Larval ectoderm, organizational homology, and the origins of evolutionary novelty

Journal of Experimental Zoology Part B: Molecular and Developmental Evolution

Volumn 306, Issue 1, 2006, Pages 18-34

  Love, Alan C ^a,b   Raff, Rudolf A ^a  

^a INDIANA UNIVERSITY   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BIOLOGICAL MODEL; COMPARATIVE STUDY; ECTODERM; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; LARVA; MORPHOGENESIS; PHYLOGENY; PHYSIOLOGY; REVIEW; SEA URCHIN; SPECIES DIFFERENCE;

ANIMALS; BODY PATTERNING; ECTODERM; LARVA; MODELS, BIOLOGICAL; MORPHOGENESIS; PHYLOGENY; SEA URCHINS; SPECIES SPECIFICITY;

ECHINOIDA; ECHINOIDEA; HELIOCIDARIS; HELIOCIDARIS ERYTHROGRAMMA; HELIOCIDARIS TUBERCULATA; INVERTEBRATA;

EID: 33644676367     PISSN: 15525007     EISSN: 15525015     Source Type: Journal    
DOI: 10.1002/jez.b.21064     Document Type: Review

References (135)

1. Abouheif E. 1997. Developmental genetics and homology: a hierarchical approach. Trends Ecol Evol 12:405-408.
2. Abouheif E, Akam M, Dickinson WJ, Holland PWH, Meyer A, Patel NH, Raff RA, Roth VL, Wray GA. 1997. Homology and developmental genes. Trends Genet 13:432-433.
3. Akasaka K, Uemoto H, Wilt FH, Mitsunaga-Nakatsubo K, Shimada H. 1997. Oral-aboral ectoderm differentiation of sea urchin embryos is disrupted in response to calcium ionophore. Dev Growth Differ 39:373-379.
4. Alberch P. 1985. Problems with the interpretation of developmental sequences. Syst Zool 34:46-58.
5. Amore G, Yavrouian RG, Peterson KJ, Ransick A, McClay DR, Davidson EH. 2003. Spdeadringer, a sea urchin embryo gene required separately in skeletogenic and oral ectoderm gene regulatory networks. Dev Biol 261:55-81.
6. Angerer LM, Angerer RC. 2003. Patterning the sea urchin embryo: gene regulatory networks, signaling pathways, and cellular interactions. Curr Top Dev Biol 53:159-198.
7. Bisgrove BW, Burke RD. 1987. Development of the nervous system of the pluteus larva of Strongylocentrotus droebachiensis. Cell Tissue Res 248:335-343.
8. Bisgrove BW, Raff RA. 1989. Evolutionary conservation of the larval serotonergic nervous system in a direct developing sea urchin. Dev Growth Differ 31:363-370.
9. Bisgrove BW, Andrews ME, Raff RA. 1995. Evolution of the fibropellin gene family and patterns of fibropellin gene expression in sea urchin phylogeny. J Mol Evol 41:34-45.
10. Bolker JA, Raff RA. 1996. Developmental genetics and traditional homology. BioEssays 18:489-494.
11. Brandhorst BP, Klein WH. 2002. Molecular patterning along the sea urchin animal-vegetal axis. Int Rev Cytol 213:183-232.
12. Brigandt I. 2003. Homology in comparative, molecular, and evolutionary developmental biology. J Exp Zool Part B: Mol Dev Evol 299B:9-17.
13. Cameron RA, Coffman JA. 1999. Gene expression and early cell fate specification in embryos of the purple sea urchin (Strongylocentrotus purpuratus). In: Moody SA, editor. Cell lineage and fate determination. San Diego: Academic Press. p 11-23.
14. Cameron RA, Fraser SE, Britten RJ, Davidson EH. 1989. The oral-aboral axis of a sea urchin embryo is specified by first cleavage. Development 106:641-647.
15. Chia F-S, Burke RD. 1978. Echinoderm metamorphosis: fate of larval structures. In: Chia F-S, Rice ME, editors. Settlement and metamorphosis of marine invertebrate larvae. New York: Elsevier. p 219-234.
