The initiation of metamorphosis as an ancient polyphenic trait and its role in metazoan life-cycle evolution

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 365, Issue 1540, 2010, Pages 641-651

  Degnan, Sandie M ^a   Degnan, Bernard M ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Amphimedon queenslandica; Dispersal; Larval competence; Metamorphosis; Pelagobenthic; Porifera

Indexed keywords

ALLOPATRY; BENTHIC ENVIRONMENT; COMPARATIVE STUDY; EVOLUTIONARY BIOLOGY; GENOMICS; JUVENILE; LARVAL DEVELOPMENT; LARVAL TRANSPORT; METAMORPHOSIS; MORPHOGENESIS; PLANKTON; PROTOZOAN; SPECIATION (BIOLOGY); SPONGE;

AMPHIMEDON; BILATERIA; CNIDARIA; METAZOA; PORIFERA;

EID: 76749133185     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2009.0248     Document Type: Article

References (97)

1. Adamska, M., Degnan, S. M., Green, K. M., Adamski, M., Craigie, A., Larroux, C. Degnan, B. M. 2007a WNT and TGF-b expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning. PLoS One 2, e1031. (doi:10.1371/journal.pone.0001031)
2. Adamska, M., Matus, D. Q., Adamski, M., Green, K. M., okhsar, D. S., Martindale, M. Q. Degnan, B. M. 2007b The evolutionary origin of hedgehog proteins. Curr. Biol. 17, R836-R837. (doi:10.1016/j.cub.2007.08.010) (Pubitemid 47503799)
3. Adell, T. Mü ller, W. E. 2005 Expression pattern of the Brachyury and Tbx2 homologues from the sponge Suberites domuncula. Biol. Cell 97, 641-650. (doi:10.1042/BC20040135) (Pubitemid 41079036)
4. Amador-Cano, G., Carpizo-Ituarte, E. Cristino-Jorge, D. 2006 Role of protein kinase C, G-protein coupled receptors, and calcium flux during metamorphosis of the sea urchin Strongylocentrotus purpuratus. Biol. Bull. 210, 121-131. (doi:10.2307/4134601)
5. Arndt, A. Smith, M. J. 1998 Genetic diversity and population structure in two species of sea cucumber: differing patterns according to mode of development. Mol. Ecol. 7, 1053-1064. (doi:10.1046/j.1365-294x.1998.00429.x) (Pubitemid 28376696)
6. Avila, C., Tamse, C. T. Kuzirian, A. M. 1996 Induction of metamorphosis in Hermissenda crassicornis larvae (Mollusca: Nudibranchia) by GABA, choline and serotonin. Invert. Reprod. Dev. 29, 127-141.
7. Ayre, D. J. Hughes, T. P. 2000 Genotypic diversity and gene flow in brooding and spawning corals along the Great Barrier Reef, Australia. Evolution 54, 1590-1605.
8. Bishop, C. D. Brandhorst, B. P. 2003 On nitric oxide signaling, metamorphosis, and the evolution of biphasic life cycles. Evol. Dev. 5, 542-550. (doi:10.1046/j.1525- 142X.2003.03059.x)
9. Bishop, C. D., Pires, A., Norby, S. W., Boudko, D., Moroz, L. L. Hadfield, M. G. 2008 Analysis of nitric oxidecyclic guanosine monophosphate signaling during metamorphosis of the nudibranch Phestilla sibogae Bergh (Gastropoda: Opisthobranchia). Evol. Dev. 10, 288-299.
10. Breton, S., Dufresne, F., Desrosiers, G. Blier, P. U. 2003 Population structure of two northern hemisphere polychaetes, Neanthes virens and Hediste diversicolor (Nereididae), with different life-history traits. Mar. Biol. 142, 707-715.
11. Byrne, M. 2006 Life history diversity and evolution in the Asterinidae. Integr. Comp. Biol. 46, 243-254. (doi:10.1093/icb/icj033) (Pubitemid 44290591)
12. Davidson, B. Swalla, B. J. 2002 A molecular analysis of ascidian metamorphosis reveals activation of an innate immune response. Development 129, 4739-4751.
13. Degnan, B. M. Morse, D. E. 1995 Developmental and morphogenetic gene regulation in Haliotis rufescens larvae at metamorphosis. Am. Zool. 35, 391-398.
