Developmental regulatory genes and echinoderm evolution

Systematic Biology

Volumn 49, Issue 1, 2000, Pages 28-51

  Wray, Gregory A ^a,b   Lowe, Christopher J ^a,c  

^a STONY BROOK UNIVERSITY   (United States)

^b DUKE UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Echinodermata; Evolution of development; Homeobox gene; Homology; Metazoa; Regulatory gene

Indexed keywords

BILATERIA; ECHINODERMATA; METAZOA;

ANIMAL; CLASSIFICATION; ECHINODERM; EVOLUTION; GENETICS; NON-PROGRAMMATIC; PHYLOGENY; REGULATOR GENE; REVIEW;

NON-PROGRAMMATIC;

ANIMALS; ECHINODERMATA; EVOLUTION; GENES, REGULATOR; PHYLOGENY;

EID: 0034350363     PISSN: 10635157     EISSN: None     Source Type: Journal    
DOI: 10.1080/10635150050207375     Document Type: Article

References (122)

1. ABOUHEIF, E. 1997. Developmental genetics and homology: A hierarchical approach. Trends Ecol. Evol. 12:405-408.
2. ABOUHEIF, E., M. AKAM, W. J. DICKINSON, P. W. H. HOLLAND, A. MEYER, N. H. PATEL, R. A. RAFF, V. L. ROTH, AND G. A. WRAY. 1997. Homology and developmental genes. Trends Genet. 13:432-433.
3. ABZHANOV, A., AND T. C. KAUFMAN. 1999. Novel regulation of the homeotic gene Scr associated with a crustacean leg-to-maxilliped appendage transformation. Development 126:1121-1128.
4. AGUINALDO, A. M. A., J. M. TURBEVILLE, L. S. LINFORD, M. C. RIVERA, J. R. GAREY, R. A. RAFF, AND J. A. LAKE. 1997. Evidence for a clade of nematodes, arthropods, and other moulting animals. Nature 387: 489-493.
5. AMEMIYA, S., AND R. B. EMLET. 1992. The development and larval form of an echinothurioid echinoid, Asthenosomal ijimai, revisited. Biol. Bull. 182:15-30.
6. ANGERER, L. M., G. J. DOLECKI, M. L. GAGNON, G. WANG, Q. YANG, T. HUMPHREYS, AND R. C. ANGERER. 1989. Progressively restricted expression of a homeobox gene within the aboral ectoderm of developing sea urchin embryos. Genes Dev. 3:370-383.
7. ARENAS-MENA, C., P. MARTINEZ, R. A. CAMERON, AND E. H. DAVIDSON. 1998. Expression of the Hox gene complex in the indirect development of the sea urchin. Proc. Natl. Acad. Sci. USA 95:13062-13067.
8. ARNONE, M. I., AND E. H. DAVIDSON. 1997. The hardwiring of development: Organization and function of genomic regulatory systems. Development 124: 1851-1864.
9. ARTHUR, W. 1988. A theory of the evolution of development. Wiley, Chichester, UK.
10. ARTHUR, W. 1997. The origin of animal body plans. Cambridge University Press, Cambridge, UK.
11. ATCHLEY, W. R., AND W. M. FITCH. 1997. A natural classification of the basic helix-loop-helix class of transcription factors. Proc. Natl. Acad. Sci. USA 94:5172-5176.
12. AVEROF, M., AND S. M. COHEN. 1997. Evolutionary origin of insect wings from ancestral gills. Nature 385:627-630.
13. AVEROF, M., R. DAWES, AND D. FERRIER. 1996. Diversification of arthropod Hox genes as a paradigm for the evolution of gene functions. Sem. Cell Dev. Biol. 7:539-551.
14. BHARATHAN, G., B.-J. JANNSEN, E. A. KELLOGG, AND N. SINHA. 1997. Were homeodomain proteins duplicated before the origin of angiosperms, fungi and metazoa? Proc. Natl. Acad. Sci. USA 94:13749-13753.
15. BRITTEN, R. J., AND E. H. DAVIDSON. 1969. Gene regulation for higher cells: A theory. Science 165:349-357.
16. BROWN, S. J., R. B. HILGENFELD, AND R. E. DENELL. 1994. The beetle Tribolium has a fushi-tarazu homolog expressed in stripes during segmentation. Proc. Natl. Acad. Sci. USA 91:12922-12926.
17. BRUSCA, R. C., AND G. J. BRUSCA. 1990. Invertebrates. Sinauer Associates, Sunderland, Massachusetts.
