Larval Development of Phoronis pallida (Phoronida): Implications for Morphological Convergence and Divergence among Larval Body Plans

Journal of Morphology

Volumn 259, Issue 3, 2004, Pages 347-358

  Santagata, Scott ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b SMITHSONIAN MARINE STATION   (United States)

Author keywords

Actinotroch; Competence; Larval development; Lophotrochozoa; Muscle; Phoronida

Indexed keywords

ANIMAL; ANIMAL EMBRYO; ARTICLE; COMPARATIVE STUDY; CYTOLOGY; EMBRYO DEVELOPMENT; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; INVERTEBRATE; LARVA; PRENATAL DEVELOPMENT;

ANIMALS; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; INVERTEBRATES; LARVA;

BRACHIOPODA; LOPHOTROCHOZOA; PHORONIFORMEA; PHORONIS; PHORONIS PALLIDA; PHORONIS VANCOUVERENSIS;

EID: 1542289720     PISSN: 03622525     EISSN: None     Source Type: Journal    
DOI: 10.1002/jmor.10205     Document Type: Article

References (74)

1. Arendt D, Technau U, Wittbrodt J. 2001. Evolution of the bilaterian larval foregut. Nature 409:81-85.
2. Bartolomaeus T. 2001. Ultrastructure and formation of the body cavity lining in Phoronis muelleri (Phoronida, Lophophorata). Zoomorphology 120:135-148.
3. Basch LV, Pearse JS. 1996. Consequences of larval feeding environment for settlement and metamorphosis of a temperate echinoderm. Oceanol Acta 19:273-285.
4. Brooks WK, Cowles RP. 1905. Phoronis architecta: its life history, anatomy and breeding habits. Mem Natl Acad Sci Wash 10:71-148.
5. Clark G. 1981. Staining procedures. Baltimore: Williams & Wilkins.
6. Cohen BL. 2000. Monophyly of brachiopods and phoronids: Reconciliation of molecular evidence with Linnaean classification (the subphylum Phoroniformea nov.). Proc R Soc Lond B Biol Sci 267:225-231.
7. Cohen BL, Gawthrop A, Cavalier-Smith T. 1998. Molecular phylogeny of brachiopods and phoronids based on nuclear-encoded small subunit ribosomal RNA gene sequences. Philos Trans R Soc Lond B Biol Sci 353:2039-2061.
8. de Rosa R, Grenier JK, Andreeva T, Cook CE, Adoutte A, Akam M, Carroll SB, Balavoine G. 1999. Hox genes in brachiopods and priapulids and protostome evolution. Nature 399:772-776.
9. Emig CC. 1974. The systematics and evolution of the phylum Phoronida. Z Zool Syst Evol Forsch 12:128-151.
10. Emig CC. 1982. The biology of Phoronida. Adv Mar Bio 19:1-89.
11. Emlet RB. 1991. Functional constraints on the evolution of larval forms of marine invertebrates: experimental and comparative evidence. Am Zool 31:707-725.
12. Erber A, Riemer D, Bovenschulte M, Weber K. 1998. Molecular phylogeny of metazoan intermediate filament proteins. J Mol Evol 47:751-762.
13. Freeman G. 1991. The bases for and timing of regional specification during larval development in Phoronis. Dev Biol 147:157-173.
14. Freeman G. 1993. Regional specification during embryogenesis in the articulate brachiopod Terebratalia. Dev Biol 160:196-213.
15. Freeman G. 1999. Regional specification during embryogenesis in the inarticulate brachiopod Discinisca. Dev Biol 209:321-339.
16. Freeman G. 2000. Regional specification during embryogenesis in the craniiform brachiopod Crania anomala. Dev Biol 227:219-238.
17. Freeman G, Lundelius JW. 1999. Changes in the timing of mantle formation and larval life history traits in linguliform and craniiform brachiopods. Lethaia 32:197-217.
18. Freeman G, Martindale MQ. 2002. The origin of mesoderm in phoronids. Dev Biol 252:301-311.
19. Galis F, Sinervo B. 2002. Divergence and convergence in early embryonic stages of metazoans. Contrib Zool 71:101-113.
20. Gilmour THJ. 1978. Ciliation and function of food-collecting and waste-rejecting organs of lophophorates. Can J Zool 56:2142-2155.
21. Hadfield MG, Carpizo-Ituarte EJ, del Carmen K, Nedved BT. 2001. Metamorphic competence, a major adaptive convergence in marine invertebrate larvae. Am Zool 41:1123-1131.
22. Halanych KM, Bacheller JD, Aguinaldo AMA, Liva SM, Hillis DM, Lake JA. 1995. Evidence from 18S ribosomal DNA that the lophophorates are protostome animals. Science 267:1641-1643.