14. Degnan, B. M., Souter, D., Degnan, S. M. Long, S. C. 1997 Induction of metamorphosis in larvae of the ascidian Herdmania momus with potassium ions requires attainment of competence and an anterior signaling center. Dev. Genes Evol. 206, 370-376. (doi:10.1007/s004270050066) (Pubitemid 27087035)
15. Degnan, B. M., Leys, S. P. Larroux, C. 2005 Sponge development and antiquity of animal pattern formation. Integr. Comp. Biol. 45, 335-341. (doi:10.1093/icb/45.2.335)
16. Degnan, B. M. et al. 2009 The demosponge Amphimedon queenslandica: reconstructing the ancestral metazoan genome and deciphering the origin of animal multicellularity. In Emerging model organisms: a laboratory manual, vol.1, pp. 139-166. New York, NY: Cold Spring Harbor Laboratory Press.
17. Degnan, S. M. Degnan, B. M. 2006 The origin of the pelagobenthic metazoan life cycle: what's sex got to do with it? Integr. Comp. Biol. 46, 683-690. (doi:10.1093/icb/icl028) (Pubitemid 44736410)
18. De Tomaso, A. W., Nyholm, S. V., Palmeri, K. J., Ishizuka, K. J., Ludington, W. B., Mitchel, K. Weissman, I. L. 2005 Isolation and characterization of a protochordate histocompatibility locus. Nature 438, 454-459. (doi:10.1038/nature04150) (Pubitemid 41742011)
19. Dunn, C. W. et al. 2008 Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452, 745-749. (doi:10.1038/nature06614)
20. Eri, R., Arnold, J. M., Hinman, V. F., Green, K. M., Jones, M. K., Degnan, B. M. Lavin, M. F. 1999 Hemps, a novel EGF-like protein, plays a central role in ascidian metamorphosis. Development 126, 5809-5818.
21. Ettinger-Epstein, P., Whalan, S., Battershill, C. N. de Nys, R. 2008 A hierarchy of settlement cues influences larval behaviour in a coral reef sponge. Mar. Ecol. Prog. Ser. 365, 103-113. (doi:10.3354/meps07503)
22. Fahey, B., Larroux, C., Woodcroft, B. Degnan, B. M. 2008 Does the high gene density in the sponge NK homeobox gene cluster reflect limited regulatory capacity? Biol. Bull. 214, 205-217.
23. Fernàndez-Busquets, X. Burger, M. M. 1997 The main protein of the aggregation factor responsible for speciesspecific cell adhesion in the marine sponge Microciona prolifera is highly polymorphic. J. Biol. Chem. 272, 27 839-27 847. (doi:10.1074/jbc.272.44.27839) (Pubitemid 27473585)
24. Gauthier, M. Degnan, B. M. 2008 The transcription factor NF-kB in the sponge Amphimedon queenslandica: insights into the evolutionary origin of the Rel homology domain. Dev. Genes Evol. 218, 23-32. (doi:10.1007/s00427-007-0197- 5)
25. Gazave, E., Lapébie, P., Renard, E., Bézac, C., Boury-Esnault, N., Vacelet, J., Pérez, T., Manuel, M. Borchiellini, C. 2008 NK homeobox genes with choanocyte- specific expression in homoscleromorph sponges. Dev. Genes Evol. 218, 479-489. (doi:10.1007/s00427-008-0242-z)
26. Glusman, G., Yanai, I., Rubin, I. Lancet, D. 2001 The complete human olfactory subgenome. Genome Res. 11, 685-702. (doi:10.1101/gr.171001) (Pubitemid 32447857)
27. Grimson, A., Srivastava, M., Fahey, B., Woodcroft, B. J., Chiang, H. R., King, N., Degnan, B. M., Rokhsar, D. S. Bartel, D. P. 2008 Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals. Nature 455, 1193-1197. (doi:10.1038/nature07415)
28. Gröger, H. Schmid, V. 2001 Larval development in Cnidaria: a connection to Bilateria? Genesis 29, 110-114. (doi:10.1002/gene.1013) (Pubitemid 32260223)
29. Hadfield, M. G. 1977 Chemical interactions in larval settling of a marine gastropod. In Marine natural products chemistry (eds D. J. Faulkner W. H. Fenical), pp. 403-413. San Diego, CA: Plenum Press.
