Sipuncula: An emerging model of spiralian development and evolution

International Journal of Developmental Biology

Volumn 58, Issue 6-8, 2014, Pages 485-499

  Boyle, Michael J ^a   Rice, Mary E ^b  

^a SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^b SMITHSONIAN MARINE STATION   (United States)

Author keywords

Ectomesoderm; Metatroch; Pelagosphera; U shaped; Unequal

Indexed keywords

ARTICLE; ASEXUAL REPRODUCTION; CELL DIVISION; CELL FATE; CELL PROLIFERATION; DEVELOPMENTAL STAGE; ECTODERM; EMBRYO DEVELOPMENT; FOXA GENE; GASTROPOD; GASTRULATION; GATA GENE; GENE; GENE EXPRESSION; HABITAT; LARVAL DEVELOPMENT; LARVAL STAGE; MESODERM; METAMORPHOSIS; MOLECULAR PHYLOGENY; MOLLUSC; NEXT GENERATION SEQUENCING; NONHUMAN; PHYLUM; PRIORITY JOURNAL; SEASONAL VARIATION; SIPUNCULA; TROCHOPHORE; ANATOMY AND HISTOLOGY; ANIMAL; ANIMAL EMBRYO; CELL LINEAGE; CYTOLOGY; EMBRYOLOGY; ENDODERM; EVOLUTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; MORPHOGENESIS; PARTHENOGENESIS; PHYSIOLOGY; POLYCHAETA;

ANNELIDA; METAZOA; NEPHASOMA; PHASCOLION CRYPTUM; SIPUNCULA; SIPUNCULUS NUDUS; SPIRALIA; THEMISTE LAGENIFORMIS;

TRANSCRIPTOME;

ANIMALS; BIOLOGICAL EVOLUTION; BODY PATTERNING; CELL LINEAGE; ECTODERM; EMBRYO, NONMAMMALIAN; ENDODERM; LARVA; MESODERM; PARTHENOGENESIS; POLYCHAETA; TRANSCRIPTOME;

EID: 84919807049     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.140095mb     Document Type: Article

References (101)