16. Coffman JA, Davidson EH. 2001. Oral-aboral axis specification in the sea urchin embryo I. Axis entrainment by respiratory asymmetry. Dev Biol 230:18-28.
17. Coffman JA, McCarthy JJ, Dickey-Sims C, Robertson AJ. 2004. Oral-aboral axis specification in the sea urchin embryo II. Mitochondrial distribution and redox state contribute to establishing polarity in Strongylocentrotus purpuratus. Dev Biol 273:160-171.
18. 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.
19. David B, Mooi R. 1998. Major events in the evolution of echinoderms viewed by the light of embryology. In: Mooi R, Telford M, editors. Echinoderms. San Francisco, Rotterdam: Balkema. p 21-28.
20. Davidson EH, Cameron RA, Ransick A. 1998. Specification of cell fate in the sea urchin embryo: summary and some proposed mechanisms. Development 125:3269-3290.
21. 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.
22. Emlet RB. 1991. Functional constraints on the evolution of larval forms of marine invertebrates: experimental and comparative evidence. Am Zool 31:707-725.
23. Emlet RB. 1994. Body form and patterns of ciliation in nonfeeding larvae of echinoderms: functional solutions to swimming in the plankton? Am Zool 34:570-585.
24. Emlet RB. 1995. Larval spicules, cilia, and symmetry as remnants of indirect development in the direct developing sea urchin Heliocidaris erythrogramma. Dev Biol 167:405-415.
25. Ettensohn CA, Sweet HC. 2000. Patterning the early sea urchin embryo. Curr Top Dev Biol 50:1-44.
26. Ferkowicz MJ, Raff RA. 2001. Wnt gene expression in sea urchin development: heterochronies associated with the evolution of developmental mode. Evol Dev 3:24-33.
27. Fitch WM. 2000. Homology: a personal view on some of the problems. Trends Genet 16:227-231.
28. Gan L, Mao C-A, Wikramanayake AH, Angerer LM, Angerer RC, Klein WH. 1995. An Orthodenticle-related protein from Strongylocentrotus purpuratus. Dev Biol 167:517-528.
29. Ganfornina MD, Sánchez D. 1999. Generation of evolutionary novelty by functional shift. BioEssays 21:432-439.
30. Gilbert SF, Bolker JA. 2001. Homologies of process and modular elements of embryonic construction. In: Wagner GP, editor. The character concept in evolutionary biology. San Diego: Academic Press. p 437-456.
31. Gilbert SF, Opitz JM, Raff RA. 1996. Resynthesizing evolutionary and developmental biology. Dev Biol 173:357-372.
32. Gross JM, McClay DR. 2001. The role of Brachyury (T) during gastrulation movements in the sea urchin Lytechinus variegatus. Dev Biol 239:132-147.
33. Gross JM, Peterson RE, Wu S-Y, McClay DR. 2003. LvTbx2/3: a T-box family transcription factor involved in formation of the oral/aboral axis of the sea urchin embryo. Development 130:1989-1999.
34. Guralnick R. 2002. A recapitulation of the rise and fall of the cell lineage research program: the evolutionary-developmental relationship of cleavage to homology, body plans, and life history. J Hist Biol 35:537-567.
35. Haag ES, Raff RA. 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.
36. Haag ES, Sly BJ, Andrews ME, Raff RA. 1999. Apextrin, a novel extracellular protein associated with larval ectoderm evolution in Heliocidaris erythrogramma. Dev Biol 211:77-87.
37. Hall BK. 1995. Homology and embryonic development. In: Hecht MK, Macintyre RJ, Clegg MT, editors. Evolutionary biology, Vol. 28. New York: Plenum Press.
38. Hall BK. 1998. Germ layers and the germ-layer theory revisited: primary and secondary germ layers, neural crest as a fourth germ layer, homology, and demise of the germ-layer theory. In: Hecht MK, Macintyre RJ, Clegg MT, editors. Evolutionary biology, Vol. 30. New York: Plenum Press.
39. Hall BK. 2003. Descent with modification: the unity underlying homology and homoplasy as seen through an analysis of development and evolution. Biol Rev Camb Philos Soc 78:409-433.