30. Hadfield, M. G. 1978 Metamorphosis in marine molluscan larvae: an analysis of stimulus and response. In Settlement and metamorphosis of marine invertebrate larvae (eds F. S. Chia M. E. Rice), pp. 165-175. Amsterdam, The Netherlands: Elsevier.
31. Hadfield, M. G. 1984 Settlement requirements of molluscan larvae: new data on chemical and genetic roles. Aquaculture 39, 283-298. (doi:10.1016/0044-8486(84)90272-2)
32. Hadfield, M. G. 2000 Why and how marine-invertebrate larvae metamorphose so fast. Semin. Cell Dev. Biol. 11, 437-443. (doi:10.1006/scdb.2000.0197) (Pubitemid 32120133)
33. Hadfield, M. G. Strathmann, M. F. 1996 Variability, flexibility and plasticity in life histories of marine invertebrates. Oceanol. Acta 19, 323-334.
34. Hadfield, M. G., Carpizo-Ituarte, E. J., del Carmen, K. Nedved, B. T. 2001 Metamorphic competence, a major adaptive convergence in marine invertebrate larvae. Am. Zool. 41, 1123-1131. (doi:10.1668/0003-1569(2001) 041[1123:MCAMAC]2.0.CO;2)
35. Hejnol, A. Martindale, M. Q. 2008 Acoel development supports a simple planula-like urbilaterian. Phil. Trans. R. Soc. B 363, 1493-1501. (doi:10.1098/rstb.2007.2239)
36. Heyland, A. Moroz, L. L. 2006 Signalling mechanisms underlying metamorphic transitions in animals. Integr. Comp. Biol. 46, 743-759. (doi:10.1093/icb/icl023) (Pubitemid 44736414)
37. Imron, Jefferey, B., Hale, Degnan, P. Degnan, S. M. 2007 Pleistocene isolation and recent gene flow in Haliotis asinina, an Indo-Pacific vetigastropod with limited dispersal capacity and specific settlement requirements. Mol. Ecol. 16, 289-304. (doi:10.1111/j.1365-294X.2006.03141.x) (Pubitemid 46058965)
38. Jackson, D., Leys, S. P., Hinman, V. F., Woods, R., Lavin, M. F. Degnan, B. M. 2002 Ecological regulation of development: induction of marine invertebrate metamorphosis. Int. J. Dev. Biol. 46, 679-686.
39. Jackson, D. J., Ellemor, N. Degnan, B. M. 2005 Correlating gene expression with larval competence and the effect of larval age and parentage on rates of metamorphosis in the tropical abalone. Haliotis asinina. Mar. Biol. 147, 681-697. (doi:10.1007/s00227-005-1603-z) (Pubitemid 40950487)
40. Jager, M., Quéinnec, E., Chiori, R., Le Guyader, H. Manuel, M. 2008 Insights into the early evolution of SOX genes from expression analyses in a ctenophore. J. Exp. Zool. (Mol. Dev. Evol.) 310B, 650-667. (doi:10.1002/jez.b.21244)
41. Jägersten, G. 1972 Evolution of the metazoan life cycle: a comprehensive theory. New York, NY: Academic Press.
42. King, N. et al. 2008 The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451, 783-788. (doi:10.1038/nature06617) (Pubitemid 351253174)
43. Kyle, C. J. Boulding, E. G. 2000 Comparative population genetic structure of marine gastropods (Littorina spp.) with and without pelagic larval dispersal. Mar. Biol. 137, 835-845. (doi:10.1007/s002270000412) (Pubitemid 32122143)
44. Lapébie, P., Gazave, E., Ereskovsky, A., Derelle, R., Bézac, C., Renard, E., Houliston, E. Borchiellini, C. 2009 WNT/beta-catenin signalling and epithelial patterning in the homoscleromorph sponge Oscarella. PLoS One 4, e5823. (doi:10.1371/journal.pone.0005823)
45. Larroux, C., Fahey, B., Liubicich, D., Hinman, V. F., Gongora, M., Green, K. M., Wö rheide, G., Leys, S. P. Degnan, B. M. 2006 Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity. Evol. Dev. 8, 150-173. (doi:10.1111/j.1525- 142X.2006.00086.x)
46. Larroux, C., Fahey, B., Degnan, S. M., Adamski, M., Rokhsar, D. S. Degnan, B. M. 2007 NK homeobox gene cluster predates the origin of Hox genes. Curr. Biol. 17, 706-710. (doi:10.1016/j.cub.2007.03.008) (Pubitemid 46552249)
47. Larroux, C., Luke, G. N., Koopman, P., Rokhsar, D. S., Shimeld, S. M. Degnan, B. M. 2008 Genesis and expansion of metazoan transcription factor gene families and classes. Mol. Biol. Evol. 25, 980-996. (doi:10.1093/molbev/msn047)
48. Leys, S. P. 2004 Gastrulation in sponges. In Gastrulation: from cells to embryo (ed. C. D. Stern), pp. 23-32. New York, NY: Cold Spring Harbor Laboratory Press.