1. ÅKESSON, B. (1958). A study of the Nervous System of the Sipunculoideae. With Some Remarks on the Development of the Two Species Phascolion Strombi Montagu and Golfngia Minuta Keferstein. In Undersökningar Över Öresnund XXXVIII. Lunds Universitet. pp. 249.
2. ANDERSON, D.T. (1973). Embryology and phylogeny in annelids and arthropods. Pergamon Press, Oxford, New York.
3. ARENAS-MENA, C. (2006). Embryonic expression of HeFoxA1 and HeFoxA2 in an indirectly developing polychaete. Dev Genes Evol 216: 727-736.
4. ARENDT, D., TECHNAU, U. and WITTBRODT, J. (2001). Evolution of the bilaterian larval foregut. Nature 409: 81-85.
5. BOORE, J.L. and STATON, J.L. (2002). The mitochondrial genome of the Sipunculid Phascolopsis gouldii supports its association with Annelida rather than Mollusca. Mol Biol Evol 19: 127-137.
6. BOYER, B.C., HENRY, J.J. and MARTINDALE, M.Q. (1996). Dual Origins of Me-soderm in a Basal Spiralian: Cell Lineage Analyses in the Polyclad Turbellarian Hoploplana inquilina. Dev Biol 179: 329-338.
7. BOYER, B.C. and HENRY, J.Q. (1998). Evolutionary modifcations of the Spiralian developmental program. Am Zool 38: 621-633.
8. BOYLE, M.J. and SEAVER, E.C. (2008). Developmental expression of foxA and gata genes during gut formation in the polychaete annelid, Capitella sp. I. Evol Dev 10: 89-105.
9. BOYLE, M.J. and SEAVER, E.C. (2010). Expression of FoxA and GATA transcription factors correlates with regionalized gut development in two lophotrochozoan marine worms: Chaetopterus (Annelida) and Themiste lageniformis (Sipuncula). Evodevo 1: 2.
10. BOYLE, M.J., YAMAGUCHI, E. and SEAVER, E.C. (2014). Molecular conservation of metazoan gut formation: evidence from expression of endomesoderm genes in Capitella teleta (Annelida). EvoDevo 5: 39.
11. CHEN, J.Y., BOTTJER, D.J., DAVIDSON, E.H., DORNBOS, S.Q., GAO, X., YANG, Y.H., LI, C.W., LI, G., WANG, X.Q., XIAN, D.C. et al., (2006). Phosphatized polar lobe-forming embryos from the Precambrian of southwest China. Science 312: 1644-1646.
12. CHRISTODOULOU, F., RAIBLE, F., TOMER, R., SIMAKOV, O., TRACHANA, K., KLAUS, S., SNYMAN, H., HANNON, G.J., BORK, P. and ARENDT, D. (2010). Ancient animal microRNAs and the evolution of tissue identity. Nature 463: 1084-1088.
13. CLARK, R.B. (1969). Systematics and Phylogeny: Annelida, Echiura, Sipuncula. Chem Zool 4: 1-68.
14. CLEMENT, A.C. (1962). Development of Ilyanassa following removal of the D quadrant at successive cleavage stages. J Exp Zool 149: 193-216.
15. CONKLIN, E.G. (1897). The embryology of Crepidula. J Morphol 13: 1-226.
16. COSTELLO, D.P. and HENLEY, C. (1976). Spiralian Development: A Perspective. Am Zool 16: 277-291.
17. CUTLER, E.B. (1994). The Sipuncula: their systematics, biology, and evolution. Comstock Pub. Associates, Ithaca.
18. CUTLER, E.B. and CUTLER, N.J. (1988). A revision of the genus Themiste (Sipun-cula). P Biol Soc Wash 101: 741-766.
19. DAVIDSON, E.H., RAST, J.P., OLIVERI, P., RANSICK, A., CALESTANI, C., YUH, C.H., MINOKAWA, T., AMORE, G., HINMAN, V., ARENAS-MENA, C. et al., (2002). A genomic regulatory network for development. Science 295: 1669-1678.
20. DICTUS, W.J. and DAMEN, P. (1997). Cell-lineage and clonal-contribution map of the trochophore larva of Patella vulgata (mollusca). Mech Dev 62: 213-226.
21. DORDEL, J., FISSE, F., PURSCHKE, G. and STRUCK, T.H. (2010). Phylogenetic position of Sipuncula derived from multi-gene and phylogenomic data and its implication for the evolution of segmentation. J Zool Syst Evol Res 48: 197-207.
22. 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. et al., (2008). Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452: 745-749.
23. FREEMAN, G. and LUNDELIUS, J.W. (1992). Evolutionary implications of the mode of D quadrant specifcation in coelomates with spiral cleavage. J Evol Biol 5: 205-247.
24. GEROULD, J.H. (1906). The Development of Phascolosoma (Studies on the embryology of the Sipunculidae II). Zoologische Jahrbücher Abteilung Für Anatomie Und Ontogenie Der Tiere 23: 77-162.
25. HANNIBAL, R.L. and PATEL, N.H. (2013). What is a segment? Evodevo 4: 35.
