Co-option and dissociation in larval origins and evolution: The sea urchin larval gut

Evolution and Development

Volumn 10, Issue 1, 2008, Pages 74-88

  Love, Alan C ^a,b   Lee, Abigail E ^a   Andrews, Mary E ^a   Raff, Rudolf A ^a,c  

^a INDIANA UNIVERSITY   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BETAINE HOMOCYSTEINE METHYLTRANSFERASE; FLOTILLINS; MEMBRANE PROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG;

BENTHOS; ECHINODERM; EVOLUTION; FEEDING; GENE EXPRESSION; LARVA; METAZOAN; MORPHOLOGY; ORIGIN OF LIFE;

ANIMAL; ARTICLE; CHEMISTRY; COMPARATIVE STUDY; DEVELOPMENTAL GENE; DNA SEQUENCE; EVOLUTION; FEEDING BEHAVIOR; GASTROINTESTINAL TRACT; GASTRULA; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; IN SITU HYBRIDIZATION; LARVA; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SEA URCHIN;

ANIMALS; BETAINE-HOMOCYSTEINE S-METHYLTRANSFERASE; CLONING, MOLECULAR; EVOLUTION; FEEDING BEHAVIOR; GASTROINTESTINAL TRACT; GASTRULA; GENE EXPRESSION; GENES, DEVELOPMENTAL; IN SITU HYBRIDIZATION; LARVA; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; RNA, MESSENGER; SEA URCHINS; SEQUENCE ANALYSIS, DNA;

DEUTEROSTOMIA; ECHINOIDEA; HELIOCIDARIS TUBERCULATA; INVERTEBRATA; METAZOA;

EID: 37749038377     PISSN: 1520541X     EISSN: 1525142X     Source Type: Journal    
DOI: 10.1111/j.1525-142X.2007.00215.x     Document Type: Article

References (125)

1. Aitken, A., et al. 2002. Specificity of 14-3-3 isoform dimer interactions and phosphorylation. Biochem. Soc. Trans. 30 : 351 360.
2. Angerer, L. M. Angerer, R. C. 2000. Animal-vegetal axis patterning mechanisms in the early sea urchin embryo. Dev. Biol. 18 : 1 12.
3. Arendt, D., Technau, U. Wittbrodt, J. 2001. Evolution of the bilaterian larval foregut. Nature 409 : 81 85.
4. Baron, W., Decker, L., Colognato, H. ffrench-Constant, C. 2003. Regulation of integrin growth factor interactions in oligodendrocytes by lipid raft microdomains. Curr. Biol. 13 : 151 155.
5. Benton, R., Palacios, I. M. St Johnston, D. 2002. Drosophila 14-3-3/par-5 is an essential mediator of par-1 function in axis formation. Dev. Cell 3 : 659 671.
6. Bickel, P. E., Scherer, P. E., Schnitzer, J. E., Oh, P., Lisanti, M. P. Lodish, H. F. 1997. Flotillin and epidermal surface antigen define a new family of caveolae-associated integral membrane proteins. J. Biol. Chem. 272 : 13793 13802.
7. Bisgrove, B. W., Andrews, M. E. Raff, R. A. 1995. Evolution of the Fibropellin gene family and patterns of Fibropellin gene expression in sea urchin phylogeny. J. Mol. Evol. 41 : 34 45.
8. Bisgrove, B. W. Raff, R. A. 1993. The SpEGF III gene encodes a member of the Fibropellins: EGF repeat-containing proteins that form the apical lamina of the sea urchin embryo. Dev. Biol. 157 : 526 538.
9. Bishop, C. D. Brandhorst, B. P. 2003. On nitric oxide signaling, metamorphosis, and the evolution of biphasic life cycles. Evol. Dev. 5 : 542 550.
10. Bork, P. Beckmann, G. 1993. The CUB domain: a widespread module in developmentally regulated proteins. J. Mol. Biol. 231 : 539 545.