18. BULLOCK, T., AND G. HORRIGE. 1969. Structure and function of the nervous systems of invertebrates. W. H. Freeman, San Francisco.
19. BYRNE, M. 1994. Ophiuroidea. Pages 247-343 in Microscopic anatomy of invertebrates, vol. 14: Echinodermata. Wiley-Liss, New York.
20. COFFMAN, J. A., C. V. KIRCHHAMER, M. G . HARRINGTON, AND E. H. DAVIDSON. 1996. SpRunt-1, a new member of the runt-domain family of transcription factors, is a positive regulator of the aboral ectoderm-specific CyIIIa gene in sea urchin embryos. Dev. Biol. 174:43-54.
21. COLLINS, F. S. 1995. Ahead of schedule and under budget: The genome project passes its fifth birthday. Proc. Natl. Acad. Sci. USA 92:10821-10823.
22. CORBO, J., M. LEVINE, AND R. W. ZELLER. 1997. Characterization of a notochord-specific enhancer from the brachyury promoter region of the ascidian, Cionn intestinalis. Development 124:589-602.
23. DAVIDSON, E. H., K. J. PETERSON, AND R. A. CAMERON. 1995. Origin of bilaterian body plans: Evolution of developmental regulatory mechanisms. Science 270:1319-1325.
24. DAVIS, C. A., D. P. HOLMYARD, K. J. MILLEN, AND A. L. JOYNER. 1991. Examining pattern formation in mouse, chicken, and frog embryos with an En-specific antiserum. Development 111:287-298.
25. DAVIS, C. A., AND A. L. JOYNER. 1988. Expression patterns of the homeobox-containing genes En-1 and En-2 and the proto-oncogene int-1 diverge during development. Genes Dev. 2:1736-1744.
26. DAWES, R., I. DAWSON, F. FALCIANI, G. TEAR, AND M. AKAM. 1994. Dax, a locust Hox gene related to fushi-tarazu but showing no pair-rule expression. Development 120:1561-1672.
27. DEGNAN, B., AND D. MORSE. 1993. Identification of eight homeobox-containing transcripts expressed during larval development and at metamorphosis in the gastropod mollusc Haliotis rufescens. Mar. Biol. Biotechnol. 2:1-9.
28. DEROBERTIS, E. M., AND Y. SASAI. 1996. A common plan for dorsoventral patterning in Bilateria. Nature 380:37-40.
29. DICKINSON, W. J. 1995. Molecules and morphol-ogy: where's the homology? Trends Genet. 11:119-121.
30. DOE, C. Q., D. SMOUSE, AND C. S. GOODMAN. 1988. Control of neuronal fate by the Drosophila segmentation gene even-skipped. Nature 333:376-378.
31. DUBOULE, D., ED. 1994. Guidebook to the homeobox genes. Oxford Univ. Press, Oxford.
32. 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.
33. EMLET, R. B. 1991. Functional constraints on the evolution of larval forms of marine invertebrates: Experimental and comparative evidence. Am. Zool. 31:707-725.
34. FALCIANI, F., B. HAUSDORF, R. SCHRÖDER, M. AKAM, D. TAUTZ, R. DENELL, AND S. BROWN. 1996. Class 3 Hox genes in insects and the origin of zen. Proc. Natl. Acad. Sci. USA 93:8479-8484.
35. FINKELSTEIN, R., AND E. BONCINELLI. 1994. From fly head to mammalian forebrain: the story of otd and Otx. Trends Genet. 10:310-315.
36. FINKELSTEIN, R., D. SMOUSE, T. M. CAPACI, A. C. SPRADLING, AND N. PERRIMON. 1990. The orthodenticle gene encodes a novel homeodomain protein involved in the development of the Drosophila nervous system and ocellar visual structures. Genes Dev. 4:1516-1527.
37. GAN, L., C.-A. MAO, A. WICKRAMANYAKE, L. M. ANGERER, R. C. ANGERER, AND W. H. KLEIN. 1995. An orthodenticle-related protein from Strongylocentrotus purpuratus. Dev. Biol. 167:517-528.
38. GARCIA-FERNÀNDEZ, J., J. BAGUÑA, AND E. SALÓ. 1991. Planarian homeobox genes: Cloning, sequence analysis, and expression. Proc. Natl. Acad. Sci. USA 88:7339-7342.
