Embryonic and post-embryonic development of the polyclad flatworm Maritigrella crozieri; implications for the evolution of spiralian life history traits

Frontiers in Zoology

Volumn 7, Issue , 2010, Pages

  Rawlinson, Kate A ^a,b  

^a SMITHSONIAN MARINE STATION   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTA; MARITIGRELLA CROZIERI; PLATYHELMINTHES; POLYCLADIDA; SPIRALIA;

EID: 77951600142     PISSN: None     EISSN: 17429994     Source Type: Journal    
DOI: 10.1186/1742-9994-7-12     Document Type: Article

References (97)

1. Ax P. The position of the Gnathostomulida and Platyhelminthes in the phylogenetic system of the Bilateria. The origins and relationships of lower invertebrates 1985, 168-180. Oxford: Clarendon Press, Conway Morris S, George JD, Gibson R, Platt HM.
2. Larsson K, Jondelius U. Phylogeny of Catenulida and support for Platyhelminthes. Orgs Divers Evol 2008, 8:378-387.
3. Giribet G, Dunn CW, Edgecombe GD, Hejnol A, Martindale MQ, Rouse GW. Assembling the spiralian tree of life. Animal Evolution: genomes, fossils and trees 2009, 52-64. Oxford University Press, Telford MJ, Littlewood DTJ.
4. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sorensen MV, Haddock SHD, Schmidt-Rhaesa A, Okusu A, Mobjerg Kristensen R, Wheeler WC, Martindale MQ, Giribet G. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 2008, 452:745-749. 10.1038/nature06614, 18322464.
5. Paps J, Baguna J, Riutort M. Lophotrochozoa internal phylogeny: new insights from an up-to-date analysis of nuclear ribosomal genes. Proc R Soc Lond Ser B-Biol Sci 2009, 276:1245-1254.
6. Hejnol A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Martinez P, Baguñà J, Bailly X, Jondelius U, Wiens M, Werner E, Müller G, Seaver E, Wheeler WC, Martindale MQ, Giribet G, Dunn CW. Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc R Soc Lond Ser B-Biol Sci 2009, doi: 10.1098/rspb.2009.
7. Sly BJ, Snoke MS, Raff RA. Who came first - larvae or adults? Origins of bilaterian metazoan larvae. Int J Dev Biol 2003, 47:623-632.
8. Arendt D, Technau U, Wittbrodt J. Evolution of the bilaterian larval foregut. Nature 2001, 409:81-85. 10.1038/35051075, 11343117.
9. Kato K. On the development of some Japanese polyclads. Jpn J Zool 1940, 8:537-573.
10. Jägersten G. Evolution of the metazoan life cycle. A comprehensive theory 1972, London: Academic Press.
11. Rooney LM, Boyer BC. New aspects of development of the polyclad, Hoploplana inquilina. Biol Bull 1984, 167:519-520.
12. Smith NF, Johnson KB, Young C. Phylum Platyhelminthes. Atlas of marine invertebrate larvae 2002, 123-148. San Diego: Academic Press, Young CM, Sewell MA, Rice ME.
13. Nielsen C. Trochophora larvae: cell lineages, ciliary bands and body regions.2. Other groups and general discussion. J Exp Zool Part B 2005, 304B:401-47.
14. Littlewood DTJ, Rohde K, Clough KA. The inter-relationships of all major groups of Platyhelminthes: phylogenetic evidence from morphology and molecules. Biol J Linn Soc 1999, 66:75-114.
15. Lockyer AE, Olson PD, Littlewood DTJ. Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biol J Linn Soc 2003, 78:155-171.
16. Baguñà J, Riutort M. Molecular phylogeny of the Platyhelminthes. Can J Zool 2004, 82:168-193.
17. Wanninger A, Haszprunar G. Chiton myogenesis: Perspectives for the development and evolution of larval and adult muscle systems in mollusks. J Morphol 2002, 251:103-113. 10.1002/jmor.1077, 11748697.
18. Wanninger A. Comparative lophotrochozoan neurogenesis and larval neuroanatomy: recent advances from previously neglected taxa. Acta Biol Hung 2008, 59:127-136. 10.1556/ABiol.59.2008.Suppl.21, 18652385.
