Small deviations in kinematics and body form dictate muscle performances in the finely tuned avian downstroke.

Avian takeoff requires peak pectoralis muscle power to generate sufficient aerodynamic force during the downstroke. Subsequently, the much smaller supracoracoideus recovers the wing during the upstroke. How the pectoralis work loop is tuned to power flight is unclear. We integrate wingbeat-resolved muscle, kinematic, and aerodynamic recordings in vivo with a new mathematical model to disentangle how the pectoralis muscle overcomes wing inertia and generates aerodynamic force during takeoff in doves. Doves reduce the angle of attack of their wing mid-downstroke to efficiently generate aerodynamic force, resulting in an aerodynamic power dip, that allows transferring excess pectoralis power into tensioning the supracoracoideus tendon to assist the upstroke-improving the pectoralis work loop efficiency simultaneously. Integrating extant bird data, our model shows how the pectoralis of birds with faster wingtip speed need to generate proportionally more power. Finally, birds with disproportionally larger wing inertia need to activate the pectoralis earlier to tune their downstroke.

Unexpected Performance in Developing Birds.

Birds are well known for their ability to fly, and flight-capable adult birds have many anatomical specializations for meeting the demands of aerial locomotion. Juvenile birds in altricial species typically acquire these specializations close to fledging and leave the nest with some flight capability. In contrast, juveniles in most precocial species begin navigating their environment with rudimentary anatomies and may not develop full-sized wings or musculoskeletal apparatuses for several months. This manuscript explores how juvenile birds achieve high levels of locomotor performance in the absence of flight specializations, by synthesizing work on two groups of precocial birds with very different developmental strategies. Galliforms like the Chukar Partridge (Alectoris chukar) have early wing development and are capable of flight within weeks. Compared with adults, juvenile chukars have less aerodynamically effective feathers and smaller muscles but compensate through anatomical, kinematic, and behavioral mechanisms. In contrast, waterfowl have delayed wing development and initially rely on leg-based locomotion. In Mallards (Anas platyrhynchos) and their domesticated derivatives, leg investment and performance peak early in ontogeny, but then decline when wings develop. Chukar and mallard juveniles thus rely on different mechanisms for negotiating their surroundings in the absence of flight specializations. In conjunction with work in other animals, these patterns indicate that juveniles with developing locomotor apparatuses can achieve surprisingly high levels of locomotor performance through a variety of compensatory mechanisms.

Waxing and Waning of Wings.

A major challenge to Darwinian evolution is explaining 'rudimentary' organs. This is particularly relevant to birds: rudimentary wings occur in fossils, as well as in developing, molting, and flight-impaired birds. Evidence shows that young birds flap small wings to improve locomotion and transition to flight. Although small wings also occur in adults, their potential role in locomotion is rarely considered. Here we describe the prevalence of rudimentary wings in extant birds, and how wings wax and wane on many timescales. This waxing and waning is integral to the avian clade and offers a rich arena for exploring links between form, function, performance, behavior, ecology, and evolution. Although our understanding is nascent, birds clearly show that rudimentary structures can enhance performance and survival.

Building a Bird: Musculoskeletal Modeling and Simulation of Wing-Assisted Incline Running During Avian Ontogeny.

Flapping flight is the most power-demanding mode of locomotion, associated with a suite of anatomical specializations in extant adult birds. In contrast, many developing birds use their forelimbs to negotiate environments long before acquiring "flight adaptations," recruiting their developing wings to continuously enhance leg performance and, in some cases, fly. How does anatomical development influence these locomotor behaviors? Isolating morphological contributions to wing performance is extremely challenging using purely empirical approaches. However, musculoskeletal modeling and simulation techniques can incorporate empirical data to explicitly examine the functional consequences of changing morphology by manipulating anatomical parameters individually and estimating their effects on locomotion. To assess how ontogenetic changes in anatomy affect locomotor capacity, we combined existing empirical data on muscle morphology, skeletal kinematics, and aerodynamic force production with advanced biomechanical modeling and simulation techniques to analyze the ontogeny of pectoral limb function in a precocial ground bird (Alectoris chukar). Simulations of wing-assisted incline running (WAIR) using these newly developed musculoskeletal models collectively suggest that immature birds have excess muscle capacity and are limited more by feather morphology, possibly because feathers grow more quickly and have a different style of growth than bones and muscles. These results provide critical information about the ontogeny and evolution of avian locomotion by (i) establishing how muscular and aerodynamic forces interface with the skeletal system to generate movement in morphing juvenile birds, and (ii) providing a benchmark to inform biomechanical modeling and simulation of other locomotor behaviors, both across extant species and among extinct theropod dinosaurs.

New Perspectives on the Ontogeny and Evolution of Avian Locomotion.