49. Leys, S. P. Degnan, B. M. 2001 The cytological basis of photoresponsive behavior in a sponge larva. Biol. Bull. 201, 323-338. (doi:10.2307/1543611)
50. Leys, S. P. Degnan, B. M. 2002 Embryogenesis and metamorphosis in a haplosclerid demosponge: gastrulation and transdifferentiation of larval ciliated cells to choanocytes. Invert. Biol. 121, 171-189.
51. Leys, S. P. Ereskovsky, A. E. 2006 Embryogenesis and larval differentiation in sponges. Can. J. Zool. 84, 262-287. (doi:10.1139/z05-170) (Pubitemid 43900035)
52. Leys, S. P., Cronin, T. W., Degnan, B. M. Marshall, J. N. 2002 Spectral sensitivity in a sponge larva. J. Comp. Physiol. A 188, 199-202. (doi:10.1007/s00359-002-0293-y) (Pubitemid 36251073)
53. Li, C., Chen, J. Hua, T. 1998 Precambrian sponges with cellular structures. Science 279, 879-882. (doi:10.1126/science.279.5352.879) (Pubitemid 28106285)
54. Love, G. D. et al. 2009 Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457, 718-721. (doi:10.1038/nature07673)
55. Maldonado, M. 2006 Ecology of the sponge larva. Can. J. Zool. 84, 175-194. (doi:10.1139/z05-177) (Pubitemid 43900030)
56. Marlow, H. Q., Srivastava, M., Matus, D. Q., Rokhsar, D. Martindale, M. Q. 2009 Anatomy and development of the nervous system of Nematostella vectensis, an anthozoan cnidarian. Dev. Neurobiol. 69, 235-254. (doi:10.1002/dneu.20698)
57. Matus, D. Q., Pang, K., Daly, M. Martindale, M. Q. 2007 Expression of Pax gene family members in the anthozoan cnidarian, Nematostella vectensis. Evol. Dev. 9, 25-38.
58. Mazza, M. E., Pang, K., Martindale, M. Q. Finnerty, J. R. 2007 Genomic organization, gene structure, and developmental expression of three clustered otx genes in the sea anemone Nematostella vectensis. J. Exp. Zool. (Mol. Dev. Evol.) 308B, 494-506.
59. Minelli, A. 2009 Perspectives in animal phylogeny and evolution. Oxford, UK: Oxford University Press.
60. Morse, D. E. Morse, A. N. C. 1991 Enzymatic characterization of the morphogen recognized by Agaricia humilis (scleractinian coral) larvae. Biol. Bull. 181, 104-122. (doi:10.2307/1542493)
61. Nei, M., Niimura, Y. Nozawa, M. 2008 The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity. Nat. Rev. Genet. 9, 951-963. (doi:10.1038/nrg2480) (Pubitemid 50329069)
62. Nichols, S. A., Dirks,W., Pearse, J. S. King, N. 2006 Early evolution of animal cell signaling and adhesion genes. Proc. Natl Acad. Sci. USA 103, 12 451-12 456. (doi:10.1073/pnas.0604065103) (Pubitemid 44267280)
63. Pang, K. & Martindale, M. Q. 2008 Developmental expression of homeobox genes in the ctenophore Mnemiopsis leidyi. Dev. Genes Evol. 218, 307-319. (doi:10.1007/s00427-008-0222-3)
64. Pawlik, J. R. 1992 Chemical ecology of the settlement of benthic marine invertebrates. Oceanogr. Mar. Biol. 30, 273-335.
