Transformation of a functional complex: early evolution of the flight apparatus of birds

Although finds of pre-modern (non-Neornithine) Mesozoic birds were exceptionally rare for over a century following the discovery of Archaeopteryx in the mid-nineteenth century, new material has accumulated at an extraordinary rate in the previous two to three decades. These finds document one of the most striking functional transformations in the evolution of terrestrial vertebrates, but arguably remain under-exploited by studies of the functional or biomechanical evolution of flight. This study probes the morphological and functional transformations that occurred in the furcula, or wishbone, an element formed by midline fusion of the clavicles. The furcula plays a central role in the avian musculoskeletal flight complex, as it is a key site of muscular attachment for the flight musculature, and is also known to play a dynamic physiological function in the secondary respiratory system. A geometric morphometric analysis of furcular morphology in extant birds reveals that curvature is partially correlated with flight mode. Only members of the more derived Mesozoic clade Ornithuromorpha share regions of furcular morphospace occupied by modern taxa; their sister-group, the enantiornithes, reside in a comparatively unique region. Variation in furcular morphology captured by this morphospace analysis is shown to have potentially important consequences for the structural performance of the furcula; flexural stiffness is greatest in furculae with a narrow interclavicular angle and U-shaped curvature, while broad interclavicular angles and V-shapes confer greater stiffness. Although it appears plausible that the correlation between furcular morphology and flight mode is the result of the demands placed on the structural performance of the element, with certain modes demanding greater stiffness or flexibility, structural analysis of large sample of extant avian furculae using finite-element analysis does not show statistically significant differences in flexural stiffness. However, a clear trend toward greater flexibility in more derived lineages is evident in pre-modern birds, and it appears most likely that a dynamic physiological role was not acquired in clades more basal than the group that encompasses crown-group birds, the ornithuromorphs.