11. Bork, P. Sander, C. 1992. A large domain common to sperm receptors (ZP2 and ZP3) and TGF-β type III receptor. FEBS Lett. 300 : 237 240.
12. Bunney, T. D., De Boer, A. H. Levin, M. 2003. Fusicoccin signaling reveals 14-3-3 protein function as a novel step in left-right patterning during amphibian embryogenesis. Development 130 : 4847 4858.
13. Burke, R. D. 1981. Structure of the digestive tract of the pluteus larva of Dendraster excentricus (Echinodermata: Echinoida). Zoomorphology 98 : 209 225.
14. Cameron, R. A., Zeller, R. W., Coffman, J. A. Davidson, E. H. 1996. The analysis of lineage-specific gene activity during sea urchin development. In J. D. Ferraris S. R. Palumbi (eds.). Molecular Zoology: Advances, Strategies, and Protocols. Wiley-Liss Inc, New York, pp. 221 243.
15. Chen, D., et al. 1999. Cloning and uterus/oviduct-specific expression of a novel estrogen-regulated gene (ERG1). J. Biol. Chem. 274 : 32215 32224.
16. Chen, S. W. Wessel, G. M. 1996. Endoderm differentiation in vitro identifies a transitional period for endoderm ontogeny in the sea urchin embryo. Dev. Biol. 175 : 57 65.
17. Chia, F.-S. Burke, R. D. 1978. Echinoderm metamorphosis: fate of larval structures. In F. -S. Chia M. E. Rice (eds.). Settlement and Metamorphosis of Marine Invertebrate Larvae. Elsevier, New York, pp. 219 234.
18. Chomcynski, P. Sacchi, N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162 : 156 159.
19. Coffman, J. A., Dickey-Sims, C., Haug, J. S., McCarthy, J. J. Robertson, A. J. 2004. Evaluation of developmental phenotypes produced by morpholino antisense targeting of a sea urchin RUNX gene. BMC Biol. 2 : 6.
20. Croce, J., Lhomond, G. Gache, C. 2001. Expression pattern of brachyury in the embryo of the sea urchin Paracentrotus lividus. Dev. Genes Evol. 211 : 617 619.
21. Davidson, E. H., Cameron, R. A. Ransick, A. 1998. Specification of cell fate in the sea urchin embryo: summary and some proposed mechanisms. Development 125 : 3269 3290.
22. Davidson, E. H., Peterson, K. J. Cameron, R. A. 1995. Origin of bilaterian body plans: evolution of developmental regulatory mechanisms. Science 270 : 1319 1325.
23. Davidson, E. H., et al. 2002. A provisional regulatory gene network for specification of endomesoderm in the sea urchin embryo. Dev. Biol. 246 : 162 190.
24. Duboc, V., Röttinger, E., Besnardeau, L. Lepage, T. 2004. Nodal and Bmp2/4 signaling organizes the oral-aboral axis of the sea urchin embryo. Dev. Cell 6 : 397 410.
25. Dunn, W. F., Moy, V. N., Angerer, L. M., Angerer, R. C., Morris, R. L. Peterson, K. J. 2007. Molecular paleoecology: using gene regulatory analysis to address the origins of complex life cycles in the late Precambrian. Evol. Dev. 9 : 10 24.
26. Emlet, R. B. 1988. Larval form and metamorphosis of a "primitive" sea urchin, Eucidaris thouarsi (Echinodermata: Echinoidea Cidaroida), with implications for developmental and phylogenetic studies. Biol. Bull. 174 : 4 19.
27. Emlet, R. B. 1991. Functional constraints on the evolution of larval forms of marine invertebrates: experimental and comparative evidence. Am. Zool. 31 : 707 725.
28. Emlet, R. B. 1994. Body form and patterns of ciliation in nonfeeding larvae of echinoderms: functional solutions to swimming in the plankton? Am. Zool. 34 : 570 585.
29. Emlet, R. B. 1995. Larval spicules, cilia, and symmetry as remnants of indirect development in the direct developing sea urchin Heliocidaris erythrogramma. Dev. Biol. 167 : 405 415.
