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. J. Exp. Zool. (Mol. Dev. Evol.) 298B:123–139, 2003. © 2003 Wiley-Liss, Inc.