Abstract
Feathers are considered to be one of the most complex integumentary organs. The diverse morphology of a feather has made it a popular platform for investigating the cellular and molecular mechanisms for regional specificity, periodical patterning, organ shaping, and regeneration over the past two decades. Paleontological findings on feathered dinosaurs and Mesozoic birds have led to the identification of some unusual and unexpected intermediate or extinct feather forms, which can all be categorically called “protofeathers”. From the primitive protofeathers, every evolutionary novel step increases feather diversity and help the species adapt to diverse eco-spaces. Although it is compelling to trace the origin of morphological evolution, the proposed evolutionary transformations are constrained by the limited understanding of developmental mechanisms. In this chapter, we review some recent advances toward the understanding of the molecular and cellular mechanisms of these processes. We discuss how these mechanisms provide a basis for evolutionary novel steps to occur, as well as how the complexity of feather types increases successively. The important questions include the regional specification of feather tracts, the formation of periodically arranged feather buds and their anterior-posterior orientation, the formation of feather follicles, and the establishment of cyclic regeneration with clustered stem cells and dermal papilla. Within each follicle, the cylindrical feather filament undergoes branching morphogenesis. Because each follicle can have its own form, even on the same bird, complexity emerges with differential arrangement of radially symmetric barb branches, rachis and bilateral symmetric feather forms, medial-lateral asymmetric feather vanes, and pennaceous/plumulaceous regionalization along the proximal-distal axis. Each feather form has a functional implication for adaptation, and different forms can be produced under hormonal and seasonal regulation. Thus, collectively, the enormously diverse plumage patterns (the increased biological traits) of the avian integument are made possible by adaptive evolution.
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References
Atit R, Conlon RA, Niswander L (2003) EGF signaling patterns the feather array by promoting the interbud fate. Dev Cell 4(2):231–240
Brush AH (1996) On the origin of feathers. J Evol Biol 9(2):131–142
Chang CH, Jiang TX, Lin CM, Burrus LW, Chuong CM, Widelitz R (2004a) Distinct Wnt members regulate the hierarchical morphogenesis of skin regions (spinal tract) and individual feathers. Mech Dev 121(2):157–171. https://doi.org/10.1016/j.mod.2003.12.004
Chang CH, Yu M, Wu P, Jiang TX, Yu HS, Widelitz RB et al (2004b) Sculpting skin appendages out of epidermal layers via temporally and spatially regulated apoptotic events. J Invest Dermatol 122(6):1348–1355. https://doi.org/10.1111/j.0022-202X.2004.22611.x
Chang C, Wu P, Baker RE, Maini PK, Alibardi L, Chuong CM (2009) Reptile scale paradigm: evo-devo, pattern formation and regeneration. Int J Dev Biol 53(5–6):813–826. https://doi.org/10.1387/ijdb.072556cc
Chen CW, Jung HS, Jiang TX, Chuong CM (1997) Asymmetric expression of notch/Delta/serrate is associated with the anterior-posterior axis of feather buds. Dev Biol 188(1):181–187. https://doi.org/10.1006/dbio.1997.8643
Chen CF, Foley J, Tang PC, Li A, Jiang TX, Wu P et al (2015) Development, regeneration, and evolution of feathers. Annu Rev Anim Biosci 3:169–195. https://doi.org/10.1146/annurev-animal-022513-114127
Chen CK, Ng CS, Wu SM, Chen JJ, Cheng PL, Wu P et al (2016) Regulatory differences in natal down development between altricial zebra finch and precocial chicken. Mol Biol Evol 33(8):2030–2043. https://doi.org/10.1093/molbev/msw085
Chodankar R, Chang CH, Yue Z, Jiang TX, Suksaweang S, Burrus L et al (2003) Shift of localized growth zones contributes to skin appendage morphogenesis: role of the Wnt/beta-catenin pathway. J Invest Dermatol 120(1):20–26. https://doi.org/10.1046/j.1523-1747.2003.12008.x
Chu Q, Cai L, Fu Y, Chen X, Yan Z, Lin X et al (2014) Dkk2/Frzb in the dermal papillae regulates feather regeneration. Dev Biol 387(2):167–178. https://doi.org/10.1016/j.ydbio.2014.01.010
Chuong CM, Edelman GM (1985) Expression of cell-adhesion molecules in embryonic induction. II. Morphogenesis of adult feathers. J Cell Biol 101(3):1027–1043
Chuong CM, Chodankar R, Widelitz RB, Jiang TX (2000) Evo-devo of feathers and scales: building complex epithelial appendages. Curr Opin Genet Dev 10(4):449–456
Chuong CM, Wu P, Zhang FC, Xu X, Yu M, Widelitz RB et al (2003) Adaptation to the sky: defining the feather with integument fossils from mesozoic China and experimental evidence from molecular laboratories. J Exp Zool B Mol Dev Evol 298(1):42–56. https://doi.org/10.1002/jez.b.25
Chuong CM, Bhat R, Widelitz RB, Bissell MJ (2014) SnapShot: branching morphogenesis. Cell 158(5):1212-e1. https://doi.org/10.1016/j.cell.2014.08.019.
