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

Ashley M Heers,Jeffery W Rankin,John R Hutchinson

doi:10.3389/fbioe.2018.00140

Abstract

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.

Highlights

Darwin described “survival of the fittest,” illustrating how organisms with certain forms might better perform certain functions and have greater fitness, such that form and function are closely linked (Darwin, 1859)
Timing of Muscle Activations, Length Changes, and Force Development Our simulations of wing-assisted incline running (WAIR) on 65◦ slopes yielded patterns of muscle activation that were broadly consistent with patterns of EMG activity in flying birds (Figure 4)
Ascending flight provides a reasonable comparison because it has a similar body trajectory to WAIR and comparable flapping kinematics [chukars show similar directions of movement, e.g., flexion vs. extension, but greater ranges of motion, in flight vs. WAIR (Baier et al, 2013)]

Summary

Introduction

Darwin described “survival of the fittest,” illustrating how organisms with certain forms might better perform certain functions and have greater fitness, such that form and function are closely linked (Darwin, 1859). Geneticists are exploring “arrival of the fittest”: how novel phenotypes are added to the pool of individuals that encounter selective forces (Gilbert and Epel, 2009). The intermediate stages that bridge embryonic genotypes and adult phenotypes (i.e., post-hatching/postnatal ontogeny), or extinct and extant bauplans (i.e., evolution), are often an enigma in functional morphology. These types of questions have long fascinated evolutionary biologists (Mivart, 1871), and are very relevant—though less studied—in developing organisms (Heers and Dial, 2012). This “dilemma of incipient stages” (Gould, 1985) is striking among birds and their theropod dinosaur ancestors

Objectives

Methods

Results

Discussion

Conclusion