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 of the reptilian integument, and the initial formation of filamentous integumentary appendages that prepare 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 that are 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 called for. 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.

Fig. 1

Representative amniote integuments. Mouse paw shows hair, claw, and footpad. Pheasant wing shows remiges and covert feathers. Lizard trunk shows scales.

Fig. 2

Modular, hierarchical, and cyclical morphogenesis of the integumentary appendages. Panel A shows different levels of skin development. Panel B shows how the induction between epidermis and mesenchyme occurs in feather buds, feather follicles, and the subsequent molting cycles. At each level or cycle of morphogenesis, signaling molecule pathway modules are recruited to regulate specific cellular events (e.g., proliferation, migration, apoptosis). The same pathway may perform different tasks in different contexts. Not all integument appendages have evolved to include all the levels or cycles. Through these opportunities for modulation, a great diversity of integumentary appendages can be achieved.