30. Erwin, D. H. Davidson, E. H. 2002. The last common bilaterian ancestor. Development 129 : 3021 3032.
31. Ettensohn, C. A. 1985. Gastrulation in the sea urchin embryo is accompanied by the rearrangement of invaginating epithelial cells. Dev. Biol. 112 : 383 390.
32. Ferkowicz, M. J. Raff, R. A. 2001. Wnt gene expression in sea urchin development: Heterochronies associated with the evolution of developmental mode. Evol. Dev. 3 : 24 33.
33. Forestier, M., Bänninger, R., Reichen, J. Solioz, M. 2003. Betaine homocysteine methyltransferase: gene cloning and expression analysis in rat liver cirrhosis. Biochem. Biophys. Acta 1638 : 29 34.
34. Fu, H., Subramanian, R. R. Masters, S. C. 2000. 14-3-3 proteins: structure, function, and regulation. Ann. Rev. Pharmacol. Toxicol. 40 : 617 647.
35. Godin, R. E., Klinzing, D. C., Porcaro, W. A. Ernst, S. G. 1997. Specification of endoderm in the sea urchin embryo. Mech. Dev. 67 : 35 47.
36. Gross, J. M. McClay, D. R. 2001. The role of Brachyury (T) during gastrulation movements in the sea urchin Lytechinus variegatus. Dev. Biol. 239 : 132 147.
37. Haag, E. S. Raff, R. A. 1998. Isolation and characterization of three mRNAs enriched in embryos of the direct-developing sea urchin Heliocidaris erythrogramma: evolution of larval ectoderm. Dev. Genes Evol. 208 : 188 204.
38. Haag, E. S., Sly, B. J., Andrews, M. E. Raff, R. A. 1999. Apextrin, a novel extracellular protein associated with larval ectoderm evolution in Heliocidaris erythrogramma. Dev. Biol. 211 : 77 87.
39. Harder, T. Simons, K. 1997. Caveolae, digs, and the dynamics of sphingolipid-cholesterol microdomains. Curr. Opin. Cell Biol. 9 : 534 542.
40. Hardin, J. 1996. The cellular basis of sea urchin gastrulation. In R. A. Pedersen G. P. Schatten (eds.). Current Topics in Developmental Biology. Academic Press, San Diego, pp. 159 262.
41. Hart, M. W. 1996. Evolutionary loss of larval feeding: development, form and function in a facultatively feeding larva, Brisaster latifrons. Evolution 50 : 174 187.
42. Haszprunar, G., Salvini-Plawen, L. V. Rieger, R. M. 1995. Larval planktotrophy - a primitive trait in the bilateria? Acta Zool. 76 : 141 154.
43. Hinman, V. F., Nguyen, A. T., Cameron, R. A. Davidson, E. H. 2003. Developmental gene regulatory network architecture across 500 million years of echinoderm evolution. Proc. Natl. Acad. Sci. USA 100 : 13356 13361.
44. Huynh, H., et al. 2001. Induction of UO-44 gene expression by tamoxifen in the rat uterus and ovary. Endocrinology 142 : 2985 2995.
45. Ishizuka, Y., Minokawa, T. Amemiya, S. 2001. Micromere descendants at the blastula stage are involved in normal archenteron formation in sea urchin embryos. Dev. Genes Evol. 211 : 83 88.
46. Jeffery, C. H., Emlet, R. B. Littlewood, D. T. 2003. Phylogeny and evolution of developmental mode in Temnopleurid echinoids. Mol. Phylogenetics Evol. 28 : 99 118.
47. Jovine, L., Qi, H., Williams, Z., Litscher, E. Wassarman, P. M. 2002. The ZP domain is a conserved module for polymerization of extracellular proteins. Nature Cell Biol. 4 : 457 461.
48. Kasik, J. W. 1998. A cDNA cloned from pregnant mouse uterus exhibits temporo-spatial expression and predicts a novel protein. Biochem. J. 330 : 947 950.
