Morphological Evolution of Bird Wings Follows a Mechanical Sensitivity Gradient Determined by the Aerodynamics of Flapping Flight

The physical principles that govern the function of biological structures also mediate their evolution, but the evolutionary drivers of morphological traits within complex structures can be difficult to predict. Here, we use morphological traits measured from 1096 3-dimensional bird wing scans from 178 species to test the interaction of two frameworks for relating morphology to evolution. We examine whether the evolutionary rate (σ) and mode is dominated by the modular organization of the wing into handwing and armwing regions, and/or the relationship between trait morphology and functional output (i.e. mechanical sensitivity, driven here by flapping flight aerodynamics). Our results support discretization of the armwing and handwing as morphological modules, but morphological disparity and σ varied continuously with the mechanical sensitivity gradient and were not modular. Thus, mechanical sensitivity should be considered an independent and fundamental driver of evolutionary dynamics in biomechanical traits, distinct from morphological modularity.