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. 2011;6(8):e22292.
doi: 10.1371/journal.pone.0022292. Epub 2011 Aug 9.

Assessing arboreal adaptations of bird antecedents: testing the ecological setting of the origin of the avian flight stroke

T Alexander Dececchi  1 , Hans C E Larsson
Affiliations

Assessing arboreal adaptations of bird antecedents: testing the ecological setting of the origin of the avian flight stroke

T Alexander Dececchi et al. PLoS One. 2011.

Abstract

The origin of avian flight is a classic macroevolutionary transition with research spanning over a century. Two competing models explaining this locomotory transition have been discussed for decades: ground up versus trees down. Although it is impossible to directly test either of these theories, it is possible to test one of the requirements for the trees-down model, that of an arboreal paravian. We test for arboreality in non-avian theropods and early birds with comparisons to extant avian, mammalian, and reptilian scansors and climbers using a comprehensive set of morphological characters. Non-avian theropods, including the small, feathered deinonychosaurs, and Archaeopteryx, consistently and significantly cluster with fully terrestrial extant mammals and ground-based birds, such as ratites. Basal birds, more advanced than Archaeopteryx, cluster with extant perching ground-foraging birds. Evolutionary trends immediately prior to the origin of birds indicate skeletal adaptations opposite that expected for arboreal climbers. Results reject an arboreal capacity for the avian stem lineage, thus lending no support for the trees-down model. Support for a fully terrestrial ecology and origin of the avian flight stroke has broad implications for the origin of powered flight for this clade. A terrestrial origin for the avian flight stroke challenges the need for an intermediate gliding phase, presents the best resolved series of the evolution of vertebrate powered flight, and may differ fundamentally from the origin of bat and pterosaur flight, whose antecedents have been postulated to have been arboreal and gliding.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Plot of the first and second principal coordinates (PCO) of discrete locomotory traits.
PCO values are calculated in Euclidean and presented for the total dataset of a selection of extant mammals, scansorial lizards, a scansorial and arboreal chameleon, and three extinct arboreal taxa (A), the total taxon set using only hindlimb morphologies (B), a partition of only quadrupedal mammals and reptiles with non-avian theropods and Archaeopteryx using only hindlimb morphologies (C), and a partition of only non-avian theropods and birds using a dataset tailored for bird morphologies (D). Each category of taxa are plotted within their respective convex hulls and category labels are given near each category's average, denoted by a star. Non-avian theropods are represented in green hulls, birds in blue hulls, mammals in purple hulls, scansorial lizards in yellow hulls, and fossil arboreal taxa in grey hulls. Basal Mesozoic birds are plotted as red filled circles. The variance explained by each PCO axis is given in parentheses after each axis label. [planned for page width].
Figure 2
Figure 2. Box-plots of the first principal coordinate axis of discrete locomotory traits.
(A) are extant quadrupedal mammals and reptiles compared to non-avian theropods and (B) extant birds to non-avian theropods and Mesozoic birds. PCO values are calculated in Euclidean. Note that non-avian theropods and Archaeopteryx cluster with terrestrial taxa at the extreme left of the graphs and have no overlap with scansorial or arboreal mammals and reptiles nor perching birds. The arboreal and scansorial chameleons are plotted to the right of the scansorial lizards. The variance explained by each PCO axis is given in parentheses after each axis label. Basal birds are labelled as: Archaeopteryx, A; Confuciusornis, C; Jeholornis, J; Pengornis, P; Sapeornis, Sa; Sinornis, Si. The filled circles represent positions for figured taxa. In (A), non-avian theropods = Microraptor zhaoianus, terrestrial = horse (Equus), scansorial = Red Panda (Ailurus filgens), arboreal = Grey Squirrel (Sciurus carolinensis), scansorial lizards – Anolis carolinensis, fossil arboreal – Megalancosaurus. In (B) non-avian theropods = Microraptor zhaoianus, basal birds = Sinornis santensis, ground based birds = Ostrich (Struthio camelus), ground foragers = Common Raven (Corvus corax), birds of prey = Great Horned Owl (Bubo virginianus), aerial foragers = Chimney Swift (Chaetura pelagica), climbers = Eurasian Nuthatch (Sitta europaea). Silhouettes of Microrapor and Sinornis are based on Hu and colleagues and Sereno and Rao , respectively. Silhouettes are not to scale. [planned for page width].
Figure 3
Figure 3. Box-plots for four major bird-specific hindlimb indices.
Data are plotted for (A) hindlimb, (B) tibial, (C) tarsometarsus, and (D) pedal phalangeal indices for non-avian theropods and basal and extant birds. To reduce allometric influences, only non-avian theropod taxa less than 111 kg (mass of the largest bird in the sample) are plotted for all indexes except PPI. Outliers 1.5 times the standard deviation above or below the box are denoted by a circle, those 3 times by a star. Note the only taxon more than three times is the Chimney Swift for PPI. Note that Microraptor and Archaeopteryx are within the range of ground based and ground foraging birds. [planned for single column width].
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