23. Hay-Schmidt A. 1989. The nervous system of the actinotroch larva of Phoronis muelleri (Phoronida). Zoomorphology 108: 333-351.
24. Henry JJ, Martindale MQ. 1999. Conservation and innovation in spiralian development. Hydrobiologia 402:255-265.
25. Henry JQ, Martindale MQ, Boyer BC. 2000. The unique developmental program of the acoel flatworm, Neochildia fusca. Dev Biol 220:285-295.
26. Herrmann K. 1979. Larval development and metamorphosis of Phoronis psammophila (Phoronida, Tentaculata). Helgoländer Wiss Meer 32:550-581.
27. Herrmann K. 1986. Die ontogenese von Phoronis müelleri (Tentaculata) unter besonderer berücksichtigung der mesodermdifferenzierung und phylogenese des coeloms. Zool Jahrb Anat Ontog 114:441-463.
28. Herrmann K. 1995. Induction and regulation of metamorphosis in planktonic larvae: Phoronis muelleri (Tentaculata) as archetype. Helgoländer Meeresun 49:255-281.
29. Hooge MD. 2001. Evolution of body-wall musculature in the Platyhelminthes (Acoelomorpha, Catenulida, Rhabditophora). J Morphol 249:171-194.
30. Ikeda IR. 1901. Observations on the development, structure, and metamorphosis of Actinotrocha. J Coll Sci Imp Univ Tokyo 13:507-591.
31. Jacobs DK, Gates RD. 2003. Developmental genes and the reconstruction of metazoan evolution - implications of evolutionary loss, limits on inference of ancestry, and type 2 errors. Integr Comp Biol 43:11-18.
32. Lacalli TC. 1990. Structure and organization of the nervous system in the actinotroch larva of Phoronis vancouverensis. Philos Trans R Soc Lond B Biol Sci 327:655-683.
33. Ladurner P, Rieger R. 2000. Embryonic muscle development of Convoluta pulchra (Turbellaria-Acoelomorpha, Platyhelminthes). Dev Biol 222:359-375.
34. Lartillot N, Le Gouar M, Adoutte A. 2002. Expression patterns of fork head and goosecoid homologues in the mollusc Patella vulgata supports the ancestry of the anterior mesendoderm across Bilateria. Dev Genes Evol 212:551-561.
35. Lee PN, Callaerts P, de Couet HG, Martindale MQ. 2003. Cephalopod hox genes and the origin of morphological novelties. Nature 424:1061-1065.
36. Long JA, Stricker SA. 1991. Brachiopoda. In: Giese AC, Pearse JS, Pearse VB, editors. Reproduction of marine invertebrates, vol. VI. Echinoderms and lophophorates. Pacific Grove, CA: Boxwood Press. p 47-84.
37. Luter C. 2000. The origin of the coelom in Brachiopoda and its phylogenetic significance. Zoomorphology 120:15-28.
38. Malakov VV, Temereva EN. 1999. Embryonic development of the phoronid Phoronis ijimai (Lophophorata, Phoronida): Two sources of coelomic mesoderm. Dokl Akad Nauk 365:574-576.
39. Mangel M, Stamps J. 2001. Trade-offs between growth and mortality and the maintenance of individual variation in growth. Evol Ecol Res 3:583-593.
40. Nederbragt AJ, Lespinet O, van Wageningen S, van Loon AE, Adoutte A, Dictus W. 2002. A lophotrochozoan twist gene is expressed in the ectomesoderm of the gastropod mollusk Patella vulgata. Evol Devo 4:334-343.
41. Nielsen C. 1987. Structure and function of metazoan ciliary bands and their phylogenetic significance. Acta Zool 68:205-262.
42. Nielsen C. 1991. The development of the brachiopod Crania (Neocrania) anomala (Muller,o.F.) and its phylogenetic significance. Acta Zool 72:7-28.
43. Nielsen C. 2002. The phylogenetic position of Entoprocta, Ectoprocta, Phoronida, and Brachiopoda. Integr Comp Biol 42:685-691.
44. Nielsen MG, Popodi E, Minsuk S, Raff RA. 2003. Evolutionary convergence in Otx expression in the pentameral adult rudiment in direct-developing sea urchins. Dev Genes Evol 213:73-82.
45. O'Laughlin BE, Harris RN. 2000. Models of metamorphic timing: An experimental evaluation with the pond dwelling salamander Hemidactylium scutatum (Caudata: Plethodontidae). Oecologia 124:343-350.
46. Paine RT. 1963. Ecology of the brachiopod Glottidia pyramidata. Ecol Mono 33:187-213.
47. Popescu IR, Frost WN. 2002. Highly dissimilar behaviors mediated by a multifunctional network in the marine mollusk Tritonia diomedea. J Neurosci 22:1985-1993.