26. HATSCHEK, B. (1883). Ueber Entwicklung von Sipunculus nudus. In Arbeiten aus dem Zoologischen Institute der Universität-Wien und der Zoologischen Station in Triest, vol. 5 (ed. CLAUS, D.C.). Alfred Hölder, Wien, pp. 61-140.
27. HEJNOL, A. (2010). A twist in time-the evolution of spiral cleavage in the light of animal phylogeny. Integr Comp Biol 50: 695-706.
28. HEJNOL, A. and MARTINDALE, M.Q. (2008). Acoel development indicates the independent evolution of the bilaterian mouth and anus. Nature 456: 382-386.
29. HEJNOL, A., MARTINDALE, M.Q. and HENRY, J.Q. (2007). High-resolution fate map of the snail Crepidula fornicata: the origins of ciliary bands, nervous system, and muscular elements. Dev Biol 305: 63-76.
30. HENRY, J.J. (2002). Conserved Mechanism of Dorsoventral Axis Determination in Equal-Cleaving Spiralians. Dev Biol 248: 343-355.
31. HENRY, J.J. and MARTINDALE, M.Q. (1998). Conservation of the spiralian developmental program: cell lineage of the nemertean, Cerebratulus lacteus. Dev Biol 201: 253-269.
32. HENRY, J.Q. and MARTINDALE, M.Q. (1999). Conservation and innovation in spiralian development. Hydrobiologia 402: 255-265
33. HUANG, D.Y., CHEN, J.Y., VANNIER, J. and SAIZ SALINAS, J.I. (2004). Early Cambrian sipunculan worms from southwest China. Proc Biol Sci 271: 1671-1676.
34. HUANG, F.Z., KANG, D., RAMIREZ-WEBER, F.A., BISSEN, S.T. and WEISBLAT, D.A. (2002). Micromere lineages in the glossiphoniid leech Helobdella. Development 129: 719-732.
35. IRVINE, S.Q., CHAGA, O. and MARTINDALE, M.Q. (1999). Larval Ontogenetic Stages of Cheatopterus: Developmental Heterochrony in the Evolution of Chaetopterid Polychaetes. The Biol Bull 197: 319-331.
36. JÄGERSTEN, G. (1972). Evolution of the Metazoan Life Cycle. Academic Press, London.
37. JENNER, R.A. and WILLS, M.A. (2007). The choice of model organisms in evo-devo. Nat Rev Genet 8: 311-319.
38. KAWAUCHI, G.Y., SHARMA, P.P. and GIRIBET, G. (2012). Sipunculan phylogeny based on six genes, with a new classifcation and the descriptions of two new families. Zool Scr 41: 186-210.
39. KRISTOF, A., WOLLESEN, T., MAIOROVA, A.S. and WANNINGER, A. (2011). Cellular and muscular growth patterns during sipunculan development. J Exp Zool Part B 316B: 227-240.
40. KRISTOF, A., WOLLESEN, T. and WANNINGER, A. (2008). Segmental mode of neural patterning in sipuncula. Curr Biol 18: 1129-1132.
41. LAMBERT, J.D. (2007). Mesoderm in spiralians: the organizer and the 4d cell. J Exp Zool Part B 310: 15-23.
42. LAMBERT, J.D. (2010). Developmental patterns in spiralian embryos. Curr Biol 20: R72-77.
43. LAMBERT, J.D., CHAN, X.Y., SPIECKER, B. and SWEET, H.C. (2010). Characterizing the embryonic transcriptome of the snail ilyanassa. Integr Comp Biol 50: 768-777.
44. LAPRAZ, F., RAWLINSON, K.A., GIRSTMAIR, J., TOMICZEK, B., BERGER, J., JEKELY, G., TELFORD, M.J. and EGGER, B. (2013). Put a tiger in your tank: the polyclad fatworm Maritigrella crozieri as a proposed model for evo-devo. Evodevo 4: 29.
45. MADURO, M.F. (2009). Structure and evolution of the C. elegans embryonic endo-mesoderm network. Biochim Biophys Acta 1789: 250-260.
46. MADURO, M.F. and ROTHMAN, J.H. (2002). Making worm guts: the gene regulatory network of the Caenorhabditis elegans endoderm. Dev Biol 246: 68-85.
47. MARTINDALE, M.Q. and HENRY, J.Q. (1995). Modifcations of cell fate specifcation in equal-cleaving nemertean embryos: alternate patterns of spiralian development. Development 121: 3175-3185.
48. MARTINDALE, M.Q., PANG, K. and FINNERTY, J.R. (2004). Investigating the origins of triploblasty: ‘mesodermal’ gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 131: 2463-2474.
49. MASLAKOVA, S.A., MARTINDALE, M.Q. and NORENBURG, J.L. (2004). Fundamental properties of the spiralian developmental program are displayed by the basal nemertean Carinoma tremaphoros (Palaeonemertea, Nemertea). Dev Biol 267: 342-360.
50. MCHUGH, D. (1997). Molecular evidence that echiurans and pogonophorans are derived annelids. P Natl Acad Sci USA 94: 8006-8009.
51. MEAD, A.D. (1897). The Early Development of Marine Annelids. J Morphol XIII: 227-327.
