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Locomotor Ontogeny and the Evolution of Avian Flight

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Locomotor Ontogeny and the Evolution of Avian Flight Review From extant to extinct: locomotor ontogeny and the evolution of avian flight Ashley M. Heers and Kenneth P. Dial Division of Biological Sciences, University of Montana, Missoula, MT 59812, USA Evolutionary transformations are recorded by fossils with Glossary transitional morphologies, and are key to understanding Asymmetric feathers: pennaceous feathers in which the vanes on either side of the history of life. Reconstructing these transformations the rachis (central shaft) are different widths, with the trailing edge vane requires interpreting functional attributes of extinct conspicuously wider than the leading edge vane; asymmetry is thought to help forms by exploring how similar features function in extant stabilize primary flight feathers (along the metacarpals and phalanges) against oncoming airflow. organisms. However, extinct–extant comparisons are of- Avialans: members of a group of theropod dinosaurs that has traditionally ten difficult, because extant adult forms frequently differ included Archaeopteryx (the earliest ‘bird’) (cf. [80]) and living birds (Figure 1, substantially from fossil material. Here, we illustrate how node E, main text). Caudofemoral muscle: muscle that attaches to the tail and femur, and that postnatal developmental transitions in extant birds can helps retract the hindlimb in non-avian reptiles. provide rich and novel insights into evolutionary trans- Channelized wrist: wrist with restricted movement; in birds, a series of ridges formations in theropod dinosaurs. Although juveniles and grooves (ventral ridge of the carpometacarpus, V-shaped ulnare and articular ridge of the ulna) in the wrist interlock and channelize movement. have not been a focus of extinct–extant comparisons, Contour feathers: pennaceous feathers that cover the wings and body of a bird. developing juveniles in many groups transition through Controlled flapping descent (CFD): locomotor behavior used by juvenile birds that involves flapping the wings to slow and control aerial descents. intermediate morphological, functional and behavioral Keel: large, bony structure projecting beneath the sternum of a bird, similar to stages that anatomically and conceptually parallel evolu- the keel on a boat; site for attachment of major flight muscles (pectoralis and tionary transformations. Exploring developmental transi- supracoracoideus). Maniraptorans: members of a group of theropod dinosaurs (Figure 1, nodes B tions may thus disclose observable, ecologically relevant and C, main text). answers to long puzzling evolutionary questions. Manus: hand (metacarpals and phalanges); also known as the carpometacar- pus in birds. Evolutionary transformations Ontogenetic transitional wing (OTW) hypothesis: hypothesis stating that extinct theropods with protowings might have behaved similar to juvenile Evolutionary transformations are central to the history of birds, flapping their incipient wings to navigate three-dimensional environ- life. Throughout the 3–4-billion year saga of life on Earth, ments by flap-running up steep terrains (wing-assisted incline running) and using controlled flapping descents to come back down [66]. fossils with transitional morphologies have recorded large- Ornithurines: members of a group of theropod dinosaurs, whose most basal scale evolutionary changes that are key for understanding members are similar in appearance to extant birds (Figure 1, node H, main text). the origins of major clades and adaptations [1–3]. To Paravians: members of a group of theropod dinosaurs (Figure 1, node D, main text). reconstruct these transformations, scientists attempt to Pennaceous feathers: feathers that have a rachis (central shaft) with barbs deduce the functional attributes of extinct morphological attached to either side, forming vanes. forms by exploring how similar features function in or Plumulaceous feathers: ‘downy’ feathers that lack a rachis (central shaft). Primary feathers: pennaceous feathers along the distal forelimb (metacarpals across extant organisms. However, comparing extinct and phalanges); in extant flight-capable adult birds, primary feathers are and extant organisms to interpret the functional capacities asymmetric, whereas secondary feathers (along the ulna) are more symmetric. of fossils with transitional morphologies is often difficult, Protowings: small, incipient wings that are often characterized by distally unfurled and/or symmetric feathers, and that are often restricted to the distal because transitional fossils occur as morphological mosaics forelimb [secondary feathers (along the ulna) and/or tertial feathers (along the of ancestral and derived character states, with suites of humerus) not