19. Rieter D, Boyer BC, Ladurner P, Mair G, Salvenmoser W, Rieger R. Differentiation of the body wall musculature in Macrostomum hystricinum and Hoploplana inquilina (Platyhelminthes), as models for muscle development in lower Spiralia. Roux's Arch Dev Biol 1996, 205:410-423.
20. Bolaños DM, Litvatis M. Embryonic muscle development in direct and indirect developing marine flatworms (Platyhelminthes, Polycladida). Evol Dev 2009, 11:290-301. 10.1111/j.1525-142X.2009.00331.x, 19469856.
21. Younossi-Hartenstein A, Hartenstein V. The embryonic development of the polyclad flatworm Imogine mcgrathi. Dev Genes Evol 2000, 210:383-398. 10.1007/s004270000086, 11180845.
22. Ruppert EE. A review of metamorphosis of turbellarian larvae. Settlement and metamorphosis of marine invertebrate larvae 1978, 65-81. New York: Elsevier, Chia F-S, Rice ME.
23. Lacalli TC. The nervous system and ciliary band of Müller's larva. Proc R Soc Lond Ser B-Biol Sci 1982, 217:37-58.
24. Lacalli TC. The brain and central nervous system of Müller's larva. Can J Zool 1983, 61:39-51.
25. Surface FM. The early development of a polyclad, Planocera inquilina Wh. Proc Acad Natl Sci Phil 1907, 59:514-559.
26. Scarpa J, Weis B, Ruppert E, Frick J, Ford A, Wright A. Direct evidence of planktotrophy in Muller's larva of the tiger flatworm Pseudoceros crozieri [abstract]. Am Zool 1996, 36(5):107.
27. Wanninger A. Shaping the things to come: Ontogeny of Lophotrochozoan Neuromuscular Systems and the Tetraneuralia concept. Biol Bull 2009, 216:293-306. 10.2307/25548161, 19556595.
28. Morris J, Nallur R, Ladurner P, Egger B, Rieger R, Hartenstein V. The embryonic development of the flatworm Macrostomum sp. Dev Genes Evol 2004, 214(5):220-239. 10.1007/s00427-004-0406-4, 15083361.
29. Reisinger E, Cichocki I, Erlach R, Szyskowitz T. Ontogenetische Studien an Turbellarien: ein Beitrag zur Evolution der Dotterverarbeitung im ektolecitalen. Ei. Zeitschrtft fur zoologisches Systematik und Evolutions-forschung 1974, 12:161-195. 241-278.
30. Tyler S, Hooge M. Comparative morphology of the body wall of flatworms (Platyhelminthes). Can J Zool 2004, 82:194-210.
31. Gruber SA, Ewer DW. Observations on the myo-neural physiology of the polyclad, Planocera gilchristi. J Exp Biol 1962, 39:459-477.
32. MacRae EK. The fine structure of muscle in a marine turbellarian. Cell and Tissue Research 1965, 68:348-362.
33. Chien P, Koopowitz H. The ultrastructure of neuromuscular systems in Notoplana acticola, a free-living polyclad flatworm. Cell and Tissue Research 1972, 133:277-288.
34. Pedersen KJ. The organization of the connective tissue of Discocelides langi, (Turbellaria, polycladida). Cell and Tissue Research 1966, 71:94-117.
35. Johnson KB, Forward RB. Larval photoresponses of the polyclad flatworm Maritigrella crozieri (Platyhelminthes, Polycladida) (Hyman). J Exp Mar Biol Ecol 2003, 282:103-112.
36. Lang A. Die Polycladen (Seeplanarien) des Golfes von Neapel. Fauna Flora Golfes Neapel 1884, 11:1-688. Pls. 1-39.
37. Norenburg JL, Stricker SA. Phylum Nemertea. Atlas of marine invertebrate larvae 2002, 163-177. San Diego: Academic Press, Young CM, Sewell MA, Rice ME.
38. Wanninger A, Koop D, Degnan BM. Immunocytochemistry and metamorphic fae of the larval nervous system of Triphyllozoon mucronatum (Ectoprocta: Gymnolaemata: Cheilostomata). Zoomorphology 2005, 124:161-170.