40. Hanken J, Hall BK. 1993. Mechanisms of skull diversity and evolution. In: Hanken J, Hall BK, editors. The skull: Vol. 3, functional and evolutionary mechanisms. Chicago and London: University of Chicago Press. p 1-36.
41. Hardin J, Armstrong N. 1997. Short-range cell-cell signals control ectodermal patterning in the oral region of the sea urchin embryo. Dev Biol 182:134-149.
42. 2. Development 116:671-685.
43. Hart MW. 2002. Life history evolution and comparative developmental biology. Evol Dev 4:62-71.
44. Havenhand JN. 1995. Evolutionary ecology of larval types. In: McEdward LR, editor. Ecology of marine invertebrate larvae. Boca Raton, FL: CRC Press. p 79-122.
45. Henry JJ, Klueg KM, Raff RA. 1992. Evolutionary dissociation between cleavage, cell lineage, and embryonic axes in sea urchin embryos. Development 114:931-938.
46. Heyland A, Hodin J. 2004. Heterochronic developmental shift caused by thyroid hormone in larval sand dollars and its implications for phenotypic plasticity and the evolution of nonfeeding development. Evol Int J Org Evol 58:524-538.
47. Heyland A, Reitzel AM, Hodin J. 2004. Thyroid hormones determine developmental mode in sand dollars (Echinodermata: Echinoidea). Evol Dev 6:382-392.
48. Hinman VF, Nguyen AT, Cameron RA, Davidson EH. 2003. Developmental gene regulatory network architecture across 500 million years of echinoderm evolution. Proc Natl Acad Sci USA 100:13,356-13,361.
49. Huang L, Li X, El-Hodiri HM, Dayal S, Wikramanayake AH, Klein WH. 1999. Involvement of Tcf/Lef in establishing cell types along the animal-vegetal axis of sea urchins. Dev Genes Evol 210:73-81.
50. Kenny AP, Oleksyn DW, Newman LA, Angerer RC, Angerer LM. 2003. Tight regulation of SpSoxB factors is required for patterning and morphogenesis in sea urchin embryos. Dev Biol 261:412-425.
51. Kissinger JC, Raff RA. 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.
52. Kissinger JC, Hahn JH, Raff RA. 1997. Rapid evolution in a conserved gene family. Evolution of the actin gene family in the sea urchin genus Heliocidaris and related genera. Mol Biol Evol 14:654-665.
53. Kominami T. 1988. Determination of dorso-ventral axis in early embryos of the sea urchin, Hemicentrotus pulcherrimus. Dev Biol 127:187-196.
54. Laubichler MD. 2000. Homology in development and the development of the homology Concept. Am Zool 40:777-788.
55. Laubichler MD, Maienschein J. 2003. Ontogeny, anatomy, and the problem of homology: Carl Gegenbaur and the American tradition of cell lineage studies. Theory Biosci 122:194-203.
56. Li X, Wikramanayake AH, Klein WH. 1999. Requirement of SpOtx in cell fate decisions in the sea urchin embryo and possible role as a mediator of β-catenin signaling. Dev Biol 212:425-439.
57. Littlewood DT, Smith AB. 1995. A combined morphological and molecular phylogeny for sea urchins (Echinoidea: Echinodermata). Philos Trans Roy Soc Lond B Biol Sci 347:213-234.
58. Love AC. 2003. Evolutionary morphology, innovation, and the synthesis of evolutionary and developmental biology. Biol Philos 18:309-345.
59. Löwe CJ, Wray GA. 1997. Radical alterations in the roles of homeobox genes during echinoderm evolution. Nature 389:718-721.
60. Lowe CJ, Issel-Tarver L, Wray GA. 2002. Gene expression and larval evolution: changing roles of distal-less and orthodenticle in echinoderm larvae. Evol Dev 4:111-123.
61. Lynch M, Force A. 2000. The probability of duplicate gene preservation by subfunctionalization. Genetics 154:459-473.
62. Lynch M, O'Hely M, Walsh B, Force A. 2001. The probability of preservation of a newly arisen gene duplicate. Genetics 159:1789-1804.
63. Mao C-A, Wikramanayake AH, Gan L, Chuang C-K, Summers RG, Klein WH. 1996. Altering cell fates in sea urchin embryos by overexpressing SpOtx, an orthodenticle-related protein. Development 122:1489-1498.