39. GEE, H. 1997. Before the backbone. Chapman and Hall, London.
40. GERHART, J., AND M. KIRSCHNER. 1997. Cells, embryos, and evolution. Blackwell Science, Malden, Massachusetts.
41. GILLESPIE, J. H. 1991. The causes of molecular evolution. Oxford Univ. Press, Oxford.
42. GRBIC, M., AND M. R. STRAND. 1998. Shifts in the life history of parasitic wasps correlate with pronounced alterations in early development. Proc. Natl. Acad. Sci. USA 95:1097-1101.
43. GREENWALD, I., AND G. M. RUBIN. 1992. Making a difference: The role of cell-cell interactions in establishing separate identities for equivalent cells. Cell 68:271-281.
44. GRENIER, J. K., T. L. GARBER, R. WARREN, P. M. WHITINGTON, AND S. CARROLL. 1997. Evolution of the entire arthropod Hox gene set predated the origin and radiation of the onychophoran/arthropod clade. Curr. Biol. 7:547-553.
45. HALL, B. K. 1992. Evolutionary developmental biology. Chapman and Hall, London.
46. HARADA, Y., K. AKASAKA, H. SHIMADA, K. J. PETERSON, E. H. DAVIDSON, AND N. SATOH. 1996. Spatial expression of a forkhead homologue in the sea urchin embryo. Mech. Dev. 60:163-173.
47. HARADA, Y., H. YASUO, AND N. SATOH. 1995. A sea urchin homologue of the chordate Brachyury (T) gene is expressed in the secondary mesenchyme cells. Development 121:9747-9754.
48. HERTZLER, P. L., C. Y. LOGAN, D. R. SHERWOOD, AND D. R. MCCLAY. 1996. A sea urchin hedgehog homolog. Dev. Biol. 175:40.
49. HIDALGO, A. 1996. The roles of engrailed. Trends Genet. 12:1-4.
50. HOLLAND, L. Z., M. KENE, N. A. WILLIAMS, AND N. D. HOLLAND. 1997. Sequence and embryonic expression of the amphioxus engrailed gene (AmphiEn): The metameric pattern of transcription resembles that of its segment-polarity homolog in Drosophila. Development 124:1723-1732.
51. HOLLAND, N. D. 1988. The meaning of developmental asymmetry for echinoderm evolution: A new interpretation. Pages 13-25 in Echinoderm phylogeny and evolutionary biology (C. R. C. Paul and A. B. Smith, eds.). Clarendon Press, Oxford.
52. HOLLAND, N. D., G. PANGANIBAN, E. L. HENYEY, AND L. Z. HOLLAND. 1996. Sequence and developmental expression of AmphiDll, an amphioxus Distal-less gene transcribed in the ectoderm, epidermis and nervous system: Insights into the evolution of the craniate forebrain and neural crest. Development 122:2911-2920.
53. HOLLAND, P. W. H. 1990. Homeobox genes and segmentation: Co-option, co-evolution, and convergence. Semin. Dev. Biol. 1:135-145.
54. HOTCHKISS, F. H. C. 1998. A 'rays as appendages' model for the origin of pentamerism in echinoderms. Paleobiology, 24:200-214.
55. HYMAN, L. 1955. The invertebrates, vol. 4. Echinodermata. McGraw-Hill, New York.
56. JEFFERIES, R. P. S., N. A. BROWN, AND P. E. J. DALEY. 1996. The early phylogeny of chordates and echinoderms the origins of chordate left-right asymmetry and bilateral symmetry. Acta Zool. 77: 101-122.
57. KAPHINGST, K., AND S. KUNES. 1994. Pattern formation in the visual centers of the Drosophila: wingless acts via decapentnplegic to specify the dorsoventral axis. Cell 78:437-448.
58. KIMMEL, C. B. 1996. Was Urbiltiteria segmented? Trends Genet. 12:329-331.
59. KIRCHHAMER, C. V., AND E. H. DAVIDSON. 1996. Spatial and temporal information processing in the sea urchin embryo: Modular and intramodular organization of the CyIIIa gene cis-regulatory system. Development 122:333-348.
