Shaping the things to come: Ontogeny of lophotrochozoan neuromuscular systems and the tetraneuralia concept

Biological Bulletin

Volumn 216, Issue 3, 2009, Pages 293-306

  Wanninger, Andreas ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ANNELID; BODY SHAPE; BRYOZOAN; DEVELOPMENTAL BIOLOGY; MOLLUSC; MORPHOLOGY; NEUROLOGY; ONTOGENY; PHENOTYPE; PHYLOGENETICS; RELATEDNESS;

ANIMAL; ARTICLE; GROWTH, DEVELOPMENT AND AGING; INVERTEBRATE; LARVA; MUSCLE DEVELOPMENT; NERVOUS SYSTEM; PHENOTYPE;

ANIMALS; INVERTEBRATES; LARVA; MUSCLE DEVELOPMENT; NERVOUS SYSTEM; PHENOTYPE;

ANNELIDA; BILATERIA; CHAETODERMOMORPHA; ECHIURA; ENTOPROCTA; LOPHOTROCHOZOA; MOLLUSCA; SIPUNCULIDA; SPIRALIA;

EID: 60849132425     PISSN: 00063185     EISSN: None     Source Type: Journal    
DOI: 10.2307/25548161     Document Type: Article

References (81)

1. Ax. P. 1999. Das System der Metazoa. 2nd ed. Gustav Fischer. Stuttgart.
2. Bartolomaeus. T. 1993a. Die Leibeshohlenverhaltnisse und Ver- wandtschaftsbeziehungen der Spiralia. Verh. Dtsch. Zool. Ges. 86: 42.
3. Bartolomaeus. T. 1993b. Die Leibeshohlenverhaltnisse und Nephridi- alorgane der Bilaleria-Ultrastruktur. Entwicklung und Evolution. University of Gottingen. Gottingen.
4. Bergter. A.. and A. Paululat. 2007. Pattern of body-wall muscle differentiation during embryonic development of Enchytraeus coronalus (Annelida: Oligochaeta; Enchytraeidae). J. Morphol. 268: 537-549.
5. Bergter. A.. J. Brubacher. and A. Paululat. 2008. Muscle formation during embryogenesis of the polychaete Ophryotrocha diadema (Dor- villeidae)-new insights into annelid muscle patterns. Front. Zool. 5: 1.
6. Boore. J. L.. and J. L. Staton. 2002. The mitochondrial genome of the sipunculid Phascolopsis gouldii supports its association with Annelida rather than Mollusca. Mol. Biol. Evol. 19: 127-137.
7. Brinkmann. N.. and A. Wanninger. 2008. Larval neurogenesis in Sa- bellaria alveolata reveals plasticity in polychaete neural patterning. Evol. Dev. 10: 606-618.
8. Cebria. F.. M. Vispo. P. Newmark. D. Bueno. and R. Romero. 1997. Myocyte differentiation and body wall muscle regeneration in the planarian Girardia tigrina. Dev. Genes Evol. 207: 306-316.
9. Davis. G. K.. and N. H. Patel. 1999. The origin and evolution of segmentation. Trends Biochem. Sci. 12: M68-M72.
10. De Rosa. R.. B. Prud'homme. and G. Balavoine 2005. Caudal and even-skipped in the annelid Platynereis dumerilii and the ancestry of posterior growth. Evol. Dev. 7: 574-587.
11. Dunn. C. W.. A. Hejnol. D. Q. Matus. K. Pang. W. E. Browne. S. A. Smith. E. Seaver. G. W. Rouse. M. Obst. G. D. Edgecombe. el al. 2008. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452: 745-749.
12. Friedrich. S.. A. Wanninger. M. Brückner. and G. Haszprunar. 2002. Neurogenesis in the mossy chiton. Mopalia muscosa (Gould) (Polypla- cophora): evidence against molluscan metamerism. J. Morphol. 253: 109-117.
13. Fuchs. J.. and A. Wanninger. 2008. Reconstruction of the neuromuscular system of the swimming-type larva of Loxosomella atkinsae (Entoprocta) as inferred by fluorescence labelling and confocal microscopy. Org. Divers. Evol. 8: 325-335.
14. Ghiselin. M. T. 1988. The origin of molluscs in the light of molecular evidence. Pp. 66-95 in Oxford Surveys in Evolutionary Biology. Vol. 5. P. H. Harvey and L. Partridge. eds. Oxford University Press. Oxford.
15. Giribet. G.. D. L. Distel. M. Polz. W. Sterrer. and W. C. Wheeler. 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: 539-562.
16. Götting. K. J. 1980. Argumente fur die Deszendenz der Mollusken von metameren Antezendenten. Zool. Jb. Anal. 103: 211-218.
17. Gruhl. A. 2008. Muscular systems in gymnolaemate bryozoan larvae (Bryozoa: Gymnolaemata). Zoomorphology 127: 143-159.
