The role of mechanical forces on the patterning of the avian feather‐bearing skin: A biomechanical analysis of the integumentary musculature in birds

Abstract

The integumentary musculature of birds consists of three distinct components. The smooth musculature comprises feather and apterial muscles, which form a continuous musculo-elastic layer within the dermis. The feather muscles, which consistently include at least erectors and depressors, interconnect contour feathers within pterylae (i.e., feather tracts) along gridlines that are oriented diagonally to the longitudinal and transverse axes of the body. The apterial muscles interconnect pterylae by attaching to the contour feathers along their peripheries. The striated musculature is composed of individual subcutaneous muscles, most of which attach to contour feathers along the caudal periphery of pterylae A new integrative functional analysis of the integumentary musculature proposes how apterial muscles stabilize the pterylae and modulate the tension of the musculo-elastic layer, and how subcutaneous muscles provide the initial stimulus for erector muscles being able to ruffle the contour feathers within pterylae. It also shows how the arrangement of the contour feathers and integumentary muscles reflects the stresses and strains that act on the avian skin. These mechanical forces are in effect not only in the adult, especially during flight, but may also be active during feather morphogenesis. The avian integument with its complex structural organization may, therefore, represent an excellent model for analyzing the nature of interactions between the environment and genetic material. The predictions of our model are testable, and our study demonstrates the relevance of integrated analyses of complex organs as mechanically coherent systems for evolutionary and developmental biology.

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

“…Functional morphological studies can gauge the selective regime that may have been responsible for driving the evolutionary modification of a particular structure (Bartels, 2003;Bragulla and Hirschberg, 2003;Hamrick, 2003;Homberger and de Silva, 2003). The direct mechanical interactions between the integument and its environment (i.e., land surfaces, air, and water) make locomotion possible.…”

“…Feathers are responsible for the aerodynamically streamlined body and the airfoils of the wings and tail that enable birds to fly. Furthermore, to move through air, the integument needs to ensure a laminar airflow over the body surface (e.g., see Homberger and de Silva 2003). The various physical interactions between the body surface and the environment are complex and dynamic, and they create powerful selective regimes that are responsible for a significant part of the structural diversity of the vertebrate integument (see Bragulla and Hirschberg, 2003;Hamrick, 2003;Homberger and de Silva, 2003).…”

“…Layer upon layer, molecular modules can be called upon and used in different contexts to build an increasingly complicated structure (Harris et al, 2002). Furthermore, the individual integumentary appendages need to be integrated within the organism (Homberger and de Silva, 2003).…”

“…For example, integumentary appendages are connected to and affected by muscles, nerves, blood vessels, etc. and integumentary patterns may be induced and maintained by regimens of mechanical forces acting on, or generated by, the organism (Bragulla and Hirschberg, 2003;Homberger and de Silva, 2003).…”

“…For example, oxygen concentration during development can influence the level of tracheal tube branching (Jarecki et al,'99). Mechanical forces may be instrumental in modulating and even inducing the timing, distribution, and local activity of gene expression and signaling molecules (Homberger and de Silva, 2003). Research on human pathological conditions (e.g., atherosclerosis and osteoporosis) has shown that mechanical forces may affect gene expression through integrin and, subsequently, the enhancer region of certain genes.…”