52. MEYER, N.P., BOYLE, M.J., MARTINDALE, M.Q. and SEAVER, E.C. (2010). A comprehensive fate map by intracellular injection of identifed blastomeres in the marine polychaete Capitella teleta. Evodevo 1: 8.
53. MEYER, N.P. and SEAVER, E.C. (2010). Cell Lineage and Fate Map of the Primary Somatoblast of the Polychaete Annelid Capitella teleta. Integr Comp Biol 50: 756-767.
54. MUELLER, M. (1850). Uber eine den Sipunculiden verwandte Wurmlarve. Archiv für Anatomie, Physiologie, und wissenschlaftliche Medizin 438-451.
55. NEWBY, W.W. (1932). The Early Embryology of the Echiuroid, Urechis. Biol Bull 63.
56. NEWMARK, P.A. and SANCHEZ ALVARADO, A. (2002). Not your father’s planarian: a classic model enters the era of functional genomics. Nat Rev Genet 3: 210-219.
57. NIELSEN, C. (2012). Animal evolution: interrelationships of the living phyla. Oxford University Press, New York.
58. OLIVERI, P., WALTON, K.D., DAVIDSON, E.H. and MCCLAY, D.R. (2006). Repression of mesodermal fate by foxa, a key endoderm regulator of the sea urchin embryo. Development 133: 4173-4181.
59. PETER, I.S. and DAVIDSON, E.H. (2011). A gene regulatory network controlling the embryonic specifcation of endoderm. Nature 474: 635-639.
60. PILGER, J.F. (1987). Reproductive biology and development of Themiste lageniformis, a parthenogenic sipunculan. B Mar Sci 41: 59-67.
61. PURSCHKE, G. (2002). On the ground pattern of Annelida. Org Divers Evol 2: 181-196.
62. RAWLINSON, K.A. (2010). Embryonic and post-embryonic development of the polyclad fatworm Maritigrella crozieri; implications for the evolution of spiralian life history traits. Front Zool 7: 12.
63. RICE, M.E. (1967). A Comparative Study of the Development of Phascolosoma agassizii, Golfngia pugettensis, and Themiste pyroides with a Discussion of Develpmental Patterns in the Sipuncula. Ophelia 4: 143-171.
64. RICE, M.E. (1970). Asexual reproduction in a sipunculan worm. Science 167: 1618-1620.
65. RICE, M.E. (1973). Morphology, behavior, and histogenesis of the pelagosphera larva of Phascolosoma agassizii (Sipuncula). In Smithsonian Contributions to Zoology, No. 132. Smithsonian Institution Press, Washington, pp.1-51.
66. RICE, M.E. (1975a). Observations on the Development of Six Species of Caribbean Sipuncula with a Review of Development in the Phylum. In Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura Vol. I (ed. RICE, M. E. and TODOROVÍC, M.), Naučno Delo Press, Belgrade, pp. 35-49.
67. RICE, M.E. (1975b). Sipuncula. In Reproduction of Marine Invertebrates: Entoprocts and Lesser Coelomates, vol. 2 (ed. GIESE, A. C. and PEARSE, J. S.). Academic Press, New York, pp.67-127.
68. RICE, M.E. (1976). Larval Development and Metamorphosis in Sipuncula. Am Zool 16: 563-571.
69. RICE, M.E. (1981). Larvae Adrift: Patterns and Problems in Life Histories of Sipun-culans. Am Zool 21: 605-619.
70. RICE, M.E. (1985). Sipuncula: developmental evidence for phylogenetic inference. In The origins and relationships of lower invertebrates, vol. 28 (ed. MORRIS, S. C.GEORGE, J. D.GIBSON, R. and PLATT, H. M.). Oxford University Press, USA, pp.400.
71. RICE, M.E. (1988). Observations on development and metamorphosis of Siphono-soma cumanense with comparative remarks on Sipunculus nudus (Sipuncula, Sipunculidae). B Mar Sci 42: 1-15.
72. RICE, M.E. (1989). Comparative observations of gametes, fertilization, and maturation in sipunculans. In 23rd European Biology Symposium. Olsen and Olsen, Fredensborg, Denmark, pp. 167-182.
73. RICE, M.E. (1993). Sipuncula. In Microscopic Anatomy of Invertebrates, Vol. 12: Onychophora, Chilopoda, and Lesser Protostomata., vol. 12 (ed. HARRISON, F. W. and RICE, M. E.). Wiley-Liss, New York, pp.274-296.
74. RIESGO, A., ANDRADE, S.C., SHARMA, P.P., NOVO, M., PEREZ-PORRO, A.R., VAHTERA, V., GONZALEZ, V.L., KAWAUCHI, G.Y. and GIRIBET, G. (2012). Comparative description of ten transcriptomes of newly sequenced invertebrates and effciency estimation of genomic sampling in non-model taxa. Front Zool 9: 33.
75. RÖTTINGER, E., DAHLIN, P. and MARTINDALE, M.Q. (2012). A framework for the establishment of a cnidarian gene regulatory network for “endomesoderm” specifcation: the inputs of ss-catenin/TCF signaling. PLoS Genet 8: e1003164.