18. Halanych. K. M. 1996. Convergence in the feeding apparatuses of lophophorates and pterobranch hemichordates revealed by 18S rDNA: an interpretation. Biol. Bull. 190: 1-5.
19. Halanych. K. M.. T. G. Dahlgren. and D. McHugh. 2002. Unseg- mented annelids? Possible origins of four lophotrochozoan worm taxa. Integr. Comp. Biol. 42: 678-684.
20. Haszprunar. G. 1996. The Mollusca: coelomate turbellarians or mesen-chymate annelids? Pp. 1-28 in Origin and Evolutionary Radiation of the Mollusca. J. D. Taylor. ed. Oxford University Press. Oxford.
21. Haszprunar. G. 2000. Is the Aplacophora monophyletic? A cladistic point of view. Am. Malacol. Bull. 15: 115-130.
22. Haszprunar. G.. and A. Wanninger. 2000. Molluscan muscle systems in development and evolution. J. Zool. Syst. Evol. Res. 38: 157-163.
23. Haszprunar G.. and A. Wanninger. 2008. On the fine structure of the creeping larva of Loxosomella murmanica: additional evidence for a clade of Kamptozoa (Entoprocta) and Mollusca. Acta Zool. (Stockh.) 89: 137-148.
24. Haszprunar. G.. C. Schander. and K. M. Halanych. 2008. Relationships of higher molluscan taxa. Pp. 19-32 in Phytogeny and Evolution of the Mollusca. W. F. Ponder and D. R. Lindberg. eds. University of California Press. Berkeley.
25. Hatschek. B. 1878. Studien uber die Entwicklungsgeschichte der Anne- liden. Ein Beitrag zur Morphologie der Bilaterien. Arbeiten aus dem Zoologischen lnslilul der Universitdt Wien 1: 277-404.
26. Hay-Schmidt. A. 2000. The evolution of the serotonergic nervous system. Proc. R. Soc. Lond. B 267: 1071-1079.
27. Helmkampf. M.. I. Bruchhaus. and B. Hausdorf. 2008. Multigene analysis of lophophorate and chaetognath phylogenetic relationships. Mol. Phylogenet. Evol. 46: 206-214.
28. Hessling. R. 2002. Metameric organisation of the nervous system in developmental stages of Urechis caupo (Echiura) and its phylogenetic implications. Zoomorphology 121: 221-234.
29. Hessling. R. 2003. Novel aspects of the nervous system of Bonellia viridis (Echiura) revealed by the combination of immunohistochemis- try. confocal laser-scanning microscopy and three-dimensional reconstruction. Hydrobiologia 496: 225-239.
30. Hessling. R.. and W. Westheide. 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.
31. Hill. S. D.. and B. C. Boyer. 2001. Phalloidin labeling of developing muscle in embryos of the polychaete Capitella sp. I. Biol. Bull. 201: 257-258.
32. Kristof. A.. T. Wollesen. and A. Wanninger. 2008. Segmental mode of neural patterning in Sipuncula. Curr. Biol. 18: 1129-1132.
33. Ladurner. P.. and R. M. Rieger. 2000. Embryonic muscle development of Convoluta pulchra (Turbellaria-Acoelomorpha. Platyhelminthes). Dev. Biol. 222: 359-375.
34. Lake. J. A. 1990. Origin of the Metazoa. Proc. Natl. Acad. Sci. USA 87: 763-766.
35. Mackey. L. J.. B. Winnepenninckx. R. De Wachter. T. Backeljau. P. Emschermann. and J. R. Garey. 1996. 18S rRNA suggests that Entoprocta are protostomes. unrelated to Ectoprocta. J. Mol. Evol. 42: 552-559.
36. Mair. G. R.. A. G. Maule. C. Shaw. and D. W. Halton. 1998. Muscling in on parasitic flatworms. Parasitol. Today 14: 73-76.
37. Maslakova. S. A.. M. Q. Martindale. and J. L. Norenburg. 2004. Vestigial prototroch in a basal nemertean. Carinoma tremaphoros (Nemertea; Palaeonemertea). Evol. Dev. 6: 219-226.
38. McDougall. C. W. C. Chen. S. M. Shimeld. and D. E. Ferrier. 2006. The development of the larval nervous system. musculature and ciliary bands of Pomatocerus lamarckii (Annelida): heterochrony in polychaetes. Front. Zool. 3: 16.
39. McHugh. D. 1997. Molecular evidence that echiurans and pogono- phorans are derived annelids. Proc. Nail. Acad. Sci. USA 94: 8006- 8009.
