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

PLoS One. 2016 Apr 21;11(4):e0153446. doi: 10.1371/journal.pone.0153446. eCollection 2016.

Abstract

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.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.
  • Validation Study

MeSH terms

  • Animals
  • Biomechanical Phenomena
  • Flight, Animal*
  • Galliformes / physiology*
  • Leg Bones / anatomy & histology
  • Leg Bones / physiology*
  • Tomography, X-Ray Computed
  • Wings, Animal / anatomy & histology
  • Wings, Animal / physiology*

Grant support

Funding was provided by the National Science Foundation Graduate Research Fellowship, award number GRFP-2007057068 to AMH, by the National Science Foundation grant entitled, ‘‘Ontogeny of Avian Locomotion: Aerodynamics, Skeletal Kinematics, and Neuromuscular Control’’, award number 0919799 to KPD and others, and by the W.M. Keck Foundation grant entitled, ‘‘A Proposal to Design and Build a Dynamic 3-D Skeletal Imaging System’’, to KPD and others.