Desbiens X, Queva C, Jaffredo T, Stehelin D, Vandenbunder B (1991) The relationship between cell proliferation and the transcription of the nuclear oncogenes c-myc, c-myb and c-ets-1 during feather morphogenesis in the chick embryo. Development 111(3):699–713
Dyke G, de Kat R, Palmer C, van der Kindere J, Naish D, Ganapathisubramani B (2013) Aerodynamic performance of the feathered dinosaur microraptor and the evolution of feathered flight. Nat Commun 4:2489. https://doi.org/10.1038/ncomms3489
Feduccia A, Tordoff HB (1979) Feather of Archaeopteryx: asymmetric vanes indicate aerodynamic function. Science 203:1021–1022
Feo TJ, Prum RO (2014) Theoretical morphology and development of flight feather vane asymmetry with experimental tests in parrots. J Exp Zool B Mol Dev Evol 322(4):240–255. https://doi.org/10.1002/jez.b.22573
Feo TJ, Field DJ, Prum RO (2015) Barb geometry of asymmetrical feathers reveals a transitional morphology in the evolution of avian flight. Proc Biol Sci 282(1803):20142864. https://doi.org/10.1098/rspb.2014.2864
Gill FB (1994) Ornithology, 2nd edn. Freeman, New York
Harris MP, Williamson S, Fallon JF, Meinhardt H, Prum RO (2005) Molecular evidence for an activator-inhibitor mechanism in development of embryonic feather branching. Proc Natl Acad Sci U S A 102(33):11734–11739. https://doi.org/10.1073/pnas.0500781102
Hornik C, Krishan K, Yusuf F, Scaal M, Brand-Saberi B (2005) cDermo-1 misexpression induces dense dermis, feathers, and scales. Dev Biol 277(1):42–50. https://doi.org/10.1016/j.ydbio.2004.08.050
Jiang TX, Jung HS, Widelitz RB, Chuong CM (1999) Self-organization of periodic patterns by dissociated feather mesenchymal cells and the regulation of size, number and spacing of primordia. Development 126(22):4997–5009
Jiang TX, Tuan TL, Wu P, Widelitz RB, Chuong CM (2011) From buds to follicles: matrix metalloproteinases in developmental tissue remodeling during feather morphogenesis. Differentiation 81(5):307–314. https://doi.org/10.1016/j.diff.2011.03.004
Jung HS, Francis-West PH, Widelitz RB, Jiang TX, Ting-Berreth S, Tickle C et al (1998) Local inhibitory action of BMPs and their relationships with activators in feather formation: implications for periodic patterning. Dev Biol 196(1):11–23. https://doi.org/10.1006/dbio.1998.8850
Lai YC, Chuong CM (2016) The “tao” of integuments. Science 354(6319):1533–1534. https://doi.org/10.1126/science.aal4572
Lei MI, Inaba M, Chuong CM (2016) Vertebrate embryo: development of the skin and its appendages. https://doi.org/10.1002/9780470015902.a0026601
Li A, Chen M, Jiang TX, Wu P, Nie Q, Widelitz R et al (2013) Shaping organs by a wingless-int/Notch/nonmuscle myosin module which orients feather bud elongation. Proc Natl Acad Sci U S A 110(16):E1452–E1461. https://doi.org/10.1073/pnas.1219813110
Li AFS, Jiang TX, Wu P, Widelitz R, Nie Q, Chuong CM (2017) Diverse feather shape evolution enabled by coupling anisotropic signalling modules with self-organizing branching programme. Nat Commun 8:14139. https://doi.org/10.1038/ncomms14139
Lillie FR, Wang H (1944) Physiology of development of the feather. VII. An experimental study of induction. Physiol Zool 17(1):1–31
Lin CM, Jiang TX, Widelitz RB, Chuong CM (2006) Molecular signaling in feather morphogenesis. Curr Opin Cell Biol 18(6):730–741. https://doi.org/10.1016/j.ceb.2006.10.009
