28.
33. Hausen H. 2005. Chaetae and chaetogenesis in polychaetes (Annelida). Hydrobiologia. 535/536:37-52.
34. Hessling R, Westheide W. 2002. Are Echiura derived from a segmented ancestor? Immunohistochemical analysis of the nervous system in developmental stages of Bonellia viridis. J Morphol. 252:100-113.
35. Huelsenbeck J. 1997. Is the Felsenstein zone a fly trap? Syst Biol. 46:69-74.
36. Jägersten G. 1936. Zur Kenntnis der Parapodialborsten bei Myzostomum. Zool Bidrag fran Uppsala. 16:283-294.
37. Jägersten G. 1940. Zur Kenntnis der Morphologie, Entwicklung und Taxanomie der Myzostomida. Nova Acta Reg Soc Sci Ups. 11:1-84.
38. Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ. 1998. Multiple sequence alignment with Clustal X.. Trends Biochem Sci. 23:403-405.
39. Jenner RA. 2001. Bilaterian phylogeny and uncritically recycling of morphological data sets. Syst Biol. 50:730-742.
40. Jenner RA. 2003. Unleashing the force of cladistics? Metazoan phylogenetics and hypothesis testing. Integr Comp Biol. 43:207-218.
41. Jenner RA. 2004. When molecules and morphology clash: reconciling conflicting phylogenies of the Metazoa by considering secondary character loss. Evol Dev. 6:372-378.
42. Jennings RM, Halanych KM. 2005. Mitochondrial genomes of Clymenella torquata (Maldanidae) and Riftia pachyptila (Siboglinidae). Evidence for conserved gene order in Annelida. Mol Biol Evol. 22:210-222.
43. Jermiin LS, Ho SYW, Ababneh F, Robinson J, Larkum AWD. 2004. The biasing effect of compositional heterogeneity on phylogenetic estimates may be underestimated. Syst Biol. 53:638-643.
44. Kass RE, Raftery AE. 1995. Bayes factors. J Amer Stat Ass. 90:773-795.
45. Kato K. 1952. On the development of myzostome. Sci Rep Saitama Univ. (B). 1:1-16.
46. Kennedy M, Holland BR, Gray RD, Spencer HG. 2005. Untangling long branches: Identifying conflicting phylogenetic signals using spectral analysis, neighbour-net, and consensus networks. Syst Biol. 54:620-633.
47. Lanterbecq D, Bleidorn C, Michel S, Eeckhaut I. Locomotion and fine structure of parapodia in Myzostoma cirriferum (Myzostomida). Zoomorphology submitted.
48. Lanterbecq D, Rouse GW, Milinkovitch MC, Eeckhaut I. 2006. Molecular phylogenetic analyses indicate multiple independent emergences of parasitism in Myzostomida (Protostomia). Syst Biol. 55:208-227.
49. Lavrov DV, Lang BF. 2005. Poriferan mtDNA and animal phylogeny based on mitochondrial gene arrangements. Syst Biol. 54:651-659.
50. Leuckart FS. 1827. Versuch einer naturgemässen Eintheilung der Helminthen. Heidelberg: Neue Akademische Buchhandlung von Karl Gross.
51. Littlewood DTJ, Olson PD, Telford MJ, Herniou EA, Riutort M. 2001. Elongation Factor 1-alpha sequences alone do not assist in resolving the position of the Acoela within Metazoa. Mol Biol Evol. 18:437-442.
52. Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25:955-964.
53. Mayer C, Wägele JW. 2005. SAMS (Split analysis methods) Version 1.4 beta. Distributed by the authors.
54. Mattei X, Marchand B. 1987. Les spermatozoids des Acanthocephales et des Myzostomides. Resemblances et consequences phyletiques. Paris: C. R. Acad. Sci., Serie III, Sci. p. 525-529.
55. McHugh D. 1997. Molecular evidence that echiurans and pogonophorans are derived annelids. Proc Natl Acad Sci USA. 94:8006-8009.
56. McHugh D. 2005. Molecular systematics of polychaetes (Annelida). Hydrobiologia. 535/536:309-318.
57. Müller MC, Westheide W. 2000. Structure of the nervous system of Myzostoma cirriferum (Annelida) as revealed by immunohistochemistry and cLSM analyses. J Morph. 245:87-98.
58. Nielsen C. 2001. Animal evolution: Interrelationships of the living phyla. New York: Oxford University Press.
59. Nylander J, Ronquist F, Huelsenbeck J, Nieves-Aldrey J. 2004. Bayesian phylogenetic analysis of combined data. Syst Biol. 53:47-67.