64. McEdward LR. 1997. Relationships among development, ecology, and morphology in the evolution of echinoderm larvae and life cycles. Biol J Linn Soc 60:381-400.
65. McEdward LR. 2000. Adaptive evolution of larvae and life cycles. Semin Cell Dev Biol 11:403-409.
66. Minelli A. 1998. Molecules, developmental modules, and phenotypes: a combinatorial approach to homology. Mol Phys Evol 9:340-347.
67. Minelli A. 2003. The development of animal form: ontogeny, morphology, and evolution. Cambridge: Cambridge University Press.
68. Minsuk SB, Raff RA. 2002. Pattern formation in a pentameral animal: induction of early adult rudiment development in sea urchins. Dev Biol 247:335-350.
69. Mooi R, David B. 2000. What a new model of skeletal homologies tells us about asteroid evolution. Am Zool 40:326-339.
70. Mooi R, David B, Marchland D. 1994. Echinoderm skeletal homologies: classical morphology meets modern phylogenetics. In: David B, Guille A, Féral J-P, Roux M, editors. Echinoderms through time. Rotterdam: Balkema. p 87-95.
71. Morris VB, Zhao J-T, Shearman DCA, Byrne M, Frommer M. 2004. Expression of an Otx gene in the adult rudiment and the developing central nervous system in the vestibula larva of the sea urchin Holopneustes purpurescens. Int J Dev Biol 48:17-22.
72. Müller GB. 2003. Homology: The evolution of morphological organization. In: Müller GB, Newman SA, editors. Origination of organismal form: beyond the gene in developmental and evolutionary biology. Cambridge, MA: A Bradford Book, The MIT Press. p 51-69.
73. Müller GB, Newman SA. 1999. Generation, integration, autonomy: three steps in the evolution of homology. In: Bock GR, Cardew G, editors. Homology. Chichester, England: John Wiley & Sons. p 65-73.
74. Müller GB, Wagner GP. 1991. Novelty in evolution: restructuring the concept. Annu Rev Ecol Syst 22:229-256.
75. Müller GB, Wagner GP. 1996. Homology, Hox genes and developmental integration. Am Zool 36:4-13.
76. Müller GB, Wagner GP. 2003. Innovation. In: Hall BK, Olsson WM, editors. Keywords and concepts in evolutionary developmental biology. Cambridge, MA: Harvard University Press. p 218-227.
77. Nakajima Y, Kaneko H, Murray G, Burke RD. 2004. Divergent patterns of neural development in larval echinoids and asteroids. Evol Dev 6:95-104.
78. Newman SA, Müller GB. 2000. Epigenetic mechanisms of character origination. J Exp Zool Part B: Mol Dev Evol 288:304-317.
79. Nielsen MG, Wilson KA, Raff EC, Raff RA. 2000. Novel gene expression patterns in hybrid embryos between species with different modes of development. Evol Dev 2:133-144.
80. Nielsen MG, Popodi EM, 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.
81. Okasaki K. 1975. Normal development to metamorphosis. In: Czihak G, editor. The sea urchin embryo: biochemistry and morphogenesis. Berlin: Springer-Verlag. p 177-232.
82. Parks AL, Parr BA, Chin J-E, Leaf DS, Raff RA. 1988. Molecular analysis of heterochronic changes in the evolution of direct developing sea urchins. J Evol Biol 1:27-44.
83. Philip GM. 1965. The Tertiary echinoids of south-eastern Australia III. Stirodonta, Aulodonta, and Camarodonta (1). Proc Roy Soc Victoria 78:181-196.
84. Poustka AJ, Kühn A, Radosavljevic V, Wellenreuther R, Lehrach H, Panopoulou GD. 2004. On the origin of the chordate central nervous system: expression of onecut in the sea urchin embryo. Evol Dev 6:227-236.
85. Raff RA. 1992. Direct-developing sea urchins and the evolutionary reorganization of early development. BioEssays 14:211-218.
86. Raff RA. 1996. The shape of life: genes, development and the evolution of animal form. Chicago: University of Chicago Press.
87. Raff RA. 1999a. Larval homologies and radical evolutionary changes in early development. In: Bock GR, Cardew G, editors. Homology. Chicester: John Wiley & Sons. p 110-124.