49. Kingsley, P. D., Angerer, L. M. Angerer, R. C. 1993. Major temporal and spatial patterns of gene expression during differentiation of the sea urchin embryo. Dev. Biol. 155 : 216 234.
50. Kissinger, J. C. Raff, R. A. 1998. Evolutionary changes in sites and timing of actin gene expression in embryos of the direct- and indirect-developing sea urchins, Heliocidaris erythrogramma and H. tuberculata. Dev. Genes Evol. 208 : 82 93.
51. Klueg, K. M., Harkey, M. A. Raff, R. A. 1997. Mechanisms of evolutionary changes in timing, spatial expression, and mRNA processing in the msp130 gene in a direct-developing sea urchin, Heliocidaris erythrogramma. Dev. Biol. 182 : 121 133.
52. Kumar, S., Tamura, K., Jakobsen, I. B. Nei, M. 2001. Mega2: molecular evolutionary genetics analysis software. Bioinformatics 17 : 1244 1245.
53. Lee, Y.-H., et al. 1999. EST analysis of gene expression in early cleavage-stage sea urchin embryos. Development 126 : 3857 3867.
54. Leitinger, B. Hogg, N. 2001. The involvement of lipid rafts in the regulation of integrin function. J. Cell Sci. 115 : 963 972.
55. Leong, C. T. C., et al. 2004. Molecular cloning, characterization and isolation of novel spliced variants of the human ortholog of a rat estrogen-regulated membrane-associated protein, UO-44. Oncogene 23 : 5707 5718.
56. Logan, C. Y. McClay, D. R. 1999. Lineages that give rise to endoderm and mesoderm in the sea urchin embryo. In S. A. Moody (ed.). Cell lineage and Fate Determination. Academic Press, San Diego, CA, pp. 41 57.
57. Love, A. C., Andrews, M. E. Raff, R. A. 2007. Gene expression patterns in a novel appendage: the sea urchin pluteus arm. Evol. Dev. 9 : 51 68.
58. Lowe, C. J., Issel-Tarver, L. Wray, G. A. 2002. Gene expression and larval evolution: changing roles of distal-less and orthodenticle in echinoderm larvae. Evol. Dev. 4 : 111 123.
59. Lowe, C. J. Wray, G. A. 1997. Radical alterations in the roles of homeobox genes during echinoderm evolution. Nature 389 : 718 721.
60. Lynch, M., O'Hely, M., Walsh, B. Force, A. 2001. The probability of preservation of a newly arisen gene duplicate. Genetics 159 : 1789 1804.
61. Malinda, K. M., Fisher, G. W. Ettensohn, C. A. 1995. Four-dimensional microscopic analysis of the filopodial behavior of primary mesenchyme cells during gastrulation in the sea urchin embryo. Dev. Biol. 172 : 552 566.
62. Marsden, M. Burke, R. D. 1997. Cloning and characterization of novel β integrin subunits from a sea urchin. Dev. Biol. 181 : 234 245.
63. Marsden, M. Burke, R. D. 1998. The βl integrin subunit is necessary for gastrulation in sea urchin embryos. Dev. Biol. 203 : 134 148.
64. McClay, D. R., Ferkowicz, M. J., Sherwood, D. R. Logan, C. Y. 2000. Specification of mesoderm and endoderm during cleavage in sea urchin embryos. In L. Olsson C. -O. Jacobson (eds.). Regulatory Processes in Development. Portland Press, London, pp. 19 30.
65. McEdward, L. R. 1997. Relationships among development, ecology, and morphology in the evolution of echinoderm larvae and life cycles. Biol. J. Linnean Soc. 60 : 381 400.
66. Miller, J., Fraser, S. E. McClay, D. R. 1995. Dynamics of thin filopodia during sea urchin gastrulation. Development 121 : 2501 2511.
67. Minokawa, T. Amemiya, S. 1999. Timing of the potential of micromere-descendants in echinoid embryos to induce endoderm differentiation of mesomere-descendants. Dev. Growth Differentiation 41 : 535 547.