39. Rieger RM, Salvenmoser W, Legniti A, Tyler S. Phalloidin-rhodamine preparations of Macrostomum hystricinum marinum (Plathelminthes): morphology and postembryonic development of the musculature. Zoomorphology 1994, 114:133-147.
40. Lacalli TC. The suboral complex in the Müller's larva of Pseudoceros canadensis (Platyhelminthes, Polycladida). Can J Zool 1988, 66:1893-1895.
41. Hay-Schmidt A. The Evolution of the Serotonergic Nervous System. Proc R Soc Lond Ser B-Biol Sci 2000, 267:1071-1079.
42. Croll RP. Development of embryonic and larval cells containing serotonin, catecholamines, and FMRFamide-related peptides in the gastropod mollusc Phestilla sibogae. Biol Bull 2006, 211:232-247. 10.2307/4134546, 17179383.
43. Jékely G, Colombelli J, Hausen H, Guy K, Stelzer E, Nédélec F, Arendt D. Mechanism of phototaxis in marine zooplankton. Nature 2008, 456:395-400. 10.1038/nature07590, 19020621.
44. Rawlinson KA, Bolaños DM, Liana MK, Litvaitis MK. Reproduction, Development and Parental Care of two direct developing flatworms (Platyhelminthes: Polycladida: Acotylea). J Nat Hist 2008, 42:173-2192.
45. Sopott-Ehlers SB, Salvenmoser W, Reiter D, Rieger R, Ehlers U. Photoreceptors in species of the Macrostomida (Plathelminthes): ultrastructural findings and phylogenetic implications. Zoomorphology 2001, 121(1):1-12.
46. Arendt D, Tessmar-Raible K, Snyman H, Dorresteijn AW, Wittbrodt J. Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science 2004, 306(5697):869-871. 10.1126/science.1099955, 15514158.
47. Page L, Kempf SC. Larval apical sensory organ in a neritimorph gastropod, an ancient gastropod lineage with feeding larvae. Zoomorphology 2009, 128:327-338.
48. Cronin TW. Photoreception in Marine Invertebrates. Am Zool 1986, 26:403-415.
49. Koopowitz H. On the evolution of central nervous systems: Implications from polyclad turbellarian neurobiology. Hydrobiologia 1986, 132:79-87.
50. Nielsen C, Nørrevang A. The trochaea theory: an example of life cycle evolution. The origins and relationships of lower invertebrates 1985, 28-41. Oxford: Clarendon Press, Conway Morris S, George JD, Gibson R, Platt HM.
51. Nielsen C. Origin and evolution of animal life cycles. Biol Rev 1998, 73:125-155.
52. Nielsen C. The phylogenetic position of Entoprocta and Ectoprocta. Proceedings of the 11th International Bryozoology Association Conference: 2002; Balboa: Smithsonian Tropical Research Institute 2000, 66-73. Herrera Cubilla A, Jackson JBC.
53. Nielsen C. Animal evolution. Interrelationships of the living phyla 2001, Oxford University Press.
54. Rouse GW. Trochophore concepts: ciliary bands and the evolution of larvae in spiralian Metazoa. Biol J Linn Soc 1999, 66:411-464.
55. Lacalli TC. Structure and organization of the nervous system in the trochophore larva of Spirobranchus. Phil Trans R Soc Lond B 1984, 306:79-135.
56. Nielsen C. Animal evolution. Interrelationships of the living phyla 1995, Oxford: Oxford University Press.
57. Peterson KJ, Cameron RA, Davidson EH. Bilaterian origins: significance of new experimental observations. Dev Biol 2000, 219:1-17. 10.1006/dbio.1999.9475, 10677251.
58. Telford MJ. Embryology and developmental genes as clues to platyhelminth relationships. Interrelationships of the Platyhelminthes 2001, Ch 24. Taylor and Francis London, Littlewood DTJ, Bray RA.
59. Ehlers U. Das phylogenetische System der Plathelminthes 1985, Stuttgart: Verlag.
60. Damen P, Dictus WJAG. Cell lineage of the prototroch of Patella vulgata (Gastropoda, Mollusca). Dev Biol 1994, 162:364-383. 10.1006/dbio.1994.1094, 8150201.
61. Mead AD. The cell origin of the prototroch. Biological Lectures, Marine Biological Laboratoy, Woods Hole 1899, 1898:113-138.