Close correspondence between form and function is a central tenet of natural selection. One of the most striking, textbook cases for form-function congruence is the evolution of flight and the body plan of birds: compared with other tetrapods, extant adult birds have highly modified integuments and skeletons, and it has traditionally been assumed that many of these modifications are adaptations or exaptations for flight. However, developing birds that lack many of the morphological signatures of flight capacity nevertheless use their developing wings for a variety of flapping behaviors, such as wing-assisted incline running and even brief flight. Immature birds thereby demonstrate that rudimentary "flight" apparatuses are more functional than traditional assumptions about form-function relationships would predict. Here, I review the ontogeny of avian locomotion, highlighting how the developmental acquisition of flight in extant birds can improve our understanding of form-function relationships in the avian body plan, and provide insight into the evolutionary origin of flight among extinct non-avian theropod dinosaurs.

Flapping before Flight: High Resolution, Three-Dimensional Skeletal Kinematics of Wings and Legs during Avian Development.

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.

Wings versus legs in the avian bauplan: development and evolution of alternative locomotor strategies.

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.

Ontogeny of aerodynamics in mallards: comparative performance and developmental implications.

Wing morphology correlates with flight performance and ecology among adult birds, yet the impact of wing development on aerodynamic capacity is not well understood. Recent work using chukar partridge (Alectoris chukar), a precocial flier, indicates that peak coefficients of lift and drag (C(L) and C(D)) and lift-to-drag ratio (C(L):C(D)) increase throughout ontogeny and that these patterns correspond with changes in feather microstructure. To begin to place these results in a comparative context that includes variation in life-history strategy, we used a propeller and force-plate model to study aerodynamic force production across a developmental series of the altricial-flying mallard (Anas platyrhynchos). We observed the same trend in mallards as reported for chukar in that coefficients of vertical (C(V)) and horizontal force (C(H)) and C(V):C(H) ratio increased with age, and that measures of gross-wing morphology (aspect ratio, camber and porosity) in mallards did not account for intraspecific trends in force production. Rather, feather microstructure (feather unfurling, rachis width, feather asymmetry and barbule overlap) all were positively correlated with peak C(V):C(H). Throughout ontogeny, mallard primary feathers became stiffer and less transmissive to air at both macroscale (between individual feathers) and microscale (between barbs/barbules/barbicels) levels. Differences between species were manifest primarily as heterochrony of aerodynamic force development. Chukar wings generated measurable aerodynamic forces early (<8 days), and improved gradually throughout a 100 day ontogenetic period. Mallard wings exhibited delayed aerodynamic force production until just prior to fledging (day 60), and showed dramatic improvement within a condensed 2-week period. These differences in timing may be related to mechanisms of escape used by juveniles, with mallards swimming to safety and chukar flap-running up slopes to take refuge. Future comparative work should test whether the need for early onset of aerodynamic force production in the chukar, compared with delayed, but rapid, change in the mallard wing, leads to a limited repertoire of flight behavior in adult chukar compared with mallards.

From extant to extinct: locomotor ontogeny and the evolution of avian flight.

Evolutionary transformations are recorded by fossils with transitional morphologies, and are key to understanding the history of life. Reconstructing these transformations requires interpreting functional attributes of extinct forms by exploring how similar features function in extant organisms. However, extinct-extant comparisons are often difficult, because extant adult forms frequently differ substantially from fossil material. Here, we illustrate how postnatal developmental transitions in extant birds can provide rich and novel insights into evolutionary transformations in theropod dinosaurs. Although juveniles have not been a focus of extinct-extant comparisons, developing juveniles in many groups transition through intermediate morphological, functional and behavioral stages that anatomically and conceptually parallel evolutionary transformations. Exploring developmental transitions may thus disclose observable, ecologically relevant answers to long puzzling evolutionary questions.

Ontogeny of lift and drag production in ground birds.

The 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. Our findings demonstrate a clear relationship between feather morphology and aerodynamic performance. Independent of size and velocity, older wings with stiffer and more asymmetrical feathers, high numbers of barbicels and a high degree of overlap between barbules generate greater L and L:D ratios than younger wings with flexible, relatively symmetrical and less cohesive feathers. The gradual transition from immature feathers and drag-based performance to more mature feathers and lift-based performance appears to coincide with ontogenetic transitions in locomotor capacity. Younger birds engage in behaviors that require little aerodynamic force and that allow D to contribute to weight support, whereas older birds may expand their behavioral repertoire by flapping with higher tip velocities and generating greater L. Incipient wings are, therefore, uniquely but immediately functional and provide flight-incapable juveniles with access to three-dimensional environments and refugia. Such access may have conferred selective advantages to theropods with protowings during the evolution of avian flight.