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

Heers, Ashley M.; Dial, Kenneth P.

doi:10.1016/j.tree.2011.12.003

Cited by 88 publications

(113 citation statements)

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“…Using wingbeats to support weight and generate thrust requires enormous work and power output from the primary flight muscles [12,13,26,27] whereas gliding, with isometric contractions, requires a smaller mass of muscle to support body weight [28,29]. The massive energetic investment in paired pectoralis and supracoracoideus muscles used to power flight in extant birds [30,31], coupled with a prominent, ossified keel that does not appear in early fossil forms [1,32], make it initially appear obvious that flapping must be more derived than gliding. Historically, the argument over which kinematic event was most likely to provide an incremental first step in the origin of bird flight, something that could be favoured by directional selection for increased performance, was framed as a dichotomy between an arboreal hypothesis in which ancestors climbed up and then glided down (e.g.…”

Section: Evolutionary Origins Of Avian Flightmentioning

confidence: 99%

“…This behaviour has been studied extensively in ontogenetic series up to adults in several species of Galliform birds [32,[38][39][40][41][42][43] and in adult pigeons (C. livia; [26]). Additionally, wing-assisted swimming and branching behaviour are described for developing ducks (Anseriformes) and owls (Strigiformes; [44]).…”

Section: Evolutionary Origins Of Avian Flightmentioning

confidence: 99%

“…The central argument is that the developing wing can provide useful, incrementally increasing forces for locomotion even before the birds can fly. Notably, this is also when they do not have fully ossified skeletons [32].…”

Section: Evolutionary Origins Of Avian Flightmentioning

confidence: 99%

“…Analysed in the context of a flapping origin, the locomotor capacity of fossil forms has been bracketed or estimated using fossilized details of wing anatomy and body size, extant data on limb kinematics in flying birds and running lizards, and empirical measures of aerodynamic force production by the partially developed wings of juvenile birds [51]. According to this line of reasoning, the incremental acquisition of locomotor capacity within ontogenetic series of birds is a useful extant system that can provide insight into evolutionary trajectories precisely because the incremental changes during ontogeny each result in improved functional capacity [32,44]. Proponents argue that an extant model system is more parsimonious as an explanation for incremental evolutionary steps.…”

Section: Evolutionary Origins Of Avian Flightmentioning

confidence: 99%

“…A possible explanation for the lack of extant intermediate styles of wing motion is that they may not represent peaks in an adaptive landscape sensu Wright [52]. This possibility merits testing in ways that integrate palaeontology, phylogenetics and biomechanics [32,50,51]. Figure 1.…”

Section: Evolutionary Origins Of Avian Flightmentioning

confidence: 99%

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Evolution of avian flight: muscles and constraints on performance

Tobalske¹

2016

Phil. Trans. R. Soc. B

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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...

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Section: Evolutionary Origins Of Avian Flightmentioning

confidence: 99%

Section: Evolutionary Origins Of Avian Flightmentioning

confidence: 99%

Section: Evolutionary Origins Of Avian Flightmentioning

confidence: 99%

Section: Evolutionary Origins Of Avian Flightmentioning

confidence: 99%

Section: Evolutionary Origins Of Avian Flightmentioning

confidence: 99%

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Evolution of avian flight: muscles and constraints on performance

Tobalske¹

2016

Phil. Trans. R. Soc. B

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Evolution of Avian Flight

Heers

2013

Encyclopedia of Life Sciences

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The origin of birds and of bird flight has drawn scientific interest since the inception of evolutionary thinking. Though early investigations were hampered by a paucity of fossils, new discoveries have filled in many gaps and provided unprecedented detail into morphological changes that attended the evolutionary appearance of birds and bird flight. Birds are now widely regarded as the descendents of theropod dinosaurs. In contrast, form–function relationships and behaviours that might have facilitated the evolutionary acquisition of flight remain widely debated. Given the versatility of extant birds, we should not expect to find only one solution to this problem. Nevertheless, much debate seems to stem not from looking for multiple plausible functions and behaviours, but rather from traditional ‘ground up’ versus ‘trees down’ assumptions and a general lack of experimental and ecological support for inferred form–function relationships. Many researchers have therefore called for more rigorous hypothesis testing, and a plethora of new techniques and perspectives are up to the challenge. Key Concepts: Birds are the descendents of bipedal theropod dinosaurs. Evolutionary assembly of the avian body plan occurred gradually, with bird‐like wings evolving before bird‐like skeletons, in conjunction with a reduction in body size and then a cranial shift in centre of mass. These changes took place via a series of transitional anatomical stages that were presumably associated with transitional functions and behaviours before becoming co‐opted for flapping flight. Many origin‐of‐flight hypotheses have been proposed, and it is challenging to discriminate among them. Much debate seems to stem from traditional ‘ground up’ versus ‘trees down’ assumptions and a general lack of experimental and ecological support for inferred form–function relationships. A growing number of researchers have therefore suggested that hypotheses must be consistent not only with the fossil record, but also with experimental support for form–function relationships and behaviours inferred by origin‐of‐flight scenarios. New techniques and perspectives are meeting this challenge and providing more rigorous insight into the origin of flight in birds. For example, recent work on developing birds with dinosaur‐like anatomies clearly demonstrates that behaviours involving the cooperative use of wings and legs (e.g. wing‐assisted incline running and steaming) act as a developmental (or evolutionary) bridge between leg‐based terrestrial locomotion and wing‐based aerial locomotion, by allowing developing birds (or evolving dinosaurs) to supplement their wings with their legs until the wings can fully support body weight during flight.

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Terrestrial ecosystems

Bottjer¹

2016

Paleoecology

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

Cited by 88 publications

References 67 publications

Evolution of avian flight: muscles and constraints on performance

Evolution of avian flight: muscles and constraints on performance

Evolution of Avian Flight

Terrestrial ecosystems

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