Modularity, comparative embryology and evo-devo: Developmental dissection of evolving body plans

Developmental Biology

Volumn 332, Issue 1, 2009, Pages 61-69

  Kuratani, Shigeru ^a  

^a RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

Body plan; Developmental constraints; Evolution; Evolutionary novelty; Modularity; Morphological homology

Indexed keywords

COMPARATIVE ANATOMY; CRANIOFACIAL DEVELOPMENT; CRANIOFACIAL MORPHOLOGY; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EMBRYO SEGMENTATION; EVOLUTIONARY ADAPTATION; EVOLUTIONARY HOMOLOGY; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENOTYPE; LAMPREY; LIMB DEVELOPMENT; MORPHOGENESIS; MORPHOLOGICAL ADAPTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW;

EID: 67649884543     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.05.564     Document Type: Review

References (96)

1. Appel T.A. The Cuvier-Geoffroy Debate: French Biology in the Decades before Darwin (Monographs on the History and Philosophy of Biology) (1987), Oxford Univ. Press, New York
2. Arendt D. The evolution of cell types in animals: emerging principles from molecular studies. Nat. Rev. Genet. 9 (2008) 868-882
3. de Beer G.R. The segmentation of the head in Squalus acanthias. Quart. J. Microsc. Sci. 66 (1922) 457-474
4. de Beer G.R. The Development of the Vertebrate Skull (1937), Oxford Univ Press, London
5. de Beer G.R. Embryos and Ancestors (1958), Oxford Univ. Press, Oxford
6. de Beer G.R. In: Head J.J., and Lowenstein O.E. (Eds). Homology, An Unsolved Problem, Oxford Biology Readers (1971), Oxford Univ. Press, Oxford
7. Begbie J., Brunet J.F., Rubenstein J.L., and Graham A. Induction of the epibranchial placodes. Development 126 (1999) 895-902
8. Bellairs A.D.'A., and Gans C. A reinterpretation of the amphisbaenian orbitosphenoid. Nature 302 (1983) 243-244
9. Brito J.M., Teillet M.A., and Le Douarin N.M. An early role for sonic hedgehog from foregut endoderm in jaw development: ensuring neural crest cell survival. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 11607-11612
10. Brito J.M., Teillet M.A., and Le Douarin N.M. Induction of mirror-image supernumerary jaws in chicken mandibular mesenchyme by Sonic Hedgehog-producing cells. Development 135 (2008) 2311-2319
11. Burke A.C., Nelson C.E., Morgan B.A., and Tabin C. Hox genes and the evolution of vertebrate axial morphology. Development 121 (1995) 333-346
12. Carroll S.B. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134 (2008) 25-36
13. Carroll S.B., Greiner J.K., and Weatherbee S.D. From DNA to Diversity (2001), Blackwell Sci., Victoria
14. Cerny R., Lwigale P., Ericsson R., Meuleman D., Epperlein H.H., and Bronner-Fraser M. Developmental origins and evolution of jaws: new interpretation of "maxillary" and "mandibular". Dev. Biol. 276 (2004) 225-236
15. Cohn M.J., and Tickle C. Developmental basis of limblessness and axial patterning in snakes. Nature 399 (1999) 474-479
16. Couly G., Grapin-Botton A., Coltey P., Ruhin B., and Le Douarin N.M. Determination of the identity of the derivatives of the cephalic neural crest: incompatibility between Hox gene expression and lower jaw development. Development 125 (1998) 3445-3459
17. Darwin C. The Origin of Species by Means of Natural Selection (1859), John Murray, London
18. Denes A.S., Jékely G., Steinmetz P.R., Raible F., Snyman H., Prud homme B., Ferrier D.E., Balavoine G., and Arendt D. Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria. Cell 129 (2007) 277-288
19. Depew M.J., Lufkin T., and Rubenstein J.L. Specification of jaw subdivisions by Dlx genes. Science 298 (2002) 371-373
20. Dollé P., Izpisúa-Belmonte J.C., Falkenstein H., Renucci A., and Duboule D. Coordinate expression of the murine Hox-5 complex homoeobox-containing genes during limb pattern formation. Nature 342 (1989) 767-772
21. Duboule D. Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Dev. Suppl. 1994 (1994) 135-142
22. Echevarría D., Vieira C., Gimeno L., and Martínez S. Neuroepithelial secondary organizers and cell fate specification in the developing brain. Brain Res. Brain Res. Rev. 43 (2003) 179-191