60. KORNBERG, T., I. SIDEN, P. O'FARRELL, AND M. SIMON. 1985. The engrailed locus of Drosophila: In situ localization of transcripts reveals compartment-specific expression. Cell 40:45-53.
61. KOURAKIS, M., V. A. MASTER, D. K. LOKHORST, D. NARDELLI HAEFLIGER, C. J. WEDEEN, M. Q. MARTINDALE, AND M. SHANKLAND. 1997. Conserved anterior boundaries of Hox gene expression in the central nervous system of the leech Helobdella. Dev. Biol. 190:284-300.
62. LACALLI, T. C. 1996. Mesodermal pattern and pattern repeats in the starfish bipinnaria larva, and related patterns in other deuterostome larvae and chordates. Phil. Trans. R. Soc. Lond. B 351:1737-1758.
63. LACALLI, T. C. 1997. The nature and origin of deuterostomes: Some unresolved issues. Invert. Biol. 116:363-370.
64. LI, W. 1997. Molecular evolution. Sinauer Associates, Sunderland, Massachusetts.
65. LOGAN, C. Y, J. R. MILLER, M. J. FERKOWICZ, AND D. R. MCCLAY. 1999. Nuclear beta-catenin is required to specify vegetal cell fates in the sea urchin embryo. Development 126:345-357.
66. LOWE, C. J., AND G. A. WRAY. 1997. Radical alterations in the roles of homeobox genes during echinoderm evolution. Nature 389:718-721.
67. MASTER, V. A., M. J. KOURAKIS, AND M. Q. MARTINDALE. 1996. Isolation, characterization, and expression of Le-msx, a maternally expressed member of the msx gene family from the glossiphoniid leech, Helobdella. Dev. Dyn. 207:404-419.
68. MCCOON, P. E., E. BLACKSTONE, R. C. AUGERER, AND L. M. AUGERER. 1998. Sea urchin FGFR muscle-specific expression: post-translational regulation in embryos and adults. Dev. Biol. 200:171-181.
69. MCEDWARD, L. R., AND D. A. JANIES. 1997. Relationships among development, ecology, and morphology in the evolution of echinoderm larvae and life cycles. Biol. J. Linn. Soc. 60:381-400.
70. MEISE, M., D. HILFIKER-KLEINER, A. DUBENDORFER, C. BRUNNER, R. NOTHIGER, AND D. BOPP. 1998. Sexlethal, the master sex-determining gene in Drosophila, is not sex-specifically regulated in Musca domestica. Development 125:1487-1494.
71. MORTENSEN, T. 1921. Studies of the development and larval forms of echinoderms. G. E. C. Gad, Copenhagen.
72. MÜLLER, G. B., AND G. P. WAGNER. 1991. Novelty in evolution: Restructuring the concept. Ann. Rev. Ecol. Syst. 22:229-256.
73. MURRAY, A., AND T. HUNT. 1993. The cell cycle: An introduction. Oxford Univ. Press, New York.
74. NEI, M. 1987. Molecular evolutionary genetics. Columbia Univ. Press, New York.
75. NIELSEN, C. 1987. Structure and function of metazoan ciliary bands and their phylogenetic significance. Acta Zool. 68:205-262.
76. NIELSEN, C. 1995. Animal evolution: Interrelationships of the animal phyla. Oxford Univ. Press, Oxford.
77. OGASAWARA, M., H. WADA, H. PETERS, AND N. SATOH. 1999. Developmental expression of Pax1/9 genes in urchordate and hemichordate gills: Insights into function and evolution of the pharyngeal epithelium. Development 126:2539-2550.
78. OLSON, E. 1992. Activation of muscle-specific transcription by myogenic helix-loop-helix proteins. Symp. Soc. Exp. Biol. 46:331-341.
79. PANGANIBAN, G., S. M. IRVINE, C. LOWE, H. ROEHL, L. S. CORLEY, B. SHERBON, J. K. GREULER, J. F. FALLON, J. KIMBLE, M. WALKER, G. A. WRAY, B. J. SWALLA, M. Q. MARTINDALE, AND S. B. CARROLL. 1997. The origin and evolution of animal appendages. Proc. Natl. Acad. Sci. USA 94:5162-5166.
80. PARKS, A. L., B. W. BISGROVE, G. A. WRAY, AND R. A. RAFF. 1989. Direct development in the sea urchin Phyllacanthus parvispinus (Cidaroidea): Phylogenetic history and functional modification. Biol. Bull. 177:96-109.
