Evolution of avian flight: muscles and constraints on performance

Abstract

One contribution of 17 to a theme issue 'Moving in a moving medium: new perspectives on flight'. Competing hypotheses about evolutionary origins of flight are the 'fundamental wing-stroke' and 'directed aerial descent' hypotheses. Support for the fundamental wing-stroke hypothesis is that extant birds use flapping of their wings to climb even before they are able to fly; there are no reported examples of incrementally increasing use of wing movements in gliding transitioning to flapping. An open question is whether locomotor styles must evolve initially for efficiency or if they might instead arrive due to efficacy. The proximal muscles of the avian wing output work and power for flight, and new research is exploring functions of the distal muscles in relation to dynamic changes in wing shape. It will be useful to test the relative contributions of the muscles of the forearm compared with inertial and aerodynamic loading of the wing upon dynamic morphing. Body size has dramatic effects upon flight performance. New research has revealed that mass-specific muscle power declines with increasing body mass among species. This explains the constraints associated with being large. Hummingbirds are the only species that can sustain hovering. Their ability to generate force, work and power appears to be limited by time for activation and deactivation within their wingbeats of high frequency. Most small birds use flap-bounding flight, and this flight style may offer an energetic advantage over continuous flapping during fast flight or during flight into a headwind. The use of flap-bounding during slow flight remains enigmatic. Flap-bounding birds do not appear to be constrained to use their primary flight muscles in a fixed manner. To improve understanding of the functional significance of flap-bounding, the energetic costs and the relative use of alternative styles by a given species in nature merit study.This article is part of the themed issue 'Moving in a moving medium: new perspectives on flight'. OverviewMuscles are obviously key to the capacity of birds for flight, and the goal of this review is to explore current hypotheses of the ways muscles permit and constrain this capacity. Insight into the phylogeny of birds is improving rapidly, and this offers great promise for improving understanding of how evolution transformed ancestral theropod forms [1] into the derived, volant bird species we observe today. Genomic study [2][3][4] and the extraordinary rate of new discovery of fossil dinosaurs [5][6][7][8][9][10] have provided rich phylogenetic hypotheses from which we can begin to test patterns of historical transformation [11]. Concurrently, modern empirical and modelling techniques in comparative biomechanics offer new ways of testing hypotheses that link form and function. These include in vivo and in situ measures of the contractile behaviour of muscle [12 -14]: high-speed, three-dimensional videography that can reveal details of wing motion [15,16]; X-ray videography of skeletal kinematics [16,17]; particle ima...

Pretectal projections to the oculomotor cerebellum in hummingbirds (Calypte anna), zebra finches (Taeniopygia guttata), and pigeons (Columba livia)

“…A perplexing problem presented by the findings of this study is that pretectal projections to the oculomotor cerebellum in zebra finches look similar to that of hummingbirds-a result that was not expected. Anna's hummingbirds have an average wingbeat frequency of~34-45 Hz (Kim, Wolf, Ortega-Jimenez, Cheng, & Dudley, 2014;Tobalske, 2016) and zebra finches also have a relatively high wingbeat frequency of 27-30 Hz during forward flight (Donovan et al, 2013;Tobalske, Puccinelli, & Sheridan, 2005). In contrast, pigeons have a much lower average wingbeat frequency (6-7 Hz) during forward flight (Berg & Biewener, 2010).…”

Approaches for testing hypotheses for the hypometric scaling of aerobic metabolic rate in animals

“…Flying animals are particularly interesting regarding constraint hypotheses, as the very high MR during flight should make them particularly susceptible to supply constraints, and there is evidence that large body size negatively affects sustainable, but not burst, performance during flight (131). For birds, mammals, and insects, power requirements increase more steeply than aerobic MR as body size increases (50,80,81), and mass-specific aerobic power output during flight declines with size across species (192). A size constraint of some type on aerobic flight performance can be supported by the observations that most small birds and insects can hover, while most of the largest insects and birds cannot.…”

Evolution of Flight Muscle Contractility and Energetic Efficiency

“…Their small body size and proportionally larger pectoral muscles allow them to sustain aloft and hovering ( Achache et al, 2017 ). In comparison with other birds, hummingbirds have significantly higher frequency wing beats (∼34 Hz) with much lower force and strain generated by the pectoralis muscles ( Tobalske, 2016 ). The duration of a neural impulse during hummingbird pectoral muscle activation is shorter than that of other birds, corresponding to a shorter time for excitation-contraction coupling during high frequency wing beats and presumably less Ca 2+ influx into myocytes with lower activation of myosin motors ( Tobalske, 2016 ).…”

“…Therefore, the functional significance for the trade-off of shorter sarcomere length in avian pectoral muscles remains to be investigated. Despite the different contractile demands of flight muscles between species, the myosin heavy chain (MHC) isoform is remarkably uniform in pectoral muscles of most avian species with very limited variation ( Velten and WelchJr., 2014 ; Tobalske, 2016 ). Since the same myosin motor is able to meet the general requirement of various types of powered flight, the different contractile and performance features of the flight muscles of different avian species may depend on adaptations and variations in the thin filament regulatory proteins.…”