48. Reed CG, Ninos JM, Woollacott RM. 1988. Bryozoan larvae as mosaics of multifunctional ciliary fields: ultrastructure of the sensory organs of Bugula stolonifera (Cheilostomata, Cellularioidea). J Morphol 197:127-145.
49. Reiter D, Boyer B, Ladurner P, Mair G, Salvenmoser W, Rieger R. 1996. Differentiation of the body wall musculature in Macrostomum hystricinum marinum and Hoploplana inquilina (Plathelminthes), as models for muscle development in lower Spiralia. Roux's Arch Dev Bio 205:410-423.
50. Rieger RM, Ladurner P. 2003. The significance of muscle cells for the origin of mesoderm in Bilateria. Integr Comp Biol 43:47-54.
51. Riisgard HU. 2002. Methods of ciliary filter feeding in adult Phoronis muelleri (phylum Phoronida) and in its free-swimming actinotroch larva. Mar Bio 141:75-87.
52. Ruppert EE. 1991. Introduction to the aschelminth phyla: a consideration of mesoderm, body cavities, and cuticle. In: Harrison FW, Ruppert EE, editors. Microscopic anatomy of invertebrates, vol. 4. Aschelminths. New York: Wiley-Liss. p 1-17.
53. Santagata S. 2001. The larval development, settlement, and metamorphosis of Phoronis pallida. Ph.D. thesis, Los Angeles: University of Southern California.
54. Santagata S. 2002. Structure and metamorphic remodeling of the larval nervous system and musculature of Phoronis pallida (Phoronida). Evol Dev 4:28-42.
55. Santagata S, Zimmer RL. 2002. Comparison of the neuromuscular systems among actinotroch larvae: systematic and evolutionary implications. Evol Dev 4:43-54.
56. Schneider A. 1862. Ueber die metamorphose der Actinotrocha branchiata. Arch Anat Physiol:47-65.
57. Selys-Longchamps M de 1903. Ueber Phoronis und Actinotrocha bei Helgoland. Helgoländer Wiss Meer 6:1-55.
58. Selys-Longchamps M de 1907. Phoronis. Fauna und Flora des Golfes von Neapel 30:280.
59. Silén L. 1954. Developmental biology of the Phoronidea of the Gullmar Fiord area (west coast of Sweden). Acta Zool (Stockh) 35:215-257.
60. Staver JM, Strathmann RR. 2002. Evolution of fast development of planktonic embryos to early swimming. Biol Bull 203:58-69.
61. Strathmann RR. 1993. Hypotheses on the origins of marine larvae. Annu Rev Ecol Syst 24:89-117.
62. Strathmann RR. 2000. Functional design in the evolution of embryos and larvae. Semin Cell Dev Biol 11:395-402.
63. Strathmann RR, Bone Q. 1997. Ciliary feeding assisted by suction from the muscular oral hood of phoronid larvae. Biol Bull 193:153-162.
64. Strathmann RR, Staver JM, Hoffman JR. 2002. Risk and the evolution of cell-cycle durations of embryos. Evolution 56:708-720.
65. Telford MJ, Lockyer AE, Cartwright-Finch C, Littlewood DTJ. 2003. Combined large and small subunit ribosomal RNA phylogenies support a basal position of the acoelomorph flatworms. Proc R Soc Lond B Biol Sci 270:1077-1083.
66. Tessmar-Raible K, Arendt D. 2003. Emerging systems: between vertebrates and arthropods, the Lophotrochozoa. Curr Opin Genet Dev 13:331-340.
67. Tyler S, Rieger RM. 1999. Functional morphology of musculature in the acoelomate worm, Convoluta pulchra (Plathelminthes). Zoomorphology 119:127-141.
68. Wanninger A, Haszprunar G. 2002. Chiton myogenesis: perspectives for the development and evolution of larval and adult muscle systems in molluscs. J Morphol 251:103-113.
69. Wray GA, Strathmann RR. 2002. Stasis, change, and functional constraint in the evolution of animal body plans, whatever they may be. Vie Milieu 52:189-199.
70. Yatsu N. 1902. On the development of Lingula anatina. J Coll Sci Imp Univ Tokyo 17:1-112.
71. Zimmer RL. 1964. Reproductive biology and development of Phoronida. Ph.D. thesis, Seattle: University of Washington.
72. Zimmer RL. 1980. Mesoderm proliferation and formation of the protocoel and metacoel in early embryos of Phoronis vacouverensis (Phoronida). Zool Jahrb Anat Ontog 103:219-233.
73. Zimmer RL. 1987. Phylum Phoronida. In: Strathmann MF, editor. Reproduction and development of marine invertebrates of the northern Pacific coast: data and methods for the study of eggs, embryos, and larvae. Seattle: University of Washington Press. p 476-485.
74. Zrzavy' J. 2003. Gastrotricha and metazoan phylogeny. Zool Scr 32:61-81.