Physiology of Development of the Feather V. Experimental Morphogenesis

Lillie, Frank R.; Wang, Hsi

doi:10.1086/physzool.14.2.30161732

Cited by 83 publications

(27 citation statements)

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“…Experimental perturbations by using retinoids, thought to affect Shh signaling, can reverse orientation of the follicle such that the future dorsal ventral axis (i.e., rachis specification) is random or reversed in orientation (12). Experimental transplantations of dorsal and ventral portions of growing feather papillae demonstrate that a D͞V asymmetry within the feather is involved with specifying the position of rachis formation and the direction of helical growth (35)(36)(37) as hypothesized here.…”

Section: Discussionmentioning

confidence: 79%

“…In our models, the localization of barb ridge creation and fusion in pennaceous feathers is accomplished by polarized, regional modification of activator (Shh) signaling. The polarization of these processes is confirmed by the empirically demonstrated D͞V asymmetry, or gradient, in the developing germs of pennaceous feathers (35)(36)(37).…”

Section: An Integrated Model Of Barb Ridge Morphogenesis and Evolutionmentioning

confidence: 78%

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Molecular evidence for an activator–inhibitor mechanism in development of embryonic feather branching

Harris

Williamson

Fallon

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

150

158

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The developmental basis of morphological complexity remains a central question in developmental and evolutionary biology. Feathers provide a unique system to analyze the development of complex morphological novelties. Here, we describe the interactions between Sonic hedgehog (Shh) and bone morphogenetic protein 2 (Bmp2) signaling during feather barb ridge morphogenesis. We demonstrate that activator-inhibitor models of Shh and Bmp2 signaling in the tubular feather epithelium are sufficient to explain the initial formation of a meristic pattern of barb ridges and the observed variation in barb morphogenesis in chick natal down feathers. Empirical tests support the assumptions of the model that, within the feather ectoderm, Shh (activator) up-regulates its own transcription and that of Bmp2 (inhibitor), whereas Bmp2 signaling down-regulates Shh expression. More complex models incorporating a second activator and dorsal͞ventral polarized modification of activator signaling can produce all of the barb morphogenesis patterns observed during the growth of more complex branched pennaceous feathers: new barb ridge formation, helical growth, and barb ridge fusion. An integrated model of feather morphogenesis and evolution suggests that plumulaceous feather structure evolved by the establishment of activatorinhibitor interactions between Shh and Bmp2 signaling in the basal epithelium of the feather germ. Subsequently, pennaceous feather structure evolved through the integration of barb ridge morphogenesis with a second, local inhibitor and a dorsal͞ventral signal gradient within the feather. The model is congruent with paleontological evidence that plumulaceous feathers are primitive to pennaceous feathers. evolution ͉ Shh ͉ Bmp2 ͉ branching morphogenesis ͉ pattern formation

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Section: Discussionmentioning

confidence: 79%

Section: An Integrated Model Of Barb Ridge Morphogenesis and Evolutionmentioning

confidence: 78%

Molecular evidence for an activator–inhibitor mechanism in development of embryonic feather branching

Harris

Williamson

Fallon

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

150

158

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“…How was the Wnt3a gradient established? Classical experiments showed that the DP controls the morphology of regenerated feathers, although in some earlier studies, the papillar ectoderm (PE) was not removed from the DP (17,18,27). Here we developed a way to remove the PE from the DP (see Materials and Methods).…”

Section: Epithelial-mesenchymal Recombination Between Downy and Flightmentioning

confidence: 99%

“…Three-month-old chickens were anesthetized with ketamine and xylocaine (2:1, 10 mg͞kg). DP͞PE operations were done after Lillie and Wang (17,18). The DP͞PE complex is immersed in trypsin͞EDTA in vitro for 10 min at 37°C.…”

Section: Dmentioning

confidence: 99%

Wnt3a gradient converts radial to bilateral feather symmetry via topological arrangement of epithelia