65. Pechenik, J. A. 2006 Larval experience and latent effects- metamorphosis is not a new beginning. Integr. Comp. Biol. 46, 323-333. (doi:10.1093/icb/ icj028) (Pubitemid 44290597)
66. Pechenik, J. A. Gee, C. C. 1993 Onset of metamorphic competence in larvae of the gastropod Crepidula fornicate (L.), judged by a natural and an artificial cue. J. Exp. Mar. Biol. Ecol. 167, 59-72. (doi:10.1016/0022-0981(93) 90184-P)
67. Pechenik, J. A. Heyman, W. D. 1987 Using KCl to determine size at competence for larvae of the marine gastropod Crepidula fornicata (L.). J. Exp. Mar. Biol. Ecol. 112, 27-38. (doi:10.1016/S0022-0981(87)80012-6)
68. Pechenik, J. A. Qian, P. Y. 1998 Onset and maintenance of metamorphic competence in the marine polychaete Hydroides elegans Haswell in response to three chemical cues. J. Exp. Mar. Biol. Ecol. 226, 51-74. (doi:10.1016/S0022- 0981(97)00237-2) (Pubitemid 28268251)
69. Philippe, H. et al. 2009 Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 19, 706-712. (doi:10.1016/j.cub.2009.02.052)
70. Putnam, N. H. et al. 2007 Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317, 86-94. (doi:10.1126/science.1139158) (Pubitemid 47056460)
71. Raible, F., Tessmar-Raible, K., Arboleda, E., Kaller, T., Bork, P., Arendt, D. Arnone, M. I. 2006 Opsins and clusters of sensory G-protein-coupled receptors in the sea urchin genome. Dev. Biol. 300, 461-475. (doi:10.1016/j.ydbio.2006.08.070) (Pubitemid 44834389)
72. Raimondi, P. T. Keough, M. J. 1990 Behavioural variability in marine larvae. Aust. J. Ecol. 15, 427-437. (doi:10.1111/j.1442-9993.1990.tb01468.x)
73. Rentzsch, F., Fritzenwanker, J. H., Scholz, C. B. Technau, U. 2008 FGF signalling controls formation of the apical sensory organ in the cnidarian Nematostella vectensis. Development 135, 1761-1769. (doi:10.1242/dev.020784)
74. Richards, G. S., Simionato, E., Perron, M., Adamska, M., Vervoort, M. Degnan, B. M. 2008 Sponge genes provide new insight into the evolutionary origin of the neurogenic circuit. Curr. Biol. 18, 1156-1161. (doi:10.1016/j.cub.2008. 06.074)
75. Rodriguez, S. R., Ojeda, F. P. Inestrosa, N. C. 1993 Settlement of benthic marine invertebrates. Mar. Ecol. Prog. Ser. 97, 193-207. (doi:10.3354/meps097193)
76. Sakarya, O. et al. 2007 A post-synaptic scaffold at the origin of the animal kingdom. PLoS One 2, e506. (doi:10.1371/journal.pone.0000506)
77. Schierwater, B., Eitel, M., Jakob, W., Osigus, H. J., Hadrys, H., Dellaporta, S. L., Kolokotronis, S. O. Desalle, R. 2009 Concatenated analysis sheds light on early metazoan evolution and fuels a modern 'urmetazoon' hypothesis. PLoS Biol. 7, e20. (doi:10.1371/journal.pbio.1000020)
78. Simionato, E., Ledent, V., Richards, G., Thomas-Chollier, M., Kerner, P., Coornaert, D., Degnan, B. M. Vervoort, M. 2007 Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics. BMC Evol. Biol. 7, 33. (doi:10.1186/1471-2148-7-33) (Pubitemid 46434556)
79. Sly, B. J., Snoke, S. S. Raff, R. A. 2003 Who came first- larvae or adults? Origins of bilaterian metazoan larvae. Int. J. Dev. Biol. 47, 623-632.