81. PATEL, N. H. 1994. Developmental evolution: Insights from studies of insect segmentation. Science 266:581-590.
82. PATEL, N. H., E. E. BALL, AND C. S. GOODMAN. 1992. Changing role of even-skipped during the evolution of insect pattern formation. Nature 357:339-342.
83. PATEL, N. H., B. G. CONDRON, AND K. ZINN. 1994. Pair-rule expression patterns of even-skipped are found in both short- and long-germ beetles. Nature 367: 429-134.
84. PATEL, N. H., E. MARTIN-BLANCO, K. G. COLEMAN, S. J. POOLE, M. C. ELLIS, T. B. KORNBERG, AND C. S. GOODMAN. 1989. Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58:955-968.
85. PAUL, C. R. C., AND A. B. SMITH. 1984. The early radiation and phylogeny of echinoderms. Biol. Rev. 1984:443-481.
86. PETERSON, K. J., R. A. CAMERON, K. TAGAWA, N. SATOH, AND E. H. DAVIDSON. 1998. A comparative molecular approach to mesodermal patterning in basal deuterostomes: The expression of Brachyury in the enteropneust hemichordate Ptychodera flava. Development 126:85-95.
87. PETERSON, K. J., Y. HARADA, R. A. CAMERON, AND E. H. DAVIDSON. 1999. Expression pattern of Brachyury and not in the sea urchin: Comparative implications for the origins of mesoderm in the basal deuterostome. Dev. Biol. 207:419-431.
88. PILON, M., AND D. A. WEISBLAT. 1997. A nanos homolog in leech. Development 124:1771-1780.
89. PRICE, M., M. LEMAISTRE, M. PISCHETOLA, R. DI LAURO, AND D. DUBOULE. 1991. A mouse gene related to distal-less shows a restricted expression in the developing forebrain. Nature 351:748-751.
90. RAFF, R. A. 1996. The shape of life. Univ. Chicago Press, Chicago.
91. RAFF, R. A., AND T. C. KAUFMAN. 1983. Embryos, genes, and evolution. Macmillan, New York.
92. ROGERS, B. T., AND T. C. KAUFMAN. 1996. Structure of the insect head as revealed by the EN protein pattern in developing embryos. Development 122: 3419-3432.
93. SACCONE, G., I. PELUSO, D. ARTIACO, E. GIODIANO, D. BOPP, AND L. C. POLITO. 1998. The Ceratitis capitata homologue of the Drosophila sex-determining gene Sex-lethal is structurally conserved, but not sex-specifically regulated. Development 135:1495-1500.
94. SALSER, S. J., AND C. KENYON. 1992. Activation of a C. elegans Antennapedia homologue in migrating cells controls their direction of migration. Nature 355: 255-258.
95. SAVAGE, R. M., AND M. SHANKLAND. 1996. Identification and characterization of a hunchback orthologue, Lzf2, and its expression during leech embryogenesis. Dev. Biol. 175:205-217.
96. SCHUBERT, F. R., K. NIESELT-STRUWE, AND P. GRUSS. 1993. The Antennapedia-type homeobox genes have evolved from three precursors separated early in Metazoan evolution. Proc. Natl. Acad. Sci. USA 90:143-147.
97. SHENK, M. A., H. R. BODE, AND R. E. STEELE 1993. Expression of Cnox-2, a HOM/HOX homeobox gene in hydra, is correlated with axial pattern formation. Development 117:657-667.
98. SHERWOOD, D. R., AND D. R. MCCLAY. 1997. Identification and localization of a sea urchin Notch homologue: Insights into vegetal plate regionalization and Notch receptor regulation. Development 124: 3363-3374.
99. SHERWOOD, D. R., AND D. R. MCCLAY. 1999. LvNotch signalling mediates secondary mesenchyme specification in the sea urchin embryo. Development 126:1703-1713.
100. SHOGUCHI, E., N. SATOH, AND Y. K. MARUYAMA. 1999. Pattern of Brachyury gene expression in starfish embryos resembles that of hemichordate embryos but not of sea urchin embryos. Mech. Dev. 82:185-189.