preserved]. features that are frequently absent in extant adults. There- Pygostyle: bony structure at the end of the tail in birds, formed by the fusion of tail vertebrae; attachment site for the rectricial bulbs and associated muscles. fore, transitional fossils commonly appear to lack extant Pygostylians: members of a group of theropod dinosaurs (Figure 1, node F, homologs or analogs. Consequently, hypotheses concern- main text). ing the functional attributes of such fossils often seem Rectricial bulbs: fibro-adipose structures, on either side of the pygostyle, that encase the roots of the tail feathers; muscles associated with the rectricial untestable [4], constraining the ability to advance under- bulbs control tail fanning and orientation. standing of evolutionary transformations. Symmetric feathers: pennaceous feathers in which the vanes on either side of the rachis (central shaft) are approximately the same width. Transitional features have long been known to occur Synsacrum: fused sacral vertebrae (in a bird). in prenatal stages of extant organisms (e.g. gill slits in Tertial feathers: pennaceous wing feathers that lie along the humerus, humans [5]), but their functional significance is difficult between the elbow and the body. Theropods: members of a group of dinosaurs that includes the most probable to examine in these passive developmental stages. By ancestors of extant birds. Triosseal canal: a bony channel typically formed by the coracoid, scapula and Corresponding author: Heers, A.M. ([email protected]). furcula (bones in the shoulder girdle), through which the tendon of the Keywords: ontogeny; paleontology; transitional stages; form-function; flight; supracoracoideus (upstroke muscle) passes. evolution; birds; dinosaurs. 296 0169-5347/$ – see front matter ß 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2011.12.003 Trends in Ecology and Evolution, May 2012, Vol. 27, No. 5 Review Trends in Ecology and Evolution May 2012, Vol. 27, No. 5 Wing-assisted incline running (WAIR): a locomotor behavior used by juvenile evolution of insect flight [6]. Sea squirt larvae resemble a and adult birds that involves flapping the wings while running up steep slopes; hypothesized stage of early chordate evolution and have flapping generates aerodynamic forces that drive the feet into the substrate and increase traction, thereby allowing birds to ascend steep obstacles within been used to explore chordate and vertebrate origins [7], their habitat. whereas marsupials use an ancestral amniote-like (quad- rate-articular) jaw joint for feeding early in postnatal devel- contrast, postnatal ontogenetic trajectories among extant opment and can elucidate early mammalian evolution [9]. species offer rich opportunities for quantitatively investi- Thus, ontogenetic trajectories and the functional capacities gating form and function in transitional stages [6–11, of juveniles with transitional morphologies can provide rich B.E. Jackson, unpublished results], yet are relatively unex- and novel insight into a broad array of evolutionary trans- plored. Postnatal ontogeny has not been a focus of extinct– formations, by clarifying the potential functional capacities extant comparisons (Box 1), although many examples of fossils with similar transitional morphologies. This un- demonstrate that juveniles share unique similarities with tapped utility of postnatal ontogeny is perhaps best illus- transitional fossils. Unlike passive prenatal stages, postna- trated through one of the most highly debated and recently tal juveniles make use of transitional morphologies to loco- rejuvenated evolutionary discussions: the origin and evolu- mote and/or survive and thus actualize form–function tion of avian flight. relationships during morphological transformations. For example, during the transition from aquatic to terrestrial Ontogeny and evolution: a case study life, metamorphosing salamanders progress through sever- The origin of birds and of bird flight has attracted scientific al morphological transformations (loss of tail fins, loss of attention since the advent of evolutionary theory [13]. gills, etc.). These anatomical changes are similar to many Based on numerous lines of evidence, it is now widely of those that occurred during the aquatic-to-terrestrial evo- accepted that birds evolved from bipedal theropod dino- lutionary transition in the ancestors of tetrapods [12]. saurs [14–21] (see Glossary; Velociraptor and Tyrannosau- Therefore, investigating how morphological shifts influence rus are well-known examples). By contrast, locomotor organ function during developmental transitions in juvenile behaviors (gliding, flap-running, etc.) that might have salamanders might provide insight into the functioning of facilitated the evolutionary acquisition of flight remain a organ systems during the evolutionary transition from
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