Yue

Jiang²,

Widelitz³

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

124

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The evolution of bilaterally symmetric feathers is a fundamental process leading toward flight. One major unsolved mystery is how the feathers of a single bird can form radially symmetric downy feathers and bilaterally symmetric flight feathers. In developing downy feather follicles, barb ridges are organized parallel to the long axis of the feather follicle. In developing flight-feather follicles, the barb ridges are organized helically toward the anterior region, leading to the fusion and creation of a rachis. Here we discover an anterior-posterior molecular gradient of wingless int (Wnt3)a in flight but not downy feathers. Global inhibition of the Wnt gradient transforms bilaterally symmetric feathers into radially symmetric feathers. Production of an ectopic local Wnt3a gradient reoriented barb ridges toward the source and created an ectopic rachis. We further show that the orientation of the Wnt3a gradient is dictated by the dermal papilla (DP). Swapping DPs between wing covert and breast downy feathers demonstrates that both feather symmetry and molecular gradients are in accord with the origin of the DP. Thus the fates of feather epidermal cells are not predetermined through some molecular codes but can be modulated. Together, our data suggest feathers are shaped by a DP3 Wnt gradient3helical barb ridge organization3creation of rachis3bilateral symmetry sequence. We speculate diverse feather forms can be achieved by adjusting the orientation and slope of molecular gradients, which then shape the topological arrangements of feather epithelia, thus linking molecular activities to organ forms and novel functions.axis determination ͉ dermal papilla ͉ evo-devo (evolution and development) ͉ morphogenesis ͉ skin appendages

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“…Although the details of the observed responses are difficult to interpret, the results of Lillie & Juhn (1932) do support the role of anterior-posterior molecular gradients within the feather germ in the development of pigmentation feather patterns. Lillie & Wang (1941) and Cohen & 'Espinasse (1961) performed a series of experiments transplanting portions of the dermal papillae (with or without the epidermal collar) between regenerating follicles from pigmented and non-pigmented feather tracts. Although the results of these experiments were highly variable and showed substantial artefacts, Lillie & Wang (1941) and Cohen & 'Espinasse (1961) confirm that distal and ventral portions of the papilla generally determine the patterns of the central and marginal portions to the vane.…”

Section: (B) Testable Predictionsmentioning

confidence: 99%

Reaction–diffusion models of within-feather pigmentation patterning

Prum

Williamson

2002

Proc. R. Soc. Lond. B

113

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Feathers are complex, branched keratin structures that exhibit a diversity of pigmentation patterns. Feather pigments are transferred into developing feather keratinocytes from pigment cells that migrate into the tubular feather germ from the dermis. Within-feather pigment patterns are determined by differential pigmentation of keratinocytes within independent barb ridges during feather development. Little is known about the molecular mechanisms that determine which keratinocytes receive pigment. We apply reactiondiffusion models to the growth of within-feather pigment patterns based on a realistic model of feather growth. These models accurately simulate the growth of a diversity of the within-feather pigmentation patterns found in real feathers, including a central patch, a 'hollow' central patch, concentric central patches, bars, chevrons, a central circular spot, rows of paired spots, and arrays of offset dots. The models can also simulate the complex transitions between distinct pigmentation patterns among feathers observed in real avian plumages, including transitions from bars to chevrons, bars to paired dots, and bars to arrays of dots. The congruence between the developmental dynamics of the simulated and observed feather patterns indicates that the reaction-diffusion models provide a realistic and accurate description of the determination of pigment pattern within avian feather follicles. The models support the hypothesis that within-feather pigmentation patterning is determined by antagonistic interactions among molecular expression gradients within the tubular follicle and feather germ.

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Physiology of Development of the Feather V. Experimental Morphogenesis

Cited by 83 publications

References 0 publications

Molecular evidence for an activator–inhibitor mechanism in development of embryonic feather branching

Molecular evidence for an activator–inhibitor mechanism in development of embryonic feather branching

Wnt3a gradient converts radial to bilateral feather symmetry via topological arrangement of epithelia

Reaction–diffusion models of within-feather pigmentation patterning

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