SUMMARYThe juvenile period is often a crucial interval for selective pressure on locomotor ability. Although flight is central to avian biology, little is known about factors that limit flight performance during development. To improve understanding of flight ontogeny, we used a propeller (revolving wing) model to test how wing shape and feather structure influence aerodynamic performance during development in the precocial chukar partridge (Alectoris chukar, 4 to >100 days post hatching). We spun wings in mid-downstroke posture and measured lift (L) and drag (D) using a force plate upon which the propeller assembly was mounted. Supplementary material available online at
Wings have long been regarded as a hallmark of evolutionary innovation, allowing insects, birds, and bats to radiate into aerial environments. For many groups, our intuitive and colloquial perspective is that wings function for aerial activities, and legs for terrestrial, in a relatively independent manner. However, insects and birds often engage their wings and legs cooperatively. In addition, the degree of autonomy between wings and legs may be constrained by tradeoffs, between allocating resources to wings versus legs during development, or between wing versus leg investment and performance (because legs must be carried as baggage by wings during flight and vice versa). Such tradeoffs would profoundly affect the development and evolution of locomotor strategies, and many related aspects of animal ecology. Here, we provide the first evaluation of wing versus leg investment, performance and relative use, in birds-both across species, and during ontogeny in three precocial species with different ecologies. Our results suggest that tradeoffs between wing and leg modules help shape ontogenetic and evolutionary trajectories, but can be offset by recruiting modules cooperatively. These findings offer a new paradigm for exploring locomotor strategies of flying organisms and their extinct precursors, and thereby elucidating some of the most spectacular diversity in animal history.
Some of the greatest transformations in vertebrate history involve developmental and evolutionary origins of avian flight. Flight is the most power-demanding mode of locomotion, and volant adult birds have many anatomical features that presumably help meet these demands. However, juvenile birds, like the first winged dinosaurs, lack many hallmarks of advanced flight capacity. Instead of large wings they have small “protowings”, and instead of robust, interlocking forelimb skeletons their limbs are more gracile and their joints less constrained. Such traits are often thought to preclude extinct theropods from powered flight, yet young birds with similarly rudimentary anatomies flap-run up slopes and even briefly fly, thereby challenging longstanding ideas on skeletal and feather function in the theropod-avian lineage. Though skeletons and feathers are the common link between extinct and extant theropods and figure prominently in discussions on flight performance (extant birds) and flight origins (extinct theropods), skeletal inter-workings are hidden from view and their functional relationship with aerodynamically active wings is not known. For the first time, we use X-ray Reconstruction of Moving Morphology to visualize skeletal movement in developing birds, and explore how development of the avian flight apparatus corresponds with ontogenetic trajectories in skeletal kinematics, aerodynamic performance, and the locomotor transition from pre-flight flapping behaviors to full flight capacity. Our findings reveal that developing chukars (Alectoris chukar) with rudimentary flight apparatuses acquire an “avian” flight stroke early in ontogeny, initially by using their wings and legs cooperatively and, as they acquire flight capacity, counteracting ontogenetic increases in aerodynamic output with greater skeletal channelization. In conjunction with previous work, juvenile birds thereby demonstrate that the initial function of developing wings is to enhance leg performance, and that aerodynamically active, flapping wings might better be viewed as adaptations or exaptations for enhancing leg performance.
Reconstructing the tree of life requires deciphering major evolutionary transformations and the functional capacities of fossils with “transitional” morphologies. Some of the most iconic, well-studied fossils with transitional features are theropod dinosaurs, whose skeletons and feathered forelimbs record the origin and evolution of bird flight. However, in spite of over a century of discussion, the functions of forelimb feathers during the evolution of flight remain enigmatic. Both aerodynamic and non-aerodynamic roles have been proposed, but few of the form-function relationships assumed by these scenarios have been tested. Here, we use the developing wings of a typical extant ground bird (Chukar Partridge) as possible analogues/homologues of historical wing forms to provide the first empirical evaluation of aerodynamic potential in flapping theropod “protowings.” Immature ground birds with underdeveloped, rudimentary wings generate useful aerodynamic forces for a variety of locomotor tasks. Feather development in these birds resembles feather evolution in theropod dinosaurs, and reveals a predictable relationship between wing morphology and aerodynamic performance that can be used to infer performance in extinct theropods. By spinning an ontogenetic series of spread-wing preparations on a rotating propeller apparatus across a range of flow conditions and measuring aerodynamic force, we explored how changes in wing size, feather structure, and angular velocity might have affected aerodynamic performance in dinosaurs choosing to flap their incipient wings. At slow angular velocities, wings produced aerodynamic forces similar in magnitude to those produced by immature birds during behaviors like wing-assisted incline running. At fast angular velocities, wings produced forces sufficient to support body weight during flight. These findings provide a quantitative, biologically relevant bracket for theropod performance and suggest that protowings could have provided useful aerodynamic function early in maniraptoran history, with improvements in aerodynamic performance attending the evolution of larger wings, more effective feather morphologies, and faster angular velocities.
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