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      Reconsidering the Avian Nature of the Oviraptorosaur Brain (Dinosauria: Theropoda)

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      PLoS ONE
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          Abstract

          The high degree of encephalization characterizing modern birds is the product of a long evolutionary history, our understanding of which is still largely in its infancy. Here we provide a redescription of the endocranial space of the oviraptorosaurian dinosaur Conchoraptor gracilis with the goal of assessing the hypothesis that it shares uniquely derived endocranial characters with crown-group avians. The existence of such features has implications for the transformational history of avian neuroanatomy and suggests that the oviraptorosaur radiation is a product of the immediate stem lineage of birds—after the divergence of Archaeopteryx lithographica. Results derived from an expanded comparative sample indicate that the strong endocranial similarity between Conchoraptor and modern birds largely reflects shared conservation of plesiomorphic features. The few characters that are maintained as being uniquely expressed in these two taxa are more likely products of convergence than homology but still indicate that the oviraptorosaur endocranial cavity has much to teach us about the complex history of avian brain evolution.

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          Neuroanatomy of flying reptiles and implications for flight, posture and behaviour.

          Comparison of birds and pterosaurs, the two archosaurian flyers, sheds light on adaptation to an aerial lifestyle. The neurological basis of control holds particular interest in that flight demands on sensory integration, equilibrium, and muscular coordination are acute. Here we compare the brain and vestibular apparatus in two pterosaurs based on high-resolution computed tomographic (CT) scans from which we constructed digital endocasts. Although general neural organization resembles birds, pterosaurs had smaller brains relative to body mass than do birds. This difference probably has more to do with phylogeny than flight, in that birds evolved from nonavian theropods that had already established trends for greater encephalization. Orientation of the osseous labyrinth relative to the long axis of the skull was different in these two pterosaur species, suggesting very different head postures and reflecting differing behaviours. Their enlarged semicircular canals reflect a highly refined organ of equilibrium, which is concordant with pterosaurs being visually based, aerial predators. Their enormous cerebellar floccular lobes may suggest neural integration of extensive sensory information from the wing, further enhancing eye- and neck-based reflex mechanisms for stabilizing gaze.
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            An Archaeopteryx-like theropod from China and the origin of Avialae.

            Archaeopteryx is widely accepted as being the most basal bird, and accordingly it is regarded as central to understanding avialan origins; however, recent discoveries of derived maniraptorans have weakened the avialan status of Archaeopteryx. Here we report a new Archaeopteryx-like theropod from China. This find further demonstrates that many features formerly regarded as being diagnostic of Avialae, including long and robust forelimbs, actually characterize the more inclusive group Paraves (composed of the avialans and the deinonychosaurs). Notably, adding the new taxon into a comprehensive phylogenetic analysis shifts Archaeopteryx to the Deinonychosauria. Despite only tentative statistical support, this result challenges the centrality of Archaeopteryx in the transition to birds. If this new phylogenetic hypothesis can be confirmed by further investigation, current assumptions regarding the avialan ancestral condition will need to be re-evaluated.
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              Birds have paedomorphic dinosaur skulls.

              The interplay of evolution and development has been at the heart of evolutionary theory for more than a century. Heterochrony—change in the timing or rate of developmental events—has been implicated in the evolution of major vertebrate lineages such as mammals, including humans. Birds are the most speciose land vertebrates, with more than 10,000 living species representing a bewildering array of ecologies. Their anatomy is radically different from that of other vertebrates. The unique bird skull houses two highly specialized systems: the sophisticated visual and neuromuscular coordination system allows flight coordination and exploitation of diverse visual landscapes, and the astonishing variations of the beak enable a wide range of avian lifestyles. Here we use a geometric morphometric approach integrating developmental, neontological and palaeontological data to show that the heterochronic process of paedomorphosis, by which descendants resemble the juveniles of their ancestors, is responsible for several major evolutionary transitions in the origin of birds. We analysed the variability of a series of landmarks on all known theropod dinosaur skull ontogenies as well as outgroups and birds. The first dimension of variability captured ontogeny, indicating a conserved ontogenetic trajectory. The second dimension accounted for phylogenetic change towards more bird-like dinosaurs. Basally branching eumaniraptorans and avialans clustered with embryos of other archosaurs, indicating paedomorphosis. Our results reveal at least four paedomorphic episodes in the history of birds combined with localized peramorphosis (development beyond the adult state of ancestors) in the beak. Paedomorphic enlargement of the eyes and associated brain regions parallels the enlargement of the nasal cavity and olfactory brain in mammals. This study can be a model for investigations of heterochrony in evolutionary transitions, illuminating the origin of adaptive features and inspiring studies of developmental mechanisms.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                10 December 2014
                : 9
                : 12
                : e113559
                Affiliations
                [1 ]Stony Brook University, Department of Anatomical Sciences, Stony Brook, New York, United States of America
                [2 ]New York Institute of Technology, College of Osteopathic Medicine, Department of Anatomy, Northern Boulevard, Old Westbury, New York, United States of America
                [3 ]American Museum of Natural History, Division of Paleontology, Central Park West at 79 th Street, New York, New York, United States of America
                University of Lethbridge, Canada
                Author notes

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

                Conceived and designed the experiments: AMB GSB MAN. Performed the experiments: AMB. Analyzed the data: AMB GSB MAN. Contributed reagents/materials/analysis tools: MAN. Wrote the paper: AMB GSB MAN.

                Article
                PONE-D-14-22126
                10.1371/journal.pone.0113559
                4262302
                25494183
                177a7b09-97ed-46bc-bc97-b59e64451640
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 18 May 2014
                : 25 October 2014
                Page count
                Pages: 15
                Funding
                Funding for this project was provided by an NSF Dissertation Improvement Grant (NSF DEB-0909970) to AMB and MAN and a travel award from Columbia University to AMB. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Evolutionary Biology
                Neuroscience
                Paleoneurology
                Paleontology
                Paleobiology
                Paleozoology
                Vertebrate Paleontology
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction. Quantitative data for the plot of body size v. endocranial volume are available in the supplementary materials of Balanoff et al. (2013) Evolutionary Origins of the Avian Brain. Nature 501: 93-96.

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