68. Minsuk, S. B. Raff, R. A. 2002. Pattern formation in a pentameral animal: induction of early adult rudiment development in sea urchins. Dev. Biol. 247 : 335 350.
69. Mitsunaga-Nakatsubo, K., et al. 1998. Arylsulfatase exists as non-enzymatic cell surface protein in sea urchin embryos. J. Exp. Zool. 280 : 220 230.
70. Morrow, I. C., et al. 2002. Flotillin-1/Reggie-2 traffics to surface raft domains via a novel Golgi-independent pathway. J. Biol. Chem. 277 : 48834 48841.
71. Nielsen, C. 1998. Origin and evolution of animal life cycles. Biol. Rev. Cambridge Philos. Soc. 73 : 125 155.
72. Nielsen, M. G., Popodi, E. M., Minsuk, S. Raff, R. A. 2003. Evolutionary convergence in otx expression in the pentameral adult rudiment in direct-developing sea urchins. Dev. Genes Evol. 213 : 73 82.
73. Nielsen, M. G., Wilson, K. A., Raff, E. C. Raff, R. A. 2000. Novel gene expression patterns in hybrid embryos between species with different modes of development. Evol. Dev. 2 : 133 144.
74. Okazaki, K. 1975. Normal development to metamorphosis. In G. Czihak (ed.). The Sea Urchin Embryo: Biochemistry and Morphogenesis. Springer-Verlag, Berlin, pp. 177 232.
75. Olive, P. J. W. 1985. Covariability of reproductive traits in marine invertebrates: implications for the phylogeny of the lower invertebrates. In S. Conway Morris, J. D. George, R. Gibson H. M. Platt (eds.). The Origins and Relationships of Lower Invertebrates. Oxford University Press, Oxford, pp. 42 59.
76. Oliveri, P., Carrick, D. M. Davidson, E. H. 2002. A regulatory gene network that directs micromere specification in the sea urchin embryo. Dev. Biol. 246 : 209 228.
77. Olson, R. R., Cameron, J. L. Young, C. M. 1993. Larval development (with observations on spawning) of the pencil urchin Phyllacanthus imperialis: a new intermediate larval form? Biol. Bull. 185 : 77 85.
78. Parks, A. L., Bisgrove, B. W., Wray, G. A. Raff, R. A. 1989. Direct development in the sea urchin Phyllacanthus parvispinus (Cidaroidea): phylogenetic history and functional modification. Biol. Bull. 177 : 96 109.
79. Peterson, K. J. 2005. Macroevolutionary interplay between planktic larvae and benthic predators. Geology 33 : 929 932.
80. Peterson, K. J., Cameron, R. A. Davidson, E. H. 2000. Bilaterian origins: significance of new experimental observations. Dev. Biol. 219 : 1 17.
81. Peterson, K. J., McPeek, M. A. Evans, D. A. D. 2005. Tempo and mode of early animal evolution: inferences from rocks, Hox, and molecular clocks. Paleobiology 31 (Suppl.) : 36 55.
82. Piatigorsky, J. 1998. Multifunctional lens crystallins and corneal enzymes. Ann. NY Acad. Sci. 842 : 7 15.
83. Raff, E. C., Popodi, E. M., Sly, B. J., Turner, F. R., Villinski, J. T. Raff, R. A. 1999. A novel ontogenetic pathway in hybrid embryos between species with different modes of development. Development 126 : 1937 1945.
84. Raff, R. A. 1992. Direct-developing sea urchins and the evolutionary reorganization of early development. BioEssays 14 : 211 218.
85. Raff, R. A. Sly, B. J. 2000. Modularity and dissociation in the evolution of gene expression territories in development. Evol. Dev. 2 : 102 113.
86. Ransick, A. Davidson, E. H. 1995. Micromeres are required for normal vegetal plate specification in sea urchin embryos. Development 121 : 3215 3222.
87. Ransick, A., Rast, J. P., Minokawa, T., Calestani, C. Davidson, E. H. 2002. New early zygotic regulators expressed in endomesoderm of sea urchin embryos discovered by differential array hybridization. Dev. Biol. 246 : 132 147.