80. Srivastava, M. et al. 2008 The Trichoplax genome and the nature of placozoans. Nature 454, 955-960. (doi:10.1038/nature07191)
81. Strathmann, R. 1974 The spread of sibling larvae of sedentary marine invertebrates. Am. Nat. 108, 29-44. (doi:10.1086/282883)
82. Sutherland, J. P. 1990 Recruitment regulates demographic variation in a tropical intertidal barnacle. Ecology 71, 955-972. (doi:10.2307/1937365)
83. Todd, C. D. 1990 Larval supply and recruitment of benthic invertebrates: do larvae always disperse as much as we believe? Hydrobiologica 376, 1-21. (doi:10.1023/A:1017007527490)
84. Todd, C. D., Lambert, W. J. Thorpe, J. P. 1998 The genetic structure of intertidal populations of two species of nudibranch molluscs with planktotrophic and pelagic lecithotrophic larval stages: are pelagic larvae 'for' dispersal? J. Exp. Mar. Biol. Ecol. 228, 1-28. (doi:10.1016/S0022-0981(98)00005-7) (Pubitemid 28457933)
85. Toonen, R. J. Pawlik, J. R. 2001 Foundations of gregariousness: a dispersal polymorphism among the planktonic larvae of a marine invertebrate. Evolution 55, 2439-2454.
86. Trapido-Rosenthal, H. G. Morse, D. E. 1986a Availability of chemosensory receptors is down-regulated by habituation of larvae to a morphogenetic signal. Proc. Natl Acad. Sci. USA 83, 7658-7662. (doi:10.1073/pnas.83.20.7658) (Pubitemid 17183907)
87. Trapido-Rosenthal, H. G. Morse, D. E. 1986b Regulation of receptor-mediated settlement and metamorphosis in larvae of a gastropod mollusc (Haliotis rufescens). Bull. Mar. Sci. 39, 383-392.
88. Underwood, A. J. Keough, M. J. 2001 Supply-side ecology: the nature and consequences of variations in recruitment of intertidal organisms. In Marine community ecology (eds M. D. Bertness, S. D. Gaines M. E. Hay), pp. 183-200. Sunderland, Maine: Sinauer Associates, Inc.
89. Valentine, J. W. 2004 On the origin of phyla. Chicago, IL: The University of Chicago Press.
90. Williams, E. A. Degnan, S. M. 2009 Carry-over effect of larval settlement cue on postlarval gene expression in the marine gastropod Haliotis asinina. Mol. Ecol. 18, 4434-4449. (doi:10.1111/j.1365-294X.2009.04371.x)
91. Williams, E. A., Craigie, A., Yeates, A. Degnan, S. M. 2008 Articulated coralline algae of the genus Amphiroa are highly effective natural inducers of settlement in the tropical abalone Haliotis asinina. Biol. Bull. 215, 98-107.
92. Williams, E. A., Degnan, B. M., Gunter, H., Jackson, D. J., Woodcroft, B. J. Degnan, S. M. 2009 Widespread transcriptional changes pre-empt the critical pelagic-benthic transition in the vetigastropod Haliotis asinina. Mol. Ecol. 18, 1006-1025. (doi:10.1111/j.1365-294X.2008.04078.x)
93. Woodman, P. 2009 ESCRT proteins, endosome organization and mitogenic receptor down-regulation. Biochem. Soc. Trans. 37, 146-150. (doi:10.1042/ BST0370146)
94. Woods, R. G., Roper, K. E., Gauthier, M., Bebell, L. M., Sung, K., Degnan, B. M. Lavin, M. F. 2004 Gene expression during early ascidian metamorphosis requires signalling by Hemps, an EGF-like protein. Development 131, 2921-2933. (doi:10.1242/dev.01120) (Pubitemid 38997280)
95. Wray, G. A. Lowe, C. J. 2000 Developmental regulatory genes and echinoderm evolution. Syst. Biol. 49, 28-51. (doi:10.1080/10635150050207375)
96. Yamada, A., Pang, K., Martindale, M. Q. Tochinai, S. 2007 Surprisingly complex T-box gene complement in diploblastic metazoans. Evol. Dev. 9, 220-230.
97. Zhang, S. M., Adema, C. M., Kepler, T. B. Loker, E. S. 2004 Diversification of Ig superfamily genes in an invertebrate. Science 305, 251-254. (doi:10.1126/science.1088069) (Pubitemid 38886740)