Multiple Functional Solutions During Flightless to Flight-Capable Transitions (1 Viewer)

[RSN]

Ashley M. Heers, Stephanie L. Varghese, Leila K. Hatier and Jeremiah J. Cabrera

Multiple Functional Solutions During Flightless to Flight-Capable Transitions

Front. Ecol. Evol., 10 February 2021
doi.org/10.3389/fevo.2020.573411

Abstract

The evolution of avian flight is one of the great transformations in vertebrate history, marked by striking anatomical changes that presumably help meet the demands of aerial locomotion. These changes did not occur simultaneously, and are challenging to decipher. Although extinct theropods are most often compared to adult birds, studies show that developing birds can uniquely address certain challenges and provide powerful insights into the evolution of avian flight: unlike adults, immature birds have rudimentary, somewhat “dinosaur-like” flight apparatuses and can reveal relationships between form, function, performance, and behavior during flightless to flight-capable transitions. Here, we focus on the musculoskeletal apparatus and use CT scans coupled with a three-dimensional musculoskeletal modeling approach to analyze how ontogenetic changes in skeletal anatomy influence muscle size, leverage, orientation, and corresponding function during the development of flight in a precocial ground bird (Alectoris chukar). Our results demonstrate that immature and adult birds use different functional solutions to execute similar locomotor behaviors: in spite of dramatic changes in skeletal morphology, muscle paths and subsequent functions are largely maintained through ontogeny, because shifts in one bone are offset by changes in others. These findings help provide a viable mechanism for how extinct winged theropods with rudimentary pectoral skeletons might have achieved bird-like behaviors before acquiring fully bird-like anatomies. These findings also emphasize the importance of a holistic, whole-body perspective, and the need for extant validation of extinct behaviors and performance. As empirical studies on locomotor ontogeny accumulate, it is becoming apparent that traditional, isolated interpretations of skeletal anatomy mask the reality that integrated whole systems function in frequently unexpected yet effective ways. Collaborative and integrative efforts that address this challenge will surely strengthen our exploration of life and its evolutionary history.

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[Fred Ruhe]

Figure 1. Ontogeny and Evolution of the Avian Flight Apparatus. Flight-capable adult birds are characterized by a suite of anatomical features that presumably are adaptations or exaptations for flight. Some of these structures are functionally intuitive, whereas others have no known or demonstrated function(s) but are considered aptations based on their presence in flight capable birds and their absence in flightless birds and extinct theropods.

(A) Stiff, cohesive, and asymmetrical (primaries only) feathers presumably provide stability and reduce permeability for aerodynamic force production (Norberg, 1985; Muller and Patone, 1998; Nudds and Dyke, 2010; Heers et al., 2011; Dial et al., 2012). Fused vertebrae are thought to stabilize the trunk while transferring wing- or leg-generated forces to the body (notarium, (B), and/or absorb shock 12 (synsacrum, (C) (Ostrom, 1976, 1979; Bock, 1986; Kisia, 2010). A robust flight apparatus (e.g., keeled sternum (D), long and firmly-articulated coracoids (E), long scapulae (F), furcula (G) permits the attachment and contraction of large, powerful muscles (e.g., pectoralis, supracoracoideus) (George and Berger, 1966; Ostrom, 1974, 1976, 1979, 1986; Bock, 1986), while the triosseal canal (H) (not visible, but present in all age classes shown) allows the supracoracoideus muscle to function similarly to a pulley and elevate and rotate the wing during upstroke (Walker, 1972; Ostrom, 1976, 1979; Rayner, 1988; Norberg, 1990; Poore et al., 1997; Ostrom et al., 1999). Reduced and fused elements in the distal limbs, coupled with channelized joints (I, J), likely reduce weight and facilitate swift limb oscillation, help coordinate joint movements, and restrict joint motion to keep the wing in a planar orientation during downstroke, or the ankle confined to movements in the direction of motion (Ostrom, 1974, 1976, 1979; Coombs, 1978; Vazquez, 1992). Unlike adult birds, developing birds and early winged dinosaurs like Archaeopteryx lack many of these flight aptations: their wings are smaller and/or less aerodynamically effective, and their skeletons are more gracile and less constrained (Heers et al., 2011, 2014; Heers and Dial, 2012). Immature birds nevertheless recruit their rudimentary wings during a variety of locomotor behaviors (italicized text, and inset: wing-assisted incline running, i.e., WAIR (top left); wing assisted jumping (top right), varying degrees of flight (bottom)), and achieve flight capacity long
before flight aptations are fully acquired (Dial, 2003; Dial et al., 2008, 2015; Dial and Carrier, 2012; Heers and Dial, 2015; Heers et al., 2016). Images of Chukar Partridges modified, with permission, from (Heers and Dial, 2012; Heers et al., 2018); images of Archaeopteryx (top: by Gerhard Heilmann (Heilmann, 1927); bottom: by H. Raab, licensed under CC BY-SA 3.0) in public domain. Not to scale.