60. Passamaneck Y, Halanych KM. 2006. Lophotrochozoan phylogeny assessed with LSU and SSU data: evidence of lophophorate polyphyly. Mol Phylogenet Evol. 40:20-28.
61. Pietsch A, Wesheide W. 1987. Protonephridial organs in Myzostoma cirriferum (Myzostomida). Acta Zool. 68:195-203.
62. Podsiadlowski L, Bartolomaeus T. 2005. Organization of the mitochondrial genome of mantis shrimp Pseudosquilla ciliata (Crustacea: Stomatopoda). Mar Biotechnol. 7:618-624.
63. Posada D, Crandall KA. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics. 14:817-818.
64. Rambaut A, Grassly NC. 1997. Seq-Gen: an application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees. Comput Appl Biosci. 13:235-238.
65. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 19:1572-1574.
66. Rouse GW. 1999. Trochophore concepts: ciliary bands and the evolution of larvae in spiralian Metazoa. Biol J Linn Soc. 66:411-464.
67. Rouse GW, Fauchald K. 1997. Cladistics and polychaetes. Zool Scr. 26:139-204.
68. Rouse GW, Grygier MJ. 2005. Myzostoma seymourcollegiorum n. sp. (Myzostomida) from southern Australia, with a description of its larval development. Zootaxa. 1010:53-64.
69. Rouse GW, Pleijel F. 2001. Polychaetes. Oxford: Oxford University Press.
70. Ruiz-Trillo I, Paps J, Loukota M, Ribera C, Jondelius U, Baguna J, Riutort M. 2002. A phylogenetic analysis of myosin heavy chain type II sequences corroborates that Acoela and Nemertodermatida are basal bilaterians. Proc Nat Acad Sci USA. 99:11246-11251.
71. 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.
72. Scholtz G. 2002. The Articulata hypothesis - or what is a segment? Org Divers Evol. 2:197-215.
73. Seaver EC. 2003. Segmentation: mono- or polyphyletic? Int J Dev Biol. 47:583-595.
74. Seaver EC, Thamm K, Hill SD. 2005. Growth patterns during segmentation in the two polychaete annelids, Capitella sp. I and Hydroides elegans: comparisons at distinct life history stages. Evol Dev. 7:312-326.
75. Semper C. 1858. Zur Anatomie und Entwicklungsgeschichte der Gattung Myzostoma Leuckhart. Z Wiss Zool. 9:48-65.
76. Simon C, Buckley TR, Frati F, Stewart JB, Beckenbach AT. 2006. Incorporating molecular evolution into phylogenetic analysis, and a new compilation of conserved polymerase chain reaction primers for animal mitochondrial DNA. Ann Rev Ecol Evol Syst. 37:545-579.
77. Smith JPS, Lombardi J, Rieger RM. 1986. Ultrastructure of the body cavity lining in a secondary acoelomate, Microphthalmus cf listensis Westheide(Polychaeta, Hesionidae). J Morph. 188p. 257-271.
78. Southward EC. 1993. Pogonophora. In: Harrison FW, Rice ME, editors. Microscopic anatomy of invertebrates, vol. 12. Onychophora, Chilopoda and lesser Protostomata. New York: Wiley-Liss. p. 327-369.
79. Steel MA. 1994. Recovering a tree from the leaf colorations it generates under a Markov model. Appl Math Lett. 7:19-24.
80. Swofford DL. 2002. PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods). Sunderland, MA: Sinauer Associates. Tautz D. 2004. Segmentation. Dev Cell. 7:301-312.
81. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
82. Vallés Y, Boore JL. 2006. Lophotrochozoan mitochondrial genomes. Integr Comp Biol. 46:544-557.
83. Wägele JW, Rödding F. 1998. A priori estimation of phylogenetic information conserved in aligned sequences. Mol Phylogenet Evol. 9:358-365.
84. Willmer P. 1990. Invertebrate relationships. Patters in animal evolution. New York: Cambridge University Press.
85. Wyman SK, Jansen RK, Boore JL. 2004. Automatic annotation of organellar genomes with DOGMA. Bioinformatics. 20:3252-3255.
86. Xia X, Xie Z. 2001. DAMBE: Data analysis in molecular biology and evolution. J. Hered. 92:371-373.
87. Zrzavy J, Hypsa V, Tietz D. 2001. Myzostomida are not annelids: molecular and morphological support for a clade of animals with anterior sperm flagella. Cladistics. 17:1-29.