Organizational principles of integumentary organs: Maximizing variations for effective adaptation

Abstract

The integument serves as the interface between an organism and its environment. It primarily comprises ectoderm-derived epithelium and mesenchyme derived from various embryonic sources. These integumentary organs serve as a barrier defining the physiological boundary between the internal and exterior environments and fulfill diverse functions. How does the integument generate such a large diversity? Here, we attempt to decipher the organizational principles. We focus on amniotes and use appendage follicles as the primary examples. The integument begins as a simple planar sheet of coupled epithelial and mesenchymal cells, then becomes more complex through the following patterning processes. 1) De novo Turing periodic patterning process: This process converts the integument into multiple skin appendage units. 2) Adaptive patterning process: Dermal muscle, blood vessels, adipose tissue, and other components are assembled and organized around appendage follicles when present. 3) Cyclic renewal: Skin appendage follicles contain stem cells and their niches, enabling physiological molting and regeneration in the adult animal. 4) Spatial variations: Multiple appendage units allow modulation of shape, size, keratin types, and color patterns of feathers and hairs across the animal's surface. 5) Temporal phenotypic plasticity: Cyclic renewal permits temporal transition of appendage phenotypes, i.e. regulatory patterning or integumentary metamorphosis, throughout an animal's lifetime. The diversities in (4) and (5) can be generated epigenetically within the same animal. Over the evolutionary timescale, different species can modulate the number, size, and distributions of existing ectodermal organs in the context of micro-evolution, allowing effective adaptation to new climates as seen in the variation of hair length among mammals. Novel ectodermal organs can also emerge in the context of macro-evolution, enabling animals to explore new ecological niches, as seen in the emergence of feathers on dinosaurs. These principles demonstrate how multi-scale organ adaption in the amniotes can maximize diverse and flexible integumentary organ phenotypes, producing a vast repertoire for natural selection and thereby providing effective adaptation and evolutionary advantages.