23. Ferguson C.A., Tucker A.S., and Sharpe P.T. Temporospatial cell interactions regulating mandibular and maxillary arch patterning. Development 127 (2000) 403-421
24. Fürbringer M. Über die spino-occipitalen Nerven der Selachier und Holocephalen ind ihre vergleichende Morphologie. Festschr. für Carl Gegenbaur 3 (1897) 349-788
25. Galis F., and Sinervo B. Conserved early embryonic stages. In: Hall B.K., and Olson W.M. (Eds). Keywords and Concepts in Evolutionary Developmental Biology (2003), Harvard Univ. Press, Cambridge 43-52
26. Garcia-Fernàndez J. The genesis and evolution of homeobox gene clusters. Nat. Rev. Genet. 6 (2005) 881-892
27. Gegenbaur C. Die Metamerie des Kopfes und die Wirbeltheorie des Kopfskelets. Morphol. Jb. 13 (1887) 1-114
28. Gegenbaur C. Vergleichende Anatomie der Wirbeltihiere mit Berücksichtung der Wirbellosen (1898), Verlag von Wilhelm Engelmann, Leipzig
29. Gendron-Maguire M., Mallo M., Zhang M., and Gridley T. Hoxa-2 mutant mice exhibit homeotic transformation of skeletal elements derived from cranial neural crest. Cell 75 (1993) 1317-1331
30. Geoffroy Saint-Hilaire E. Philosophie Anatomique (tome premiere) (1818), J.B. Baillière, Paris
31. Gilbert SF. Developmental Biology. 7th Ed. (2006), Sinauer Associates, Inc, Sunderland, Massachusetts
32. Goodrich E.S. Studies on the Structure and Development of Vertebrates (1930), McMillan, London
33. Haeckel E. Anthropogenie oder Entwickelungsgeschichte des Menschen. Keimes- und Stammesgeschichte (1874), Wilhelm Engelmann, Leipzig
34. Haeckel E. Die Gastrea und die Eifurchung der Thiere. Jena Z. Naturwiss. 9 (1875) 402-508
35. Haeckel E. Natürliche Schöpfungs-Gechichte-Gemeinverständliche wissenschaftliche Verträge über die Entwickelungs-Lehre (1902), Druck und Verlag von Georg Reimer, Berlin
36. Hall B.K. Homology: The Hierarchical Basis of Comparative Biology (1994), Academic Press, San Diego
37. Hall B.K. Evolutionary Developmental Biology, 2nd Ed (1998), Chapman & Hall, London
38. Holland N.D., Holland L.Z., Honma Y., and Fujii T. Engrailed expression during development of a lamprey, Lampetra japonica: a possible clue to homologies between agnathan and gnathostome muscles of the mandibular arch. Dev. Growth Differ. 35 (1993) 153-160
39. Holzschuh J., Wada N., Wada C., Schaffer A., Javidan Y., Tallafuss A., Bally-Cuif L., and Schilling T.F. Requirements for endoderm and BMP signaling in sensory neurogenesis in zebrafish. Development 132 (2005) 3731-3742
40. Horigome N., Myojin M., Hirano S., Ueki T., Aizawa S., and Kuratani S. Development of cephalic neural crest cells in embryos of Lampetra japonica, with special reference to the evolution of the jaw. Dev. Biol. 207 (1999) 287-308
41. Janvier P. Early Vertebrates (1996), Oxford Scientific Publications, New York
42. Kessel M. Respecification of vertebral identities by retinoic acid. Development 115 (1992) 487-501
43. Kessel M., Galling R., and Gruss P. Variations of cervical vertebrate after expression of a Hox-1.1 transgene in mice. Cell 61 (1990) 301-308
44. Keynes R.J., and Stern C.D. Segmentation in the vertebrate nervous system. Nature 310 (1984) 786-789
45. Klingenberg C.P. Morphological integration and developmental modularity. Ann. Ecol. Evol. Syst. 39 (2008) 115-132
46. Kuratani S. Evolutionary developmental biology and vertebrate head segmentation: a perspective from developmental constraint. Theory Biosci. 122 (2003) 230-251
47. Kuratani S. Evolution of the vertebrate jaw: comparative embryology reveals the developmental factors behind the evolutionary novelty. J. Anat. 205 (2004) 335-347
48. Kuratani S. Cephalic crest cells and evolution of the craniofacial structures in vertebrates: morphological and embryological significance of the premandibular-mandibular boundary. Zoology 108 (2005) 13-26
49. Kuratani S. Is the vertebrate head segmented?-evolutionary and developmental considerations. Integ. Comp. Biol. 48 (2008) 647-657
50. Kuratani S.C., and Kirby M.L. Initial migration and distribution of the cardiac neural crest in the avian embryo: an introduction to the concept of the circumpharyngeal crest. Am. J. Anat. 191 (1991) 215-227