Lin SJ, Foley J, Jiang TX, Yeh CY, Wu P, Foley A et al (2013a) Topology of feather melanocyte progenitor niche allows complex pigment patterns to emerge. Science 340(6139):1442–1445. https://doi.org/10.1126/science.1230374
Lin SJ, Wideliz RB, Yue Z, Li A, Wu X, Jiang TX et al (2013b) Feather regeneration as a model for organogenesis. Develop Growth Differ 55(1):139–148. https://doi.org/10.1111/dgd.12024
Lucas AM, Stettenheim PR (1972) Avian anatomy: integument. Agriculture handbook, vol 362, 1st edn. Washington, Agricultural Research Service
Ng CS, Wu P, Foley J, Foley A, McDonald ML, Juan WT et al (2012) The chicken frizzle feather is due to an α-keratin (KRT75) mutation that causes a defective rachis. PLoS Genet 8(7):e1002748. https://doi.org/10.1371/journal.pgen.1002748
Noramly S, Morgan BA (1998) BMPs mediate lateral inhibition at successive stages in feather tract development. Development 125(19):3775–3787
Noramly S, Freeman A, Morgan BA (1999) Beta-catenin signaling can initiate feather bud development. Development 126(16):3509–3521
Norberg RA (1985a) Function of vane asymmetry and shaft curvanture in bird flight feather: inference on flight ability of Archaeopteryx. In: Hecht MK, Ostrom JH, Viohl G, Wellnhofer P (eds) The beginnings of birds. Freunde des Jura-Museums Eichstätt, Willibaldsburg, pp 303–313
Norberg UM (1985b) Evolution of flight in bird: aerodynamic, mechanical and ecological aspects. In: Hecht MK, Ostrom JH, Viohl G, Wellnhofer P (eds) The beginnings of birds. Freunde des Jura-Museums Eichstätt, Willibaldsburg, pp 293–302
Noveen A, Jiang TX, Ting-Berreth SA, Chuong CM (1995) Homeobox genes Msx-1 and Msx-2 are associated with induction and growth of skin appendages. J Invest Dermatol 104(5):711–719
Ohyama A, Saito F, Ohuchi H, Noji S (2001) Differential expression of two BMP antagonists, gremlin and Follistatin, during development of the chick feather bud. Mech Dev 100(2):331–333
Olivera-Martinez I, Thelu J, Teillet MA, Dhouailly D (2001) Dorsal dermis development depends on a signal from the dorsal neural tube, which can be substituted by Wnt-1. Mech Dev 100(2):233–244
Paul GS (2002) Dinosaurs of the air: the evolution and loss of flight in dinosaurs and birds, 1st edn. Johns Hopkins University Press, Baltimore
Pennycuick CJ (2008) Modelling the flying bird, 1st edn. Academic Press, London
Prum RO (1999) Development and evolutionary origin of feathers. J Exp Zool 285(4):291–306
Prum RO (2005) Evolution of the morphological innovations of feathers. J Exp Zool B Mol Dev Evol 304(6):570–579. https://doi.org/10.1002/jez.b.21073
Prum RO, Brush AH (2002) The evolutionary origin and diversification of feathers. Q Rev Biol 77(3):261–295
Prum RO, Williamson S (2001) Theory of the growth and evolution of feather shape. J Exp Zool B Mol Dev Evol 291(1):30–57. https://doi.org/10.1002/jez.4
Scaal M, Prols F, Fuchtbauer EM, Patel K, Hornik C, Kohler T et al (2002) BMPs induce dermal markers and ectopic feather tracts. Mech Dev 110(1–2):51–60
Scott SD, McFarland C (2010) Bird feathers: a guide to North American species, 1st edn. Stackpole Books, Mechanicsburg
Suksaweang S, Jiang TX, Roybal P, Chuong CM, Widelitz R (2012) Roles of EphB3/ephrin-B1 in feather morphogenesis. Int J Dev Biol 56(9):719–728. https://doi.org/10.1387/ijdb.120021rw
Ting-Berreth SA, Chuong CM (1996) Sonic hedgehog in feather morphogenesis: induction of mesenchymal condensation and association with cell death. Dev Dyn 207(2):157–170. https://doi.org/10.1002/(SICI)1097-0177(199610)207:2<157::AID-AJA4>3.0.CO;2-G