101. SHUBIN, N., C. TABIN, AND S. CARROLL. 1997. Fossils, genes and the evolution of animal limbs. Nature 388:639-648.
102. SIMEONE, A., D. ACAMPORA, M. GULISANO, A. STORNAIUOLO, AND E. BONCINELLI. 1992. Nested expression domains of four homeobox genes in developing rostral brain. Nature 358:687-690.
103. SLACK, J. M. W., P. W. H. HOLLAND, AND C. F. GRAHAM. 1993. The zootype and the phylotypic stage. Nature 361:490-492.
104. SMITH, A. B. 1984. Echinoid palaeobiology. Allen Unwin, London.
105. SMITH, A. B. 1988. Fossil evidence for the relationship of extant echinoderm classes and their times of divergence. Pages 85-97 in Echinoderm phylogeny and evolutionary biology (C. R. C. Paul and A. B. Smith, ed.). Clarendon Press, Oxford.
106. SMITH, T. 1999. T-box genes - what they do and how they do it. Trends Genet. 15:154-158.
107. STRATHMANN, R. R. 1988. Functional requirements and the evolution of developmental patterns. Pages 55-61 in Echinoderm biology (R. D. Burke, P. V. Mladenov, P. Lambert, and R. L. Parsley, eds.). A. A. Balkema, Amsterdam.
108. SUMRALL, C., AND J. SPRINKLE. 1998. Phylogenetic analysis of living Echinodermata based on primitive fossil taxa. Pages 81-88 in Echinoderms: San Francisco (R. Mooi and M. Telford, eds.). Balkema Press, Rotterdam.
109. SWALLA, B. J., AND W. R. JEFFERY. 1996. Requirement of the Manx gene for expression of chordate features in a tailless ascidian larva. Science 274:1205-1208.
110. TELFORD, M. J., AND R. H.THOMAS. 1998. Of mites and zen: Expression studies in a chelicerate arthropod confirm zen is a divergent Hox gene. Dev. Genes. Evol. 208:591-594.
111. TOMAREV, S. I., P. CALLAERTS, L. KOS, R. ZINOVIEVA, G. HALDER, W. GEHRING, AND J. PIATIGORSKY. 1997. Squid Pax-6 and eye development. Proc. Natl. Acad. Sci. USA 94:2098-3100.
112. UBAGHS, G. 1967. General characteristics of Echinodermata. Pages S3-S60 in Treatise on invertebrate paleontology, volume S. Univ. Kansas Press, Lawrence.
113. VAUX, D. L., I. L. WEISSMAN, AND S. K. KIM. 1992. Prevention of programmed cell death in Caenorhabditis elegans by human bcl-2. Science 258:1955-1957.
114. VENUTI, J. M., L. GAN, M. T. KOZLOWSKI, AND W. H. KLEIN. 1996. Developmental potential of muscle cell progenitors and the myogenic factor SUM-1 in the sea urchin embryo. Mech. Dev. 41:3-14.
115. WADA, H., P. W. H. HOLLAND, S. SATO, H. YAMAMOTO, AND N. SATOH. 1997. Neural tube is partially dorsalized by overexpression of HrPax-37: The ascidian homologue of Pax-3 and Pax-7. Dev. Biol. 187:240-252.
116. WEDEEN, C. J., AND D. A. WEISBLAT. 1991. Segmental expression of an engrailed-class gene during early development and neurogenesis in an annelid. Development 113:805-814.
117. WEI, Z., L. M. ANGERER, AND R. C. ANGERER. 1999. Spatially regulated SpEts4 transcription factor activity along the sea urchin animal-vegetal axis. Development 126:1729-1737.
118. WENG, W., J. CHEETHAM, J. HARDIN, AND J. M. VENUTI. 1998. Sea urchin twist - mesoderm specification and more? Dev. Biol. 198:110.
119. WILSON, A. C. 1975. Evolutionary importance of gene regulation. Stadler Symp. 7:117-134.
120. WRAY, G. A. 1992a. Rates of evolution in developmental processes. Am. Zool. 32:123-134.
121. WRAY, G. A. 1992b. The evolution of larval morphology during the post-Paleozoic radiation of echinoids. Paleobiology 18:258-287.
122. WRAY, G. A., AND E. ABOUHEIF. 1998. When is homology not homology? Curr. Opin. Genet. Dev. 8:675-680.