51. + crest cells in the vertebrate head region. Anat. Rec. 234 (1992) 263-280
52. Kuratani S., and Ota G.K. The primitive versus derived traits in the developmental program of te vertebrate head: views from cyclostome developmental studies. J. Exp. Zool. (Mol. Dev. Evol.) 310B (2008) 294-314
53. Kuratani S., Horigome N., and Hirano S. Developmental morphology of the cephalic mesoderm and re-evaluation of segmental theories of the vertebrate head: evidence from embryos of an agnathan vertebrate, Lampetra japonica. Dev. Biol. 210 (1999) 381-400
54. Kuratani S., Nobusada Y., Horigome N., and Shigetani Y. Embryology of the lamprey and evolution of the vertebrate jaw: insights from molecular and developmental perspectives. Phil. Trans. Roy. Soc. 356 (2001) 15-32
55. Kuratani S., Murakami Y., Nobusada Y., Kusakabe R., and Hirano S. Developmental fate of the mandibular mesoderm in the lamprey, Lethenteron japonicum: comparative morphology and development of the gnathostome jaw with special reference to the nature of trabecula cranii. J. Exp. Zool. (Mol. Dev. Evol.) 302B (2004) 458-468
56. Larsson H.C.E., and Wagner G.P. Pentadactyl ground state of the avian wing. J. Exp. Zool. (Mol. Devel. Evol.) 294 (2002) 146-151
57. Lee S.H., Bédard O., Buchtová M., Fu K., and Richman J.M. A new origin for the maxillary jaw. Dev. Biol. 276 (2004) 207-224
58. Lowe C.J., Wu M., Salic A., Evans L., Lander E., Stange-Thomann N., Gruber C.E., Gerhart J., and Kirschner M. Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 113 (2003) 853-865
59. Mallatt J. The origin of the vertebrate jaw: neoclassical ideas versus newer, development-based ideas. Zool. Sci. 25 (2008) 990-998
60. Matsuura M., Nishihara H., Kokubo N., Kuraku S., Kusakabe R., Okada N., Kuratani S., and Tanaka M. Identification of four Engrailed genes in the Japanese river lamprey, Lethenteron japonicum. Dev. Dyn. 237 (2008) 1581-1589
61. Maynard-Smith J., Burian R., Kauffman S., Alberch P., Campbell J., Goodwin B., Lande R., Raup D., and Wolpert L. Developmental constraints and evolution. Quart. Rev. Biol. 60 (1985) 265-287
62. Müller G.B., and Wagner G.P. Novelty in evolution: restructuring the concept. Annu. Rev. Ecol. Syst. 22 (1991) 229-256
63. Murakami Y., Ogasawara M., Satoh N., Sugahara F., Myojin M., Hirano S., and Kuratani S. Compartments in the lamprey embryonic brain as revealed by regulatory gene expression and the distribution of reticulospinal neurons. Brain Res. Bull. 57 (2002) 271-275
64. Naiche L.A., and Papaioannou V.E. Tbx4 is not required for hindlimb identity or post-bud hindlimb outgrowth. Development 134 (2007) 93-103
65. Neidert A.H., Virupannavar V., Hooker G.W., and Langeland J.A. Lamprey Dlx genes and early vertebrate evolution. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 1665-1670
66. Neubüser A., Peters H., Balling R., and Martin G.R. Antagonistic interactions between FGF and BMP signalling pathways: a mechanism for positioning the site of tooth formation. Cell 90 (1997) 247-255
67. Ohya Y.K., Kuraku S., and Kuratani S. Hox code in embryos of Chinese soft-shelled turtle Pelodiscus sinensis correlates with the evolutionary innovation in the turtle. J. Exp. Zool. (Mol. Dev. Evol.) 304B (2005) 107-118
68. Owen, R., 1848. On the Archetype and Homologies of the Vertebrate Skeleton. London.
69. Raff R.A. The Shape of Life (1996), The University of Chicago Press, Chicago
70. Rickmann M., Fawcett J., and Keynes R.J. The migration of neural crest cells and the growth of motor axons through the rostral half of the chick somite. J. Embryol. Exp. Morphol. 90 (1985) 437-455
71. Rijli F.M., Mark M., Lakkaraju S., Dierich A., Dollé P., and Chambon P. Homeotic transformation is generated in the rostral branchial region of the head by disruption of Hoxa-2, which acts as a selector gene. Cell 75 (1993) 1333-1349
72. De Robertis E. Evo-devo: variations on ancestral themes. Cell 132 (2008) 185-195
