Cell shape anisotropy contributes to self-organized feather pattern fidelity in birds

Abstract

Developing tissues can self-organize into a variety of patterned structures through the stabilization of stochastic fluctuations in their molecular and cellular properties. While molecular factors and cell dynamics contributing to self-organization have been identified in vivo, events channeling self-organized systems such that they achieve stable pattern outcomes remain unknown. Here, we described natural variation in the fidelity of self-organized arrays formed by feather follicle precursors in bird embryos. By surveying skin cells prior to and during tissue self-organization and performing species-specific ex vivo drug treatments and mechanical stress tests, we demonstrated that pattern fidelity depends on the initial amplitude of cell anisotropy in regions of the developing dermis competent to produce a pattern. Using live imaging, we showed that cell shape anisotropy is associated with a limited increase in cell motility for sharp and precisely located primordia formation, and thus, proper pattern geometry. These results evidence a mechanism through which initial tissue properties ensure stability in self-organization and thus, reproducible pattern production.

Periodic pattern formation during embryonic development

“…This research on feather formation highlights the complexities of studying periodic pattern formation especially when there is likely an intricate interplay between the mechanical and cell signalling environments driving feather pattern formation, rather than a sole mechanism, which agrees with another recent study exploring the contribution of cell shape anisotropy to feather pattern fidelity [ 47 ].…”

Migration and division in cell monolayers on substrates with topological defects

“…As cell area and aspect ratio are known to be important in determining the fate of individual cells [38,39], our work suggests that ridge patterns could be harnessed for controlled development [40,41] -but the observed feedback between growth and cell shape means that computational modeling will be required to understand the effect of any given pattern. Changes of cell shape and aspect ratio are also seen in many patterning processeses in development, including avian skin morphogenesis [42][43][44]; control of division by local cell shape may allow for additional feedback between tissue growth and local alignment. Our results suggest capturing the interplay of division, liquid-crystal alignment, and cell shape together is required to understand many patterning processes in eukaryotic development.…”

Patterning and folding of intestinal villi by active mesenchymal dewetting

“…As in the case of villus clusters, dermal papilla formation coincides with mesenchymal cell motility, subsequent exit from the cell cycle, and can occur in the absence of an apparent epidermal prepattern, suggesting that mesenchymal condensation here might also occur autonomously [89][90][91][92] . This apparent self-organizing ability of the dermis has been studied with more detail in the chick skin, where dermal condensates initiate feather bud morphogenesis 85,[93][94][95] . While the overall morphological outcome -mesenchymal condensation -is qualitatively similar to the aggregation of PDGFRA High cells of the gut, the underlying mechanisms appear distinct.…”