88. Raff RA. 1999b. Cell lineage in larval development and evolution of echinoderms. In: Hall BK, Wake MH, editors. The origin and evolution of larval forms. San Diego: Academic Press. p 255-273.
89. Raff RA, Sly BJ. 2000. Modularity and dissociation in the evolution of gene expression territories in development. Evol Dev 2:102-113.
90. Raff RA, Wray GA. 1989. Heterochrony: developmental mechanisms and evolutionary results. J Evol Biol 2:409-434.
91. Raff RA, Parr B, Parks A, Wray G. 1990. Heterochrony and other mechanisms of radical evolutionary change in early development. In: Nitecki MH, editor. Evolutionary innovations. Chicago: University of Chicago Press. p 71-98.
92. Raff EC, Popodi EM, Sly BJ, Turner FR, Villinski JT, Raff RA. 1999. A novel ontogenetic pathway in hybrid embryos between species with different modes of development. Development 126:1937-1945.
93. Raff EC, Popodi EM, Kauffman JS, Sly BJ, Turner FR, Morris VB, Raff RA. 2003. Regulatory punctuated equilibrium and convergence in the evolution of developmental pathways in direct-developing sea urchins. Evol Dev 5:478-493.
94. Ramachandran RK, Wikramanayake AH, Uzman JA, Govindarajan V, Tomlinson CR. 1997. Disruption of gastrulation and oral-aboral ectoderm differentiation in the Lytechinus pictus embryo by a dominant/negative PDGF receptor. Development 124:2355-2364.
95. Rast JP, Cameron RA, Poustka AJ, Davidson EH. 2002. brachyury target genes in the early sea urchin embryo isolated by differential macroarray screening. Dev Biol 246:191-208.
96. Reiss JO. 2003. Time. In: Hall BK, Olson WM, editors. Keywords and concepts in evolutionary developmental biology. Cambridge, MA: Harvard University Press. p 359-368.
97. Riedl R. 1978. Order in living systems: a systems analysis of evolution. Jefferies RPS, translator. New York: John Wiley & Sons, Ltd.
98. Roth VL. 1991. Homology and hierarchies: problems solved and unresolved. J Evol Biol 4:167-194.
99. Saucede T, Mooi R, David B. 2004. Evolution to the extreme: origins of the highly modified apical system in pourtalesiid echinoids. Zool J Linn Soc 140:137-155.
100. Schlosser G, Wagner GP, editors. 2004. Modularity in development and evolution. Chicago and London: University of Chicago Press.
101. Schwenk K, Wagner GP. 2003. Constraint. In: Hall BK, Olson WM, editors. Keywords and concepts in evolutionary developmental biology. Cambridge, MA: Harvard University Press. p 52-61.
102. Sly BJ. 2004. The development and evolution of the echinoderm nervous system (Ph.D.). Bloomington: Indiana University. 230 p.
103. Sly BJ, Hazel JC, Popodi EM, Raff RA, 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.
104. Sly BJ, Snoke MS, Raff RA. 2003. Who came first - larvae or adults? Origins of bilaterian metazoan larvae. Int J Dev Biol 47:623-632.
105. Smith AB. 1988. Phylogenetic relationship, divergence times, and rates of molecular evolution for camarodont sea urchins. Mol Biol Evol 5:345-365.
106. Smith AB. 1989. RNA sequence data in phylogenetic reconstruction: testing the limits of resolution. Cladistics 5:321-344.
107. Smith KK. 2002. Sequence heterochrony and the evolution of development. J Morphol 252:82-97.
108. Strathmann RR. 1978. The evolution and loss of feeding larval stages of marine invertebrates. Evol Int J Org Evol 32(4):894-906.
109. Strathmann RR. 1985. Feeding and nonfeeding larval development and life-history evolution in marine invertebrates. Annu Rev Ecol Syst 16:339-361.
110. Strathmann RR. 1993. Hypotheses on the origins of marine larvae. Annu Rev Ecol Syst 24:89-117.
111. Strathmann RR. 2000. Functional design in the evolution of embryos and larvae. Semin Cell Dev Biol 11:395-402.
112. Striedter GF. 1998. Stepping into the same river twice: homologues as recurring attractors in epigenetic landscapes. Brain Behav Evol 52:218-231.
