Nuclear β-catenin localization supports homology of feathers, avian scutate scales, and alligator scales in early development

Evolution and Development

Volumn 17, Issue 3, 2015, Pages 185-194

  Musser, Jacob M ^a   Wagner, Günter P ^a   Prum, Richard O ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANATOMY; BIRD; CROCODILIAN; EPIDEMIC; EVOLUTIONARY BIOLOGY; FEATHER; HOMOLOGY; MOLECULAR ANALYSIS; PALEONTOLOGY; SIGNAL; SKIN;

ALLIGATOR; AMNIOTA; AVES; DINOSAURIA; MAMMALIA; REPTILIA;

BETA CATENIN;

ANATOMY AND HISTOLOGY; ANIMAL; ANIMAL STRUCTURES; BIRD; CHEMISTRY; CROCODILIAN; CYTOLOGY; EMBRYOLOGY; EVOLUTION; FEATHER; GENETICS;

ALLIGATORS AND CROCODILES; ANIMAL STRUCTURES; ANIMALS; BETA CATENIN; BIOLOGICAL EVOLUTION; BIRDS; FEATHERS;

EID: 84929163244     PISSN: 1520541X     EISSN: 1525142X     Source Type: Journal    
DOI: 10.1111/ede.12123     Document Type: Article

References (63)