40. Neves. R. C. R. M. Kristensen. and A. Wanninger. 2009. Three- dimensional reconstruction of the musculature of various life cycle stages of the cycliophoran Symbion americanus. J. Morphol. 270: 257-270.
41. Nielsen. C. 1971. Entoproct life-cycles and the entoproct/ectoproct relationship. Ophelia 9: 209-341.
42. Nielsen. C. 2001. Animal Evolution: Interrelationships of the Living Phyla. 2nd ed. Oxford University Press. Oxford.
43. Nielsen. C. G. Haszprunar. B. Ruthensteiner. and A. Wanninger. 2007. Early development of the aplacophoran mollusc Chaetoderma. Acta Zool. (Stockh.) 88: 231-247.
44. Page. L. R. 2002. Comparative structure of the larval apical sensory organ in gastropods and hypotheses about function and developmental evolution. Invertebr. Reprod. Dev. 41: 193-200.
45. Passamaneck. Y. J.. and K. M. Halanych. 2004. Evidence from Hox genes that bryozoans are lophotrochozoans. Evol. Dev. 6: 275-281.
46. Passamanek. Y. J.. and K. M. Halanych. 2006. Lophotrochozoan phy- logeny assessed with LSU and SSU data: evidence of lophophorate polyphyly. Mol. Phylogenet. Evol. 40: 20-28.
47. Peterson. K. J.. and D. J. Eernisse. 2001. Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences. Evol. Dev. 3: 170-205.
48. Philippe. H.. N. Lartillot. and H. Brinkmann. 2005. Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa. Lophotrochozoa. and Protostomia. Mol. Biol. Evol. 22: 1246-1253.
49. Pires. A.. and R. M. Woollacott. 1997. Serotonin and dopamine have opposite effects on phototaxis in larvae of the bryozoan Bugula neritina. Biol. Bull. 192: 399-409.
50. Ponder. W. F.. and D. R. Lindberg. 2008. Molluscan evolution and phylogeny. Pp. 1-17 in Phylogeny and Evolution of the Mollusca. W. F. Ponder and D. R. Lindberg. eds. University of California Press. Berkeley.
51. Reiter. D.. B. Boyer. P. Ladurner. G. Mair. W. Salvenmoser. and R. Rieger. 1996. Differentiation of the body wall musculature in Mac- rostomum hyslricinum and Hoploplana inquilina (Plathelminthes). as models for muscle development in lower Spiralia. Roux's Arch. Dev. Biol. 205: 410-423.
52. Rieger. R. M.. S. Tyler. J. P. S. Smith. and G. Rieger. 1991. Platy- helminthes: Turbellaria. Pp. 7-140 in Microscopic Anatomy of Invertebrates. Vol. 3. Platyhelminthes and Nemertinea. F. W. Harrison and B. J. Bogitsch. eds. Wiley-Liss. New York.
53. Rouse. G. W. 1999. Trochophore concepts: ciliary bands and the evolution of larvae in spiralian Metazoa. Biol. J. Linn. Soc. 66: 411-464.
54. Salvini-Plawen. L. v. 1973. Zur Klarung des " Trochophora"-Begriffes. Experentia 29: 1434-1436.
55. Salvini-Plawen. L. v. 1978. On the origin and evolution of the lower Metazoa. Z Zool. Syst. Evolutionsforsch. 16: 40-88.
56. Santagata. S. 2002. Structure and metamorphic remodeling of the larval nervous system and musculature of Phoronis pallida (Phoronida). Evol. Dev. 4: 28-42.
57. Santagata. S. 2008a. The morphology and evolutionary significance of the ciliary fields and musculature among marine bryozoan larvae. J. Morphol. 269: 349-364.
58. Santagata. S. 2008b. Evolutionary and structural diversification of the larval nervous system among marine bryozoans. Biol. Bull. 215: 3-23.
59. Santagata. S.. and R. L. Zimmer. 2002. Comparison of the neuromuscular systems among actinotroch larvae: systematic and evolutionary implications. Evol. Dev. 4: 43-54.
60. Seaver. E. C. K. Thamm. and S. D. Hill. 2005. Growth patterns during segmentation in the two polychaete annelids. Capitella sp. 1 and Hy- droides elegans: comparisons at distinct life history stages. Evol. Dev. 7: 312-326.
61. Semmler. H.. X. Bailly. and A. Wanninger. 2008. Myogenesis in the basal bilaterian Symsagittifera roscoffensis (Acoela). Front. Zool. 5: 14.
