Development and evolution of the amniote integument: Current landscape and future horizon

Abstract

This special issue on the development and evolution of the amniote integument begins with a discussion of the adaptations to terrestrial conditions, the acquisition of water-impermeability by the reptilian integument, and the initial formation of filamentous integumentary appendages that pave the way towards avian flight. Recent feather fossils are reviewed and a definition of feathers is developed. Hierarchical models are proposed for the formation of complex structures, such as feathers. Molecular signals that alter the phenotype of integumentary appendages at different levels of the hierarchy are presented. Tissue interactions and the roles of keratins in evolution are discussed and linked to their bio-mechanical properties. The role of mechanical forces on patterning is explored. Elaborate extant feather variants are introduced. The regeneration/gene mis-expression protocol for the chicken feather is established as a testable model for the study of biological structures. The adaptations of the mammalian distal limb end organs to terrestrial, arboreal and aquatic conditions are discussed. The development and cycling of hair are reviewed from a molecular perspective. These contributions reveal that the structure and function of diverse integumentary appendages are variations superimposed on a common theme, and that their formation is modular, hierarchical, and cyclical. They further reveal that these mechanisms can be understood at the molecular level, and that an integrative and organismal approach to studying integumentary appendages is needed. We propose that future research should foster interdisciplinary approaches, pursue understanding at the cellular and molecular level, analyze interactions between the environment and genome, and recognize the contributions of variation in morphogenesis and evolution.

Evo-Devo of amniote integuments and appendages.

“…As we learn more about how molecular pathways work in model organisms, we need to pursue more comparative studies to appreciate how Nature formed myriad structures in many diverse ways in the wild, how the integument appendages interface with other systems to perform a physiological function for the whole organism (e.g., flight) and how genes interact with the environment. Only with these endeavors, can we truly understand the essence of integument biology (Chuong and Homberger, 2003).…”

“…They share similar hierarchical morphogenesis, but acquire variations which lead to different skin appendage phenotypes. Modified from Chuong and Homberger (2003). a proximal-distal axis can be developed by having a localized growth zone that generates special epidermal cells continuously (claw matrix).…”

“…Thus every molting event gives the bird a new opportunity to remodel its regenerating feathers, thus allowing birds to alter their integument appendage phenotypes in response to the changing environment. This is an important research issue (Chuong and Homberger, 2003) and the feather is a good model in which to study it, given its continual and physiological regenerative processes.…”

“…The many apparently epithelial organs share the use of these signaling molecular pathways (e.g., Wnt, BMP, FGF, Notch, Shh, etc.) and their differences are variations superimposed on the common theme (Chuong, 1998;Chuong and Homberger, 2003). Along this logic, if we imbalance one of fundamental signaling pathways, there should be significant consequences in multiple ectodermal organs in a spatio-temporal dependent manner.…”

Topographical mapping of α- and β-keratins on developing chicken skin integuments: Functional interaction and evolutionary perspectives

“…It serves as the first line of defense against external factors, such as physical injuries, pathogens and provides insulation, sensation, and locomotion (1-3). The integument includes not only the epidermis and dermis, but also integumentary derivatives, namely invaginated glands and protruded appendages, such as hairs, feathers, and teeth (3,4). Integumentary derivatives represent the integration of many evolutionary steps that combine to form diverse structural variations, allowing animals to adapt to various ecospaces according to their specific lifestyles (3).…”