62. Boyer BC, Henry JQ, Martindale MQ. Dual Origins of Mesoderm in a Basal Spiralian: Cell Lineage Analyses in the Polyclad Turbellarian Hoploplana inquilina. Dev Biol 1996, 179:329-338. 10.1006/dbio.1996.0264, 8903349.
63. Jenner R. Towards a phylogeny of the Metazoa: evaluating alternative phylogenetic positions of Platyhelminthes, Nemertea, and Gnathostomulida, with a critical reappraisal of cladistic characters. Contributions in Zoology 2004, 73:3-163.
64. Biggelaar JAM, van Loon AE, Damen WGM. Mesentoblast and trochoblast specification in species with spiral cleavage predict their phyletic relations. Nether J Zool 1996, 46:8-21.
65. Biggelaar JAM, Dictus WJAG, van Loon AE. Cleavage patterns, cell-lineages and cell specification are clues to phyletic lineages in Spiralia. Semin Cell & Devel Biol 1997, 8:367-378.
66. McDougall C, Chen WC, Shimeld S, Ferrier DEK. The development of the larval nervous system, musculature and ciliary band of Pomatoceros lamarckii (Annelida): heterochrony in polychaetes. Front in Zool 2006, 3:16.
67. Arenas-Mena C, Wong KS-Y, Arandi N. Ciliary band gene expression patterns in the embryo and trochophore larva of an indirectly developing polychaete. Mechanisms of Development: Gene Expression Patterns 2007, 7:544-549.
68. Wanninger A, Ruthensteiner B, Lobenwein S, Salvenmoser W, Dictus WJAG, Haszprunar G. Development of the musculature in the limpet Patella (Mollusca, Patellogastropoda). Dev Genes Evol 1999, 209:226-238. 10.1007/s004270050247, 10079366.
69. Wanninger A, Haszprunar G. Muscle development in Antalis entalis (Mollusca, Scaphopoda) and its significance for scaphopod relationships. J Morphol 2002, 254:53-64. 10.1002/jmor.10004, 12219343.
70. Wanninger A, Koop D, Bromham L, Noonan E, Degnan BM. Nervous and muscle system development in Phascolion strombus (Sipuncula). Dev Genes Evol 2005, 215:509-518. 10.1007/s00427-005-0012-0, 16133569.
71. Friedrich S, Wanninger A, Brückner M, Haszprunar G. Neurogenesis in the Mossy Chiton, Mopalia muscosa (Gould)(Polyplacophora): evidence against molluscan metamerism. J Morphol 2002, 253:109-117. 10.1002/jmor.10010, 12112126.
72. Wanninger A, Fuchs J, Haszprunar G. The anatomy of the serotonergic nervous system of an entoproct creeping-type larva and its phylogenetic implications. Invertebr Biol 2007, 126:268-278.
73. Croll RP, Jackson DL, Voronezhskaya EE. Catecholamine-containing cells in larval and post-larval bivalve molluscs. Biol Bull 1997, 193:116-124.
74. Page LR, Paries SC. Comparative study of the apical ganglion in planktotrophic caenogastropod larvae: ultrastructure and immunoreactivity to serotonin. J Comp Neurol 2000, 418:383-401. 10.1002/(SICI)1096-9861(20000320)418:4<383::AID-CNE2>3.0.CO;2-B, 10713568.
75. Kempf SC, Page LR, Pires A. Development of serotonin-like immunoreactivity in the embryos and larvae of nudibranch mollusks with emphasis on the structure and possible function of the apical sensory organ. J Comp Neurol 1997, 386:507-528. 10.1002/(SICI)1096-9861(19970929)386:3<507::AID-CNE12>3.0.CO;2-7, 9303432.
76. Marois R, Carew TJ. Ontogeny of serotonergic neurons in Aplysia californica. J Comp Neurol 1997, 386:477-490. 10.1002/(SICI)1096-9861(19970929)386:3<477::AID-CNE10>3.0.CO;2-8, 9303430.
77. Dickinson AJG, Nason J, Croll RP. Histochemical localization of FMRFamide, serotonin and catecholamine in embryonic Crepidula fornicata (Prosobranchia: Gastropoda). Zoomorphology 1999, 119:49-62.