113. Takacs CM, Amore G, Oliveri P, Poustka AJ, Wang D, Burke RD, Peterson KJ. 2004. Expression of an NK2 homeodomain gene in the apical ectoderm defines a new territory in the early sea urchin embryo. Dev Biol 269:152-164.
114. True JR, Carroll SB. 2002. Gene co-option in physiological and morphological evolution. Annu Rev Cell Dev Biol 18:53-80.
115. Wagner GP. 1989a. The biological homology concept. Annu Rev Ecol Syst 20:51-69.
116. Wagner GP. 1989b. The origin of morphological characters and the biological basis of homology. Evol Int J Org Evol 43:1157-1171.
117. Wagner GP. 1996. Homologues, natural kinds and the evolution of modularity. Am Zool 36:36-43.
118. Wagner GP. 2000. What is the promise of developmental evolution? Part I: why is developmental biology necessary to explain evolutionary innovations? J Exp Zool Part B: Mol Dev Evol 288:95-98.
119. Wagner GP, Altenberg L. 1996. Perspective: complex adaptations and the evolution of evolvability. Evol Int J Org Evol 50:967-976.
120. Wagner GP, Misof BY. 1993. How can a character be developmentally constrained despite variation in developmental pathways? J Evol Biol 6:449-455.
121. Wagner GP, Amemiya C, Ruddle F. 2003. Hox cluster duplications and the opportunity for evolutionary novelties. Proc Natl Acad Sci USA 100:14,603-14,606.
122. Wikramanayake AH, Klein WH. 1999. Otx, β-catenin, and the specification of ectodermal cell fates in the sea urchin embryo. In: Moody SA, editor. Cell lineage and fate determination. San Diego: Academic Press. p 25-39.
123. Wikramanayake AH, Brandhorst BP, Klein WH. 1995. Autonomous and non-autonomous differentiation of ectoderm in different sea urchin species. Development 121:1497-1505.
124. Williams DHC, Anderson DT. 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.
125. Wilson KA. 2003. Major effect genes in the evolution of development: changes of regulatory gene function in the transformation of developmental mode in sea urchins of the genus Heliocidaris (PhD). Bloomington: Indiana University. 250 p.
126. Wilson KA, Andrews ME, Raff RA. 2005. Dissociation of expression patterns of homeodomain transcription factors in the evolution of developmental mode in the sea urchins Heliocidaris tuberculata and H. erythrogramma, in press.
127. Winther RG. 2001. Varieties of modules: kinds, levels, origins, and behaviors. J Exp Zool Part B: Mol Dev Evol 291:116-129.
128. Witman GB. 1990. Introduction to cilia and flagella. In: Bloodgood RA, editor. Ciliary and flagellar membranes. New York: Plenum Press. p 1-30.
129. Wray GA. 1996. Parallel evolution of nonfeeding larvae in echinoids. Syst Biol 45:308-322.
130. Wray GA. 1999a. Evolutionary dissociations between homologous genes and homologous structures. In: Bock GR, Cardew G, editors. Homology. Chichester: John Wiley & Sons. p 189-206.
131. Wray GA. 1999b. Introduction to sea urchins. In: Moody SA, editor. Cell lineage and fate determination. San Diego: Academic Press. p 3-9.
132. Wray GA. 2000. The evolution of embryonic patterning mechanisms in animals. Semin Cell Dev Biol 11:385-393.
133. Wray GA, Lowe CJ. 2000. Developmental regulatory genes and echinoderm evolution. Syst Biol 49:28-51.
134. Zhou N, Wilson KA, Kauffman JS, Raff RA. 2003. Evolution of OTP-independent larval skeletal patterning in the direct-developing sea urchin, Heliocidaris erythrogramma. J Exp Zool Part B: Mol Dev Evol 300B:58-71.
135. Zigler KS, Raff EC, Popodi EM, Raff RA, Lessios HA. 2003. Adaptive evolution of bindin in the genus Heliocidaris is correlated with the shift to direct development. Evol Int J Org Evol 57:2293-2302.