62. Shimizu. K.. E. Hunter. and N. Fusetani. 2000. Localisation of biogenic amines in larvae of Buguki neritina (Bryozoa: Cheilostomatida) and their effects on settlement. Mar. Biol. 136: 1-9.
63. Smith. N. F.. K. B. Johnson. and C. M. Young. 2002. Phylum Platy- helminthes. Pp. 123-152 in Atlas of Marine Invertebrate Larvae. C. M. Young. ed. Academic Press. London.
64. Struck. T. H.. N. Schult. T. Kusen. E. Hickman. C. Bleidorn. D. McHugh. and K. M. Halanych. 2007. Annelid phytogeny and the status of Sipuncula and Echiura. BMC Evol. Biol. 7: 57.
65. Valentine. J. W. 2004. On the Origin of Phyla. The University of Chicago Press. Chicago.
66. Voronezhskaya. E. E.. S. A. Tyurin. and L. P. Nezlin. 2002. Neuronal development in larval chiton Ischnochiton hakodadensis (Mollusca: Polyplacophora). J. Comp. Neurol. 444: 25-38.
67. Voronezhskaya. E. E.. E. B. Tsitrin. and L. P. Nezlin. 2003. Neuronal development in larval polychaete Phyllodoce maculata (Phyllodoci- dae). .J. Comp. Neurol. 455: 299-309.
68. Wanninger. A. 2005. Immunocytochemistry of the nervous system and the musculature of the chordoid larva of Symbion pandora (Cyclio- phora). .J. Morphol. 265: 237-243.
69. Wanninger. A. 2007. The application of confocal microscopy and 3D imaging software in Functional. Evolutionary. and Developmental Zoology: reconstructing myo- and neurogenesis in space and time. Pp. 353-361 in Modern Research and Educational Topics in Microscopy. A. Mendéz-Vilas and J. Dias. eds. Formatex. Badajoz. Spain.
70. Wanninger. A. 2008. Comparative lophotrochozoan neurogenesis and larval neuroanatomy: recent advances from previously neglected taxa. Acta Biol. Hung. 59 (Suppl.): 127-136.
71. Wanninger. A.. and G. Haszprunar. 2002a. Chiton myogenesis: per-spectives for the development and evolution of larval and adult muscle systems in molluscs. J. Morphol. 251: 103-113.
72. Wanninger. A.. and G. Haszprunar 2002b. Muscle development in Antalis entalis (Mollusca. Scaphopoda) and its significance for scapho- pod relationships. J. Morphol. 254: 53-64.
73. Wanninger. A.. and G. Haszprunar. 2003. The development of the serotonergic and FMRF-amidergic nervous system in Antalis entalis (Mollusca. Scaphopoda). Zoomorphology 122: 77-85.
74. Wanninger. A.. B. Ruthensteiner. S. Lobenwein. W. Salvenmoser. W. J. A. G. Dictus. and G. Haszprunar. 1999. Development of the musculature in the limpet Patella (Mollusca. Patellogastropoda). Dev. Genes Evol. 209: 226-238.
75. Wanninger. A.. D. Koop. L. Bromham. E. Noonan. and B. M. Degnan. 2005a. Nervous and muscle system development in Phascolion strombus (Sipuncula). Dev. Genes Evol. 215: 509-518.
76. Wanninger A.. D. Koop. and B. M. Degnan. 2005b. Immunocyto- chemistry of the larval nervous system of Triphyllozoon mucronatmn (Ectoprocta: Gymnolaemata: Cheilostomata) and its fate during metamorphosis. Zoomorphology 124: 161-170.
77. Wanninger. A.. J. Fuchs. and G. Haszprunar. 2007. The anatomy of the serotonergic nervous system of an entoproct creeping-type larva and its phylogenetic implications. Invertebr. Biol. 126: 268-278.
78. Wanninger. A.. D. Koop. S. Moshel-Lynch. and B. M. Degnan. 2008. Molluscan evolutioanry development. Pp. 1-17 in Phyiogeny and Evolution of the Mollusca. W. F. Ponder and D. R. Lindberg. eds. University of California Press. Berkeley.
79. Wanninger. A.. A. Kristof. and N. Brinkmann. 2009. Sipunculans and segmentation. Communicative Integr. Biol. 2: 56-59.
80. Weisblat. D. A.. D. .1. Price. and C. J. Wedeen. 1988. Segmentation in leech development. Development 104 (Suppl.): 161-168.
81. Wollesen. T.. R. Loesel. and A. Wanninger 2008. FMRFamidergic immunoreactivity in the central nervous system of the cephalopod mollusc ldiosepius notoides. Acta Biol. Hung. 59 (Suppl.): 111-116.