78. Dickinson AJG, Croll RP. Development of the larval nervous system of the gastropod Ilyanassa obsoleta. J Comp Neurol 2003, 466:187-218.
79. Salvini-Plawen LV. What is convergent/homoplastic in Pogonophora?. J Zool Syst Evol Res 2000, 38:133-147.
80. Wanninger A, Haszprunar G. The development of the serotonergic and FMRF-amidergic nervous system in Antalis entalis (Mollusca, Scaphopoda). Zoomorphology 2003, 122:77-85.
81. Hadfield MG, Meleshkevitch EA, Boudko DY. The apical sensory organ of a gastropod veliger is a receptor for settlement cues. Biol Bull 2000, 198:67-76. 10.2307/1542804, 10707814.
82. Leise EM, Thavaradhara K, Durham NR, Turner BE. Serotonin and nitric oxide regulate metamorphosis in the marine snail Ilyanassa obsoleta. Am Zool 2001, 41:258-267.
83. Hay-Schmidt A. Ultrastructure and immunocytochemistry of the nervous system of the larvae of Lingula anatina and Glottidia sp. (Brachiopoda). Zoomorphology 1992, 112:189-205.
84. Voronezhskaya EE, Tyurin SA, Nezlin LP. Neuronal development in larval chiton Ischnochiton hakodadensis (Mollusca: Polyplacophora). J Comp Neurol 2002, 444:25-38. 10.1002/cne.10130, 11835180.
85. Voronezhskaya EE, Nezlin LP, Odintsova NA, Plummer JT, Croll RP. Neuronal development in larval mussel Mytilus trossulus (Mollusca: Bivalvia). Zoomorphology 2008, 127:97-110.
86. Brinkmann N, Wanninger A. Larval neurogenesis in Sabellaria alveolata reveals plasticity in polychaete neural patterning. Evol Dev 2008, 10:606-618. 10.1111/j.1525-142X.2008.00275.x, 18803778.
87. Voronezhskaya EE, Tsitrin EB, Nezlin LP. Neuronal development in larval polychaete Phyllodoce maculata (Phyllodicidae). J Comp Neurol 2003, 455:299-309. 10.1002/cne.10488, 12483683.
88. Kristof A, Wollesen T, Wanninger A. Segmental mode of neural patterning in Sipuncula. Curr Biol 2008, 18:1129-1132. 10.1016/j.cub.2008.06.066, 18656359.
89. Santagata S. Structure and metamorphic remodeling of the larval nervous system and musculature of Phoronis pallida (Phoronida). Evo Dev 2002, 4:28-42.
90. Santagata S, Zimmer RL. Comparison of the neuromuscular systems among actinotroch larvae: systematic and evolutionary implications. Evol Dev 2002, 4:43-45. 10.1046/j.1525-142x.2002.01056.x, 11868657.
91. Santagata S. Evolutionary and structural diversification of the larval nervous system among marine bryozoans. Biol Bull 2008, 215:3-23. 10.2307/25470679, 18723633.
92. Hessling R, Westheide W. Are Echiura derived from a segmented ancestor? Immunocytochemical analysis of the nervous system in developmental stages of Bonellia viridis. J Morphol 2002, 252:100-113. 10.1002/jmor.1093, 11921039.
93. Hessling R. Novel aspects of the nervous system of Bonellia viridis (Echiura) revealed by the combination of immunohistochemistry, confocal laser-scanning microscopy and three-dimensional reconstruction. Hydrobiologia 2003, 496:225-239.
94. Wanninger A. Immunohistochemistry of the nervous system and the musculature of the choroids larva of Symbion Pandora (Cycliophora). J Morphol 2005, 265:237-243. 10.1002/jmor.10354, 15986410.
95. Hadfield MG, Meleshkvitch EA, Boudko DY. The apical sensory organ of a gastropod is a receptor for settlement cues. Biol Bull 2000, 198:67-76. 10.2307/1542804, 10707814.
96. Hall BK. Descent with modification: the unity underlying homology and homoplasy as seen through an analysis of development and evolution. Biol Rev 2003, 78:409-433. 10.1017/S1464793102006097, 14558591.
97. Boyer B. Development of in vitro fertilized embryos of the polyclad flatworm, Hoploplana inquilina, following blastomere separation and deletion. Dev Genes Evol 1987, 196:158-164.