Feather arrays are patterned by interacting signalling and cell density waves

Abstract

Feathers are arranged in a precise pattern in avian skin. They first arise during development in a row along the dorsal midline, with rows of new feather buds added sequentially in a spreading wave. We show that the patterning of feathers relies on coupled fibroblast growth factor (FGF) and bone morphogenetic protein (BMP) signalling together with mesenchymal cell movement, acting in a coordinated reaction-diffusion-taxis system. This periodic patterning system is partly mechanochemical, with mechanical-chemical integration occurring through a positive feedback loop centred on FGF20, which induces cell aggregation, mechanically compressing the epidermis to rapidly intensify FGF20 expression. The travelling wave of feather formation is imposed by expanding expression of Ectodysplasin A (EDA), which initiates the expression of FGF20 . The EDA wave spreads across a mesenchymal cell density gradient, triggering pattern formation by lowering the threshold of mesenchymal cells required to begin to form a feather bud. These waves, and the precise arrangement of feather primordia, are lost in the flightless emu and ostrich, though via different developmental routes. The ostrich retains the tract arrangement characteristic of birds in general but lays down feather primordia without a wave, akin to the process of hair follicle formation in mammalian embryos. The embryonic emu skin lacks sufficient cells to enact feather formation, causing failure of tract formation, and instead the entire skin gains feather primordia through a later process. This work shows that a reaction-diffusion-taxis system, integrated with mechanical processes, generates the feather array. In flighted birds, the key role of the EDA/Ectodysplasin A receptor (EDAR) pathway in vertebrate skin patterning has been recast to activate this process in a quasi-1-dimensional manner, imposing highly ordered pattern formation.

Self‐organizing hair peg‐like structures from dissociated skin progenitor cells: New insights for human hair follicle organoid engineering and Turing patterning in an asymmetric morphogenetic field

“…This is part of the motivation for this study, to use the organoid droplet to understand more about the nature of the sequential appearance of hair or feather primordia. It is timely that a paper reporting a global Eda wave spreading from the midline to the flank is just reported, which suggests Eda induces FGF20, followed by dermal cell aggregate formation, thus facilitating Turing patterning via mechano‐chemical coupling . Based on this and other studies, we propose a new understanding on the process of propagative formation of feather arrays in vivo: a local Turing periodic patterning occurs and works together with a global propagation mechanism .…”

“…Based on this and other studies, we propose a new understanding on the process of propagative formation of feather arrays in vivo: a local Turing periodic patterning occurs and works together with a global propagation mechanism . In this new study, progressive expression of Eda and activation of Eda signalling from the midline to the flank is shown to mediate the global process by lowering the threshold of dermal condensation . Yet, what is upstream to Eda remains unclear.…”

Instructive role of melanocytes during pigment pattern formation of the avian skin

“…The patterning roles of the melanocytes and dermis (11) do not have to be in conflict. Recently, propagating periodic formation of feather buds has been shown to result from a combination of a local Turing pattern and a global ectodysplasin A (EDA)/FGF20/cell aggregation-mediated mechanochemical wave (28,29). It is possible the autonomous melanocyte patterning signaling here may work with the somite/dermis-mediated agouti patterning signals (11) to fine-tune, interact, or stabilize the final pattern.…”

An overlooked placode: Recharacterizing the papillae in the embryonic eye of reptilia

“…65,67,68 Although not involved in the initial induction of placodes, the FGF and Hh family members are expressed in feather placodes and promote their continued development through early and late stages of feather bud development. 72 F I G U R E 1 The involvement of Wnt/B-catenin, BMP, Hh, and FGF signaling pathways during early formation of taste papillae, scutes, feather papillae, and conjunctival papillae. 70,71 Ectodysplasin and its receptor have recently been shown to play a key role in patterning feather placode development.…”

“…70,71 Ectodysplasin and its receptor have recently been shown to play a key role in patterning feather placode development. 72 F I G U R E 1 The involvement of Wnt/B-catenin, BMP, Hh, and FGF signaling pathways during early formation of taste papillae, scutes, feather papillae, and conjunctival papillae. For comparison purposes, development of each structure is broken down into three main stages: placode induction, early formation of the derivative structure, and late formation of the derivative structure.…”