Flapping before Flight: High Resolution, Three-Dimensional Skeletal Kinematics of Wings and Legs during Avian Development
Fig 1
Left. Flight-capable adult birds have many morphological features that are presumably adaptations or exaptations for meeting aerial challenges. Large wings with stiff, asymmetrical primary feathers (A) are thought to stabilize feathers against oncoming airflow [48], prevent excessive deformation [23], and reduce feather permeability [49]. Fused thoracic and sacral vertebrae may increase trunk rigidity and help transmit limb-generated forces to the rest of the body (notarium, B), and/or possibly act as a shock absorber during landing (synsacrum, C) [21,26,28,50]. Appendicularly, the robust forelimb apparatus (e.g., sternum with large keel (D), strut-like and well-articulated coracoids (E), bowed ulna (F)) allows for the attachment and contraction of powerful flight muscles (e.g., pectoralis, supracoracoideus) [27,28,26,25,21,51], while the acrocoracoid and triosseal canal (not shown; present in juveniles but less elevated above glenoid) allow the supracoracoideus muscle to act as a pulley, contributing to humeral elevation and rotation [28,26,29–33]. Distally, reduced and fused skeletal elements and channelized limb joints (G, H) are thought to reduce mass and permit rapid, efficient limb oscillation, coordinate elbow and wrist movement, keep a planar wing orientation during the downstroke, and increase stride effectiveness by restricting ankle movements to a single plane of motion [27,28,26,22,52]. Collectively, these features are a key component of the avian bauplan, and a classic example of anatomical specialization. Right. Developing birds–like early winged dinosaurs–lack many hallmarks of advanced flight capacity [10]. Instead of large wings they have small protowings, with a more gracile skeleton and less constrained joints. Immature birds nevertheless flap their rudimentary wings to accomplish a variety of locomotor tasks [20,53–55]; in fact, many anatomical specializations of adults are acquired long after flight capacity is achieved. Developing birds thereby challenge the traditional, longstanding view of form-function relationships in the theropod-avian lineage (A-H). Cervical vertebrae and pedal phalanges not shown; juvenile keel on top of adult keel, for scale (D); in (G), left image is pronation of carpometacarpus, right is abduction (juvenile joints always more flexible). Although cartilaginous skeletal components are not shown, this does not alter functional interpretations of the juvenile skeleton (e.g., juveniles possess a small cartilaginous extension of the keel, but both the keel and the muscles that attach to it are still proportionally much smaller in juveniles than adults; carpal bones of developing birds have the specialized shapes of adults, but are poorly ossified and not capable of resisting enough joint torque to channelize the wrist joint (G)). Images of feather microstructure (A) reprinted from [18] under a CC BY license, with permission from The Company of Biologists Limited, original copyright 2011.