1. Aberle, H., Schwartz, H. and Kemler, R. 1996. Cadherin-catenin complex: protein interactions and their implications for cadherin function. J Cell Biochem 61: 514-523.
2. Alibardi, L. 1996. Scale morphogenesis during embryonic development in the lizard Anolis lineatopus. J Anat 188: 713-725.
3. Alibardi, L. 2006. Cells of embryonic and regenerating germinal layers within barb ridges: implication for the development, evolution and diversification of feathers. J Submicrosc Cytol Pathol 38: 51-76.
4. Alibardi, L. and Thompson, M. B. 2000. Scale morphogenesis and ultrastructure of dermis during embryonic development in the alligator (Alligator mississippiensis, Crocodilia, Reptilia). Acta Zoologica 81: 325-338.
5. Arendt, D. 2008. The evolution of cell types in animals: emerging principles from molecular studies. Nat Rev Genet 9: 868-882.
6. Brush, A. H. 2000. Evolving a protofeather and feather diversity. American Zoologist 40: 631-639.
7. Chapman, R. E. 1986. Hair, wool, quill, nail, claw, hoof and horn. In J. Bereither-Hahn, A.G. Matoltsy, and K.S. Richards (eds.) Biology of the integument Vol. 2, vertebrates. Springer-Verlag, New York, pp. 293-312.
8. Chodankar, R., Chang, C. H., Yue, Z., Jiang, T. X., Suksaweang, S., Burrus, L., Chuong, C. M. and Widelitz, R. 2003. Shift of localied growth zones contributes to skin appendage morphogenesis: role of the Wnt/B-catenin pathway. J Invest Dermatol 120: 20-26.
9. Chu, E. Y., Hens, J., Andl, T., Kairo, A., Yamaguchi, T. P., Brisken, C., Glick, A., Wysolmerski, J. J. and Millar, S. E. 2004. Canonical WNT signaling promotes mammary placode development and is essential for initiation of mammary gland morphogenesis. Development 131: 4819-4829.
10. Chuong, C. M., Chodankar, R., Widelitz, R. B. and Jiang, T. X. 2000. Evo-devo of feathers and scales: building complex epithelial appendages. Curr Opin Genet Dev 10: 449-456.
11. Clarke, J. 2013. Feathers before flight. Science 340: 690-692.
12. Clevers, H. 2006. Wnt/Β-catenin signaling in development and disease. Cell 127: 469-480.
13. Crawford, N. G., Faircloth, B. C., McCormack, J. E., Brumfield, R. T., Winker, K. and Glenn, T. C. 2012. More than 1000 ultraconserved elements provide evidence that turtles are the sister group of archosaurs. Biol Lett 8: 783-786.
14. Crowe, R. and Niswander, L. 1998. Disruption of scale development by Delta-1 misexpression. Dev Biol 195: 70-74.
15. DasGupta, R. and Fuchs, E. 1999. Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126: 4557-4568.
16. Davies, H. R. 1889. Die entwicklung der feder und ihre beziehungen zu anderen integumentgebilden. Morphol Jahrbuch (Gegenbaur) 15: 560-645.
17. Dhouailly, D. 2009. A new scenario for the evolutionary origin of hair, feather, and avian scales. J Anat 214: 587-606.
18. Ferguson, M. W. J. 1985. The reproductive biology and embryology of crocodilians. In C. Gans, F. Billett, and P.F.A. Maderson (eds.) Biology of the reptilia, vol. 14, development B. John Wiley & Sons, New York, pp. 329-491.
19. Geeta, R. 2003. Structure trees and species trees: what they say about morphological development and evolution. Evol Dev 5: 609-621.
20. Hamburger, V. and Hamilton, H. L. 1951. A series of normal stages in the development of the chick embryo. J Morphol 88: 49-92.
21. Hardy, M. H. 1992. The secret life of the hair follicle. Trends Genet 8: 55-61.
22. Harris, M. P., Fallon, J. F. and Prum, R. O. 2002. Shh-Bmp2 signaling module and the evolutionary origin and diversification of feathers. J Exp Zool (Mol Dev Evol) 294B: 160-176.
23. Harris, M. P., Williamson, S., Fallon, J. F., Meinhardt, H. and Prum, R. O. 2005. Molecular evidence for an activator-inhibitor mechanism in development of embryonic feather branching. Proc Natl Acad Sci USA 102: 11734-11739.
24. Ji, Q., Norell, M. A., Gao, K. Q., Ji, S. A. and Ren, D. 2001. The distribution of integumentary structures in a feathered dinosaur. Nature 410: 1084-1088.
25. Li, A., Chen, M., Jiang, T. X., Wu, P., Nie, Q., Widelitz, R. B. and Chuong, C. M. 2013. Shaping organs by a wingless-int/Notch/nonmuscle myosin module which orients feather bud elongation. Proc Natl Acad Sci USA 110: E1452-E1461.
26. Li, Q., Gao, K. Q., Vinther, J., Shawkey, M. D., Clarke, J. A., D'Alba, L., Meng, Q., Briggs, D. E. G. and Prum, R. O. 2010. Plumage color patterns of an extinct dinosaur. Science 327: 1369-1372.
27. Lim, X. and Nusse, R. 2013. Wnt signaling in skin development, homeostasis, and disease. Cold Spring Harb Perspect Biol 5: a008029.
28. Lucas, A. M. and Stettenheim, P. R. 1972. Avian anatomy: integument. US Dept. Agricult. Handbook 362, Washington DC.
29. Maderson, P. F. A. 1965. The embryonic development of the squamate integument. Acta Zoologica 46: 275-295.
30. Maderson, P. F. A. and Sawyer, R. H. 1979. Scale embryogenesis in birds and reptiles. Anat Rec 193: 609-609.