88. Rao, P. V., Garrow, T. A., John, F., Garland, D., Millian, N. S. Zigler, J. S. Jr. 1998. Betaine-homocysteine methyltransferase is a developmentally regulated enzyme crystallin in rhesus monkey lens. J. Biol. Chem. 273 : 30669 30674.
89. Rast, J. P., Cameron, R. A., Poutska, A. J. Davidson, E. H. 2002. Brachyury target genes in the early sea urchin embryo isolated by differential macroarray screening. Dev. Biol. 246 : 191 208.
90. Robertson, A. J., Dickey, C. E., McCarthy, J. J. Coffman, J. A. 2002. The expression of SpRunt during sea urchin embryogenesis. Mech. Dev. 117 : 327 330.
91. Robinson-Rechavi, M. Huchon, D. 2000. RRtree: relative-rate tests between groups of sequences on a phylogenetic tree. Bioinformatics 16 : 296 297.
92. Roseboom, P. H., et al. 1994. Cloning and characterization of the ε and ζ isoforms of the 14-3-3 proteins. DNA Cell Biol. 13 : 629 640.
93. Rosenquist, M., Sehnke, P., Ferl, R. J., Sommarin, M. Larsson, C. 2000. Evolution of the 14-3-3 protein family: does the large number of isoforms in multicellular organisms reflect functional specificity? J. Mol. Evol. 51 : 446 458.
94. Rouse, G. W. 2000. The epitome of hand waving? Larval feeding and hypotheses of metazoan phylogeny. Evol. Dev. 2 : 222 233.
95. Schulte, T., Paschke, K. A., Laessing, U., Lottspeich, F. Stuermer, C. A. O. 1997. Reggie-1 and Reggie2, two cell surface proteins expressed by retinal ganglion cells during axon regeneration. Development 124 : 577 587.
96. Shoguchi, E., Tokuoka, M. Kominami, T. 2002. In situ screening for genes expressed preferentially in secondary mesenchyme cells of sea urchin embryos. Dev. Genes Evol. 212 : 407 418.
97. Simons, K. Toomre, D. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1 : 31 39.
98. Sly, B. J. 2004 The development and evolution of the echinoderm nervous system, PhD thesis. Bloomington: Indiana University. 230pp.
99. Sly, B. J., Hazel, J. C., Popodi, E. M. Raff, R. A. 2002. Patterns of gene expression in the developing adult sea urchin central nervous system reveal multiple domains and deep-seated neural pentamery. Evol. Dev. 4 : 189 204.
100. Sly, B. J., Snoke, M. S. Raff, R. A. 2003. Who came first - larvae or adults? Origins of bilaterian metazoan larvae. Int. J. Dev. Biol. 47 : 623 632.
101. Smith, A. B. 1997. Echinoderm larvae and phylogeny. Annu. Rev. Ecol. Syst. 28 : 219 241.
102. Smith, M. S., Zigler, K. S. Raff, R. A. 2007. Evolution of direct-developing larvae: selection vs loss. BioEssays 29 : 566 571.
103. Strathmann, R. R. 1978. The evolution and loss of feeding larval stages of marine invertebrates. Evolution 32 : 894 906.
104. Strathmann, R. R. 1993. Hypotheses on the origins of marine larvae. Annu. Rev. Ecol. Syst. 24 : 89 117.
105. Strathmann, R. R. 2000. Functional design in the evolution of embryos and larvae. Semin. Cell Dev. Biol. 11 : 395 402.
106. Strathmann, R. R. Eernisse, D. J. 1994. What molecular phylogenies tell us about the evolution of larval forms. Am. Zool. 34 : 502 512.
107. Sunden, S. L. F., Renduchintala, M. S., Park, E. I., Miklasz, S. D. Garrow, T. A. 1997. Betaine-homocysteine methyltransferase expression in porcine and human tissues and chromosomal localization of the human gene. Arch. Biochem. Biophys. 345 : 171 174.