73. Rodriguez-Esteban C., Tsukui T., Yonei S., Magallon J., Tamura K., and Izpisua-Belmonte J.C. The T-box genes Tbx4 and Tbx5 regulate limb outgrowth and identity. Nature 398 (1999) 814-818
74. Schlosser G., and Wagner G.P. Modularity-in development and evolution (2004), Univ. Chicago Press, Chicago
75. Scholtz G. Homology and ontogeny: pattern and process in comparative developmental biology. Theory Biosci. 124 (2005) 121-143
76. Schwenk K., and Wagner G.P. Constraint. In: Hall B.K., and Olson W.M. (Eds). Keywords and Concepts in Evolutionary Developmental Biology (2003), Harvard Univ. Press, Cambridge 52-61
77. Shigetani Y., Nobusada Y., and Kuratani S. Ectodermally-derived FGF8 defines the maxillomandibular region in the early chick embryo: epithelial-mesenchymal interactions in the specification of the craniofacial ectomesenchyme. Dev. Biol. 228 (2000) 73-85
78. Shigetani Y., Sugahara F., Kawakami Y., Murakami Y., Hirano S., and Kuratani S. Heterotopic shift of epithelial-mesenchymal interactions for vertebrate jaw evolution. Science 296 (2002) 1316-1319
79. Shigetani Y., Sugahara F., and Kuratani S. Evolutionary scenario of the vertebrate jaw: the heterotopy theory from the perspectives of comparative and molecular embryology. BioEssays 27 (2005) 331-338
80. Takeuchi J.K., Koshiba-Takeuchi K., Matsumoto K., Vogel-Hopker A., Naitoh-Matsuo M., Ogura K., Takahashi N., Yasuda K., and Ogura T. Tbx5 and Tbx4 genes determine the wing/leg identity of limb buds. Nature 398 (1999) 810-814
81. Takio, Y., Pasqualetti, M., Kuraku, S., Hirano, S., M., Rijli, F., Kuratani, S., 2004. Lamprey Hox genes and the evolution of jaws. Nature OnLine 429, 1 p following 262. http://www.nature.com/cgi-taf/DynaPage.taf?file=/nature/journal/v429/n6989/full/nature02616_fs.htm006C.
82. Takio Y., Kuraku S., Kusakabe R., Murakami Y., Pasqualetti M., Rijli F.M., Narita Y., Kuratani S., and Kusakabe R. Hox gene expression patterns in Lethenteron japonicum embryos insights into the evolution of the vertebrate Hox code. Dev. Biol. 308 (2007) 606-620
83. Tucker A.S., Matthews K.L., and Sharpe P.T. Transformation of tooth type induced by inhibition of BMP signaling. Science 282 (1998) 1136-1138
84. Uchida K., Murakami Y., Kuraku S., Hirano S., and Kuratani S. Development of the adenohypophysis in the lamprey: evolution of the epigenetic patterning programs in organogenesis. J. Exp. Zool. (Mol. Dev. Evol.) 300B (2003) 32-47
85. von Baer K.E. Entwicklungsgeschichte der Thiere: Beobachtung und Reflexion (1828), Born Träger, Königsberg
86. Wada N., Javidan Y., Nelson S., Carney T.J., Kelsh R.N., and Schilling T.F. Hedgehog signaling is required for cranial neural crest morphogenesis and chondrogenesis at the midline in the zebrafish skull. Development 132 (2005) 3977-3988
87. Waddington C.H. The Evolution of an Evolutionist (1975), Cornell Univ. Press, Ithaca, New York
88. Wagner G.P. The origin of morphological characters and the biological basis of homology. Evolution 43 (1989) 1157-1171
89. Wagner G.P. The biological homology concept. Annu. Rev. Ecol. Syst. 20 (1989) 51-60
90. Wagner G.P. Homology and the mechanisms of development. In: Hall B.K. (Ed). Homology: The Hierarchical Basis of Comparative Biology (1994), Academic Press, San Diego 273-299
91. Wagner G.P. The developmental genetics of homology. Nat. Rev. 8 (2007) 473-479
92. Wagner G.P., and Altenberg L. Perspective: complex adaptations and the evolution of evolvability. Evolution 50 (1996) 967-976
93. Wagner G.P., and Müller G.B. Evolutionary innovations overcome ancestral constraints: a re-examination of character evolution in male sepsid flies (Diptera: Sepsidae). Evol. Dev. 4 (2002) 1-6
94. Wagner G.P., Pavlicev M., and Cheverud J.M. The road to modularity. Nat. Rev. 8 (2007) 921-931
95. Woodger J.H. On biological transformations. In: Le Gros Clark W.E., and Medawar P.B. (Eds). Essays on Growth and Form Presented to D'Arcy Thompson (1945), Cambridge Univ. Press, Cambridge 95-120
96. Yokouchi Y., Sasaki H., and Kuroiwa A. Homeobox gene expression correlated with the bifurcation process of limb cartilage development. Nature 353 (1991) 443-445