31. Müller, G. B. and Wagner, G. P. 1991. Novelty in evolution: restructuring the concept. Annu Rev Ecol Syst 22: 229-256.
32. Noramly, S., Freeman, A. and Morgan, B. A. 1999. β-catenin signaling can initiate feather bud development. Development 126: 3509-3521.
33. Norell, M.A and Xu, X. 2005. Feathered dinosaurs. Annu Rev Earth Planet Sci 33: 277-299.
34. Oakley, T. H. 2003. The eye as a replicating and diverging, modular developmental unit. Trends Ecol Evol 18: 623-627.
35. Prin, F., Logan, C., D'Souza, D., Ensini, M. and Dhouailly, D. 2004. Dorsal versus ventral scales and the dorsoventral patterning of chick foot epidermis. Dev Dynam 229: 564-578.
36. Prum, R. O. 1999. Development and evolutionary origin of feathers. J Exp Zool (Mol Dev Evol) 285B: 291-306.
37. Prum, R. O. 2005. Evolution of the morphological innovations of feathers. J Exp Zool (Mol Dev Evol) 304B: 570-579.
38. Prum, R. O. and Brush, A. H. 2002. The evolutionary origin and diversification of feathers. Q Rev Biol 77: 261-295.
39. Ridanpää, M., Fodde, R. and Kielman, M. 2001. Dynamic expression and nuclear accumulation of β-catenin during the development of hair follicle-derived structures. Mech Dev 109: 173-181.
40. Sawyer, R. H. 1972a. Avian scale development. 1. Histogenesis and morphogenesis of epidermis and dermis during formation of the scale ridge. J Exp Zool 181: 365-383.
41. Sawyer, R. H. 1972b. Avian scale development. II. Study of cell proliferation. J Exp Zool 181: 385-407.
42. Sawyer, R. H. and Craig, K. F. 1977. Avian scale development. Absence of an "epidermal placode" in reticulate scale morphogenesis. J Morphol 154: 83-93.
43. Sawyer, R. H. and Knapp, L. W. 2003. Avian skin development and the evolutionary origin of feathers. J Exp Zool (Mol Dev Evol) 298B: 57-72.
44. Sawyer, R. H., Rogers, L., Washington, L., Glenn, T. C. and Knapp, L. W. 2005. Evolutionary origin of the feather epidermis. Dev Dynam 232: 256-267.
45. Schlosser, G. 2005. Evolutionary origins of vertebrate placodes: insights from developmental studies and from comparisons with other deuterostomes. J Exp Zool (Mol Dev Evol) 304B: 347-399.
46. Schlosser, G. and Northcutt, R. G. 2000. Development of neurogenic placodes in Xenopus laevis. J Comp Neurol 418: 121-146.
47. Serb, J. M. and Oakley, T. H. 2005. Hierarchical phylogenetics as a quantitative analytical framework for evolutionary developmental biology. Bioessays 27: 1158-1166.
48. Tanaka, S. and Kato, Y. 1983. Epigenesis in developing avian scales. II. Cell proliferation in relation to morphogenesis and differentiation in the epidermis.
49. Tao, H., Yoshimoto, Y., Yoshioka, H., Nohno, T., Noji, S. and Ohuchi, H. 2002. FGF10 is a mesenchymally derived stimulator for epidermal development in the chick embryonic skin. Mech Develop 116: 39-49.
50. Vargas, A. O., Kohlsdorf, T., Fallon, J. F., VandenBrooks, J. and Wagner, G. P. 2008. The Evolution of HoxD-11 expression in the bird wing: insights from Alligator mississippiensis. PLoS ONE 3: e3325.
51. Veltmaat, J. M., Mailleux, A. A., Thiery, J. P. and Bellusci, S. 2003. Mouse embryonic mammogenesis as a model for the molecular regulation of pattern formation. Differentiation 71: 1-17.
52. Wagner, G. P. 2014. Homology, genes, and evolutionary innovation. Princeton University Press, Princeton, pp. 301-304.
53. Wessells, N. K. 1965. Morphology and proliferation during early feather development. Dev Biol 12: 131-153.
54. Widelitz, R.B, Jiang, T. X., Lu, J. and Chuong, C. M. 2000. β-catenin in epithelial morphogenesis: conversion of part of avian foot scales into feather buds with a Mutated β-catenin. Dev Biol 219: 98-114.
55. Xu, X. 2006. Feathered dinosaurs from China and the evolution of major avian characters. Integr Zool 1: 4-11.
56. Xu, X. and Zhang, F. 2005. A new maniraptoran dinosaur from China with long feathers on the metatarsus. Naturwissenschaften 92: 173-177.
57. Xu, X., Zhou, Z. and Prum, R. O. 2001. Branched integumental structures in Sinornithosaurus and the origin of feathers. Nature 410: 200-204.
58. Xu, X., Zhou, Z., Wang, X., Kuang, X., Zhang, F. and Du, X. 2003. Four-winged dinosaurs from China. Nature 421: 335-340.
59. Xu, X., Zheng, X. and You, H. 2009. A new feather type in a nonavian theropod and the early evolution of feathers. Proc Natl Acad Sci USA 106: 832-834.
60. Yasue, A., Tao, H., Nohno, T., Moriyama, K., Noji, S. and Ohuchi, H. 2001. Cloning and expression of the chick p63 gene. Mech Develop 100: 105-108.
61. Yu, M., Wu, P., Widelitz, R. and Chuong, C. M. 2002. The morphogenesis of feathers. Nature 420: 308-312.
62. Yue, Z., Jiang, T. X., Widelitz, R. B. and Chuong, C. M. 2005. Mapping stem cell activities in the feather follicle. Nature 438: 1026-1029.
63. Yue, Z., Jiang, T. X., Widelitz, R. B. and Chuong, C. M. 2006. Wnt3a gradient converts radial to bilateral feather symmetry via topological arrangement of epithelia. Proc Natl Acad Sci USA 103: 951-955.