108. van Hemert, M. J., Steensma, H. Y. van Heusden, G. P. H. 2001. 14-3-3 proteins: key regulators of cell division, signalling and apoptosis. BioEssays 23 : 936 946.
109. Volonté, D., Galbiati, F., Li, S., Nishiyama, K., Okamoto, T. Lisanti, M. P. 1999. Flotillins/Cavatellins are differentially expressed in cells and tissues and form a hetero-oligomeric complex with caveolins in vivo. J. Biol. Chem. 274 : 12702 12709.
110. von Ubisch, L. 1913. Die Entwicklung von Strongylocentrotus lividus (Echinus microtuberculatus, Arbacia pustulosa). Z. Wissenschaftliche Zool. 106 : 409 448.
111. Wessel, G. M. 1999. Sea urchin ECM molecules. In T. Kreis R. Vale (eds.). Guidebook to the Extracellular Matrix, Anchor, and Adhesion Proteins. 2nd ed. Oxford University Press, New York, pp. 467 477.
112. Wessel, G. M. Wikramanayake, A. H. 1999. How to grow a gut: ontogeny of the endoderm in the sea urchin embryo. BioEssays 21 : 459 471.
113. Williams, D. H. C. Anderson, D. T. 1975. The reproductive system, embryonic development, larval development and metamorphosis of the sea urchin Heliocidaris erythrogramma (Val.) (Echinoidea: Echinometridae). Aust. J. Zool. 23 : 371 403.
114. Wilson, K. A., Andrews, M. E. Raff, R. A. 2005a. Dissociation of expression patterns of homeodomain transcription factors in the evolution of developmental mode in the sea urchins Heliocidaris tuberculata and H. erythrogramma. Evol. Dev. 7 : 401 415.
115. Wilson, K. A., Andrews, M. E., Turner, F. R. Raff, R. A. 2005b. Major regulatory factors in the evolution of development: the roles of goosecoid and msx in the evolution of the direct-developing sea urchin Heliocidaris erythrogramma. Evol. Dev. 7 : 416 428.
116. Wolpert, L. 1999. From egg to adult to larva. Evol. Dev. 1 : 3 4.
117. Wray, G. A. 1996. Parallel evolution of nonfeeding larvae in echinoids. Syst. Biol. 45 : 308 322.
118. Wray, G. A. Raff, R. A. 1989. Evolutionary modification of cell lineage in the direct-developing sea urchin Heliocidaris erythrogramma. Dev. Biol. 132 : 458 470.
119. Wray, G. A. Raff, R. A. 1990. Novel origins of lineage founder cells in the direct-developing sea urchin Heliocidaris erythrogramma. Dev. Biol. 141 : 41 54.
120. Wray, G. A. Raff, R. A. 1991. Rapid evolution of gastrulation mechanisms in a sea urchin with lecithotrophic larvae. Evolution 45 : 1741 1750.
121. Yaffe, M. B. 2002. How do 14-3-3 proteins work? - Gatekeeper phosphorylation and the molecular anvil hypothesis. FEBS Lett. 513 : 53 57.
122. Yuh, C.-H., Bolouri, H. Davidson, E. H. 2001. Cis-regulatory logic in the endo16 gene: switching from a specification to a differentiation mode of control. Development 128 : 617 629.
123. Yuh, C.-H. Davidson, E. H. 1996. Modular cis-regulatory organization of endo16, a gut-specific gene of the sea urchin embryo. Development 122 : 1069 1082.
124. Zhou, N., Wilson, K. A., Kauffman, J. S. Raff, R. A. 2003. Evolution of Otp-independent larval skeletal patterning in the direct-developing sea urchin, Heliocidaris erythrogramma. J. Exp. Zool. (Mol Dev Evol) 300B : 58 71.
125. Zigler, K. S., Raff, E. C., Popodi, E. M., Raff, R. A. Lessios, H. A. 2003. Adaptive evolution of bindin in the genus Heliocidaris is correlated with the shift to direct development. Evolution 57 : 2293 2302.