76. ROUSE, G.W. (1999). Trochophore concepts: ciliary bands and the evolution of larvae in spiralian Metazoa. Biol J Linn Soc 66: 411-464.
77. ROUSE, G.W. (2000). Polychaetes have evolved feeding larvae numerous times. B Mar Sci 67: 391-409.
78. ROUSE, G.W. and FAUCHALD, K. (1997). Cladistics and polychaetes. Zool Scr 26: 139-204.
79. RUPPERT, E.E. and RICE, M.E. (1983). Structure, ultrastructure, and function of the terminal organ of a pelagosphera larva (Sipuncula). Zoomorphology 102: 143-163.
80. SCHELTEMA, R.S. and HALL, J.R. (1975). The dispersal of pelagosphaera larvae by ocean currents and the geographical distrubution of sipunculans. In Proceedings of The International Symposium on the Biology of the Sipunculan and Echiura vol. 1 (ed. RICE, M. E. and TODOROVÍC, M.), Naučno Delo Press, Belgrade, pp. 103-115.
81. SCHELTEMA, R.S. and RICE, M.E. (1990). Occurrence of teleplanic pelagosphera larvae of sipunculans in tropical regions of the Pacifc and Indian Oceans. B Mar Sci f47: 159-181.
82. SCHULZE, A., CUTLER, E.B. and GIRIBET, G. (2007). Phylogeny of sipunculan worms: A combined analysis of four gene regions and morphology. Mol Phylo-genet Evol 42: 171-192.
83. SCHULZE, A. and RICE, M.E. (2009a). Musculature in sipunculan worms: ontogeny and ancestral states. Evol Dev 11: 97-108.
84. SCHULZE, A. and RICE, M.E. (2009b). Nephasoma pellucidum: A Model Species for Sipunculan Development. In Smithsonian Contributions to Marine Science, vol. 38. Smithsonian Institution Scholarly Press, Washington, pp. 209-217.
85. SEAVER, E.C. (2003). Segmentation: mono- or polyphyletic? Int J Dev Biol 47: 583-595.
86. SELENKA, E. (1875). Eifurchung und larvenbildung von Phascolosoma elongatum Kef. Zeitschrift fur wissenschaftliche zoologie 25: 442-450.
87. SIMAKOV, O., MARLETAZ, F., CHO, S.J., EDSINGER-GONZALES, E., HAVLAK, P., HELLSTEN, U., KUO, D.H., LARSSON, T., LV, J., ARENDT, D. et al., (2012). Insights into bilaterian evolution from three spiralian genomes. Nature 493: 526-531
88. STEPHEN, A.C. and EDMONDS, S.J. (1972). The Phyla Sipuncula and Echiura. Trustees of the British Museum (Natural History), London.
89. STRATHMANN, R.R. (1978). The Evolution and Loss of Feeding Larval Stages of Marine Invertebrates. Evolution 32: 894-906.
90. STRUCK, T.H., SCHULT, N., KUSEN, T., HICKMAN, E., BLEIDORN, C., MCHUGH, D. and HALANYCH, K.M. (2007). Annelid phylogeny and the status of Sipuncula and Echiura. BMC Evol Biol 7: 57.
91. STRUCK, T.H., PAUL, C., HILL, N., HARTMANN, S., HOSEL, C., KUBE, M., LIEB, B., MEYER, A., TIEDEMANN, R., PURSCHKE, G. et al., (2011). Phylogenomic analyses unravel annelid evolution. Nature 471: 95-U113.
92. SURFACE, F.A. (1907). The early development of a polyclad, Planocera inquilina. Proc Acad Nat Sc Phila 59: 514-559.
93. TORREY, J.C. (1903). The early embryology of Thalassema mellita (Conn.). Ann NY Acad Sci 14: 165-246.
94. TREADWELL, A.L. (1901). The Cytogeny of Podarke obscura Verrill. J Morphol 17: 399-476.
95. VALENTINE, J.W. (1997). Cleavage patterns and the topology of the metazoan tree of life. Proc Nat Acad Sci USA 94: 8001-8005.
96. VAN DEN BIGGELAAR, J.A.M., DICTUS, W.J.A.G. and VAN LOON, A.E. (1997). Cleavage patterns, cell-lineages and cell specifcation are clues to phyletic lineages in Spiralia. Semin Cell Dev Biol 8: 367-378.
97. WANNINGER, A., KOOP, D., BROMHAM, L., NOONAN, E. and DEGNAN, B.M. (2005). Nervous and muscle system development in Phascolion strombus (Sipuncula). Dev Genes Evol 215: 509-518.
98. WANNINGER, A., KRISTOF, A. and BRINKMANN, N. (2009). Sipunculans and segmentation. Commun Integr Biol 2: 56-59.
99. WEIGERT, A., HELM, C., MEYER, M., NICKEL, B., ARENDT, D., HAUSDORF, B., SANTOS, S.R., HALANYCH, K.M., PURSCHKE, G., BLEIDORN, C. et al., (2014). Illuminating the Base of the Annelid Tree Using Transcriptomics. Mol Biol Evol.
100. WILSON, E.B. (1892). The cell-lineage of Nereis. J Morphol VI: 361-478.
101. WOLTERECK, R. (1904). Beiträge zur praktischen Analyse der Polygordius-Ent-wicklung nach dem “Nordsee-” und dem “Mittelmeer-Typus”. Arch EntwMech Org 18: 377-403.