Wessells NK (1965) Morphology and proliferation during early feather development. Dev Biol 12(1):131–153
Widelitz RB, Jiang TX, Noveen A, Chen CW, Chuong CM (1996) FGF induces new feather buds from developing avian skin. J Invest Dermatol 107(6):797–803
Widelitz RB, Jiang TX, Chen CW, Stott NS, Jung HS, Chuong CM (1999) Wnt-7a in feather morphogenesis: involvement of anterior-posterior asymmetry and proximal-distal elongation demonstrated with an in vitro reconstitution model. Development 126(12):2577–2587
Widelitz RB, Jiang TX, Yu M, Shen T, Shen JY, Wu P et al (2003) Molecular biology of feather morphogenesis: a testable model for evo-devo research. J Exp Zool B Mol Dev Evol 298(1):109–122. https://doi.org/10.1002/jez.b.29
Wu P, Hou LH, Plikus M, Hughes M, Scehnet J, Suksaweang S et al (2004) Evo-Devo of amniote integuments and appendages. Int J Dev Biol 48(2–3):249–270. https://doi.org/10.1387/ijdb.15272390
Wu P, Ng CS, Yan J, Lai YC, Chen CK, Lai YT et al (2015) Topographical mapping of α- and β-keratins on developing chicken skin integuments: functional interaction and evolutionary perspectives. Proc Natl Acad Sci U S A 112(49):E6770–E6779. https://doi.org/10.1073/pnas.1520566112
Xing LD, McKellar RC, Xu X, Li G, Bai M, Persons WS et al (2016) A feathered dinosaur tail with primitive plumage trapped in mid-Cretaceous amber. Curr Biol 26(24):3352–3360. https://doi.org/10.1016/j.cub.2016.10.008
Xu X (2006) Feathered dinosaurs from China and the evolution of major avian characters. Integr Zool 1(1):4–11. https://doi.org/10.1111/j.1749-4877.2006.00004.x
Xu X, Guo Y (2009) The origin and early evolution of feathers: insights from recent paleontological and neontological data. Vertebr PalAsiat 47(4):311–329
Xu X, Zhou Z, Dudley R, Mackem S, Chuong CM, Erickson GM et al (2014) An integrative approach to understanding bird origins. Science 346(6215):1253293. https://doi.org/10.1126/science.1253293
Yu M, Wu P, Widelitz RB, Chuong CM (2002) The morphogenesis of feathers. Nature 420(6913):308–312. https://doi.org/10.1038/nature01196
Yue Z, Jiang TX, Widelitz RB, Chuong CM (2005) Mapping stem cell activities in the feather follicle. Nature 438(7070):1026–1029. https://doi.org/10.1038/nature04222
Yue Z, Jiang TX, Widelitz RB, Chuong CM (2006) Wnt3a gradient converts radial to bilateral feather symmetry via topological arrangement of epithelia. Proc Natl Acad Sci U S A 103(4):951–955. https://doi.org/10.1073/pnas.0506894103
Zhang F, Kearns SL, Orr PJ, Benton MJ, Zhou Z, Johnson D et al (2010) Fossilized melanosomes and the colour of cretaceous dinosaurs and birds. Nature 463(7284):1075–1078. https://doi.org/10.1038/nature08740
Acknowledgement
This work was supported by a Dragon Gate grant from the Taiwan Ministry of Science Technology (MOST) 104-2911-I-002-577 and US NIH Grants AR47364, AR60306, and GM125322. GW. L. was supported by a Taiwan MOST postdoctoral fellowship. A. L. was supported by a CIRM fellowship. We thank Dr. Shuo Wang for reviewing this manuscript.
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Lin, GW., Li, A., Chuong, CM. (2020). Molecular and Cellular Mechanisms of Feather Development Provide a Basis for the Diverse Evolution of Feather Forms. In: Foth, C., Rauhut, O. (eds) The Evolution of Feathers. Fascinating Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-030-27223-4_2
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