Multiple Regulatory Modules Are Required for Scale-to-Feather Conversion

Abstract

The origin of feathers is an important question in Evo-Devo studies, with the eventual evolution of vaned feathers which are aerodynamic, allowing feathered dinosaurs and early birds to fly and venture into new ecological niches. Studying how feathers and scales are developmentally specified provides insight into how a new organ may evolve. We identified feather-associated genes using genomic analyses. The candidate genes were tested by expressing them in chicken and alligator scale forming regions. Ectopic expression of these genes induced intermediate morphotypes between scales and feathers which revealed several major morphogenetic events along this path: Localized growth zone formation, follicle invagination, epithelial branching, feather keratin differentiation, and dermal papilla formation. In addition to molecules known to induce feathers on scales (retinoic acid, β-catenin), we identified novel scale-feather converters (Sox2, Zic1, Grem1, Spry2, Sox18) which induce one or more regulatory modules guiding these morphogenetic events. Some morphotypes resemble filamentous appendages found in feathered dinosaur fossils, whereas others exhibit characteristics of modern avian feathers. We propose these morpho-regulatory modules were used to diversify archosaur scales and to initiate feather evolution. The regulatory combination and hierarchical integration may have led to the formation of extant feather forms. Our study highlights the importance of integrating discoveries between developmental biology and paleontology.

Genetic and Molecular Basis of Feather Diversity in Birds

“…2015 ). Recruitments of multiple regulatory modules of scale-feather converters (SOX2, ZIC1, GREM1, SPRY2, and SOX18) may allow more complex morphogenetic events to occur ( Wu et al. 2018 ).…”

“…In addition, bioinformatics analyses of identified genes that are associated with feather and scale differences ( Chang et al. 2015 ; Wu et al. 2018 ) and miRNAs that target the cell signaling, cell adhesion, and cell structure genes required in feather morphogenesis ( Zhang et al.…”

“…One lineage of feathered theropod dinosaurs survived the mass extinction and became the ancestor of birds ( Chatterjee 2015 ). Feather is believed to have evolved from scale, and novel scale-feather converters have just been identified ( Wu et al. 2018 ).…”

Transcriptome analyses of reprogrammed feather / scale chimeric explants revealed co-expressed epithelial gene networks during organ specification

“…Until today, there is no simple model to explain why so many molecules can make feathered feet (ptilopody). More recently, we have found five novel molecules (Sox2, Zic1, Grem1, Spry2 and Sox18) expressed in the mesenchyme that have the ability to convert scale forming skin toward feather morphogenesis [ 17 ]. Each of these molecules seems to act along a different molecular pathway toward the morphological conversion of scales to feathers.…”

“…Each of these molecules seems to act along a different molecular pathway toward the morphological conversion of scales to feathers. Based on these findings, we postulate these molecular modules are part of a larger morpho-regulatory gene network that may have been co-opted in evolution to generate diverse appendage types, in this case, feathers and scales [ 17 ]. It should be noted avian scales include tarso-metatarsal scutate scale and plantar reticulate scales [ 2 ] and we only study scutate scales in this paper.…”