Organisation of the feather periodic pattern through propagating molecular waves

Abstract

Members of the class Aves possess integumentary structures which distinguish them from other vertebrate lineages. The characteristic integumentary structure that defines the Aves from other vertebrates are the feathers, whose functions include insulation, camouflage, visual display, gliding, and powered flight. The recent discoveries of theropod dinosaur fossils displaying feather-like structures have led to interest in the morphological innovations of the feathers, which are associated with the evolution of flight in Aves. Most modern birds, display a highly ordered, hexagonal arrangement of feather follicles, which aids in the streamlining of the body to increase aerodynamic efficiency. Using the chicken embryo as a developmental model, I address the cellular and molecular processes involved in the initiation and formation of a high fidelity periodic pattern of feather primordia. From my studies, I propose a model in which the induction of individual feather primordia begins with the activation of FGF20 expression. This gene encodes a protein that serves as a chemoattractant. Aggregation of cells towards sources of FGF20 stimulates and reinforces FGF20 expression and also induces the expression of BMP4. Via a reaction-diffusion-like mechanism, BMP4 acts to limit the growth of the cell aggregate and promotes lateral inhibition to prevent fusions between neighbouring feather primordia through transcriptional regulation of FGF20. In order to achieve a high fidelity periodic pattern of feather primordia, three components are required; 1) a competent epidermis displaying β-Catenin and EDAR expression, 2) wave-like propagation of EDA expression, which acts synergistically with β-Catenin expression to activate FGF20 expression at the β-Catenin/EDA junction, 3) and a dermis of sufficient cell density. The spatiotemporal wave-like propagation of EDA expression, specifically, promotes the sequential induction of new feather primordium rows and is associated with the formation of a high fidelity periodic pattern. The importance of these three components appears to be evolutionarily conserved among the Aves and differences in the periodic pattern of feather primordia between species can be explained by how the three components are expressed or regulated in individual species. Independent losses of flight in ratites, such as ostriches and emus, are associated with the loss of feather pattern fidelity. In emus, this loss of pattern fidelity results from the delayed formation of a dermis of sufficient cell density, which prevents the induction of feather primordium formation within the dorsal tract, despite the presence of a fully primed and competent epidermis. These studies demonstrate how the precise feather pattern arises during embryonic development in birds, and how feather patterns can be modified through differential regulation of the molecular and cellular toolkit involved in feather primordium induction in different bird species.