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      Fossilized skin reveals coevolution with feathers and metabolism in feathered dinosaurs and early birds

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          Abstract

          Feathers are remarkable evolutionary innovations that are associated with complex adaptations of the skin in modern birds. Fossilised feathers in non-avian dinosaurs and basal birds provide insights into feather evolution, but how associated integumentary adaptations evolved is unclear. Here we report the discovery of fossil skin, preserved with remarkable nanoscale fidelity, in three non-avian maniraptoran dinosaurs and a basal bird from the Cretaceous Jehol biota (China). The skin comprises patches of desquamating epidermal corneocytes that preserve a cytoskeletal array of helically coiled α-keratin tonofibrils. This structure confirms that basal birds and non-avian dinosaurs shed small epidermal flakes as in modern mammals and birds, but structural differences imply that these Cretaceous taxa had lower body heat production than modern birds. Feathered epidermis acquired many, but not all, anatomically modern attributes close to the base of the Maniraptora by the Middle Jurassic.

          Abstract

          In addition to the evolutionary innovation of feathers, bird skin has complex adaptations. Here, McNamara and colleagues examine exceptionally preserved skin from feathered dinosaurs and ancient birds from the Cretaceous and show the early acquisition of many skin attributes seen in modern species.

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          The cornified envelope: a model of cell death in the skin.

          The epidermis functions as a barrier against the environment by means of several layers of terminally differentiated, dead keratinocytes - the cornified layer, which forms the endpoint of epidermal differentiation and death. The cornified envelope replaces the plasma membrane of differentiating keratinocytes and consists of keratins that are enclosed within an insoluble amalgam of proteins, which are crosslinked by transglutaminases and surrounded by a lipid envelope. New insights into the molecular mechanisms and the physiological endpoints of cornification are increasing our understanding of the pathological defects of this unique form of programmed cell death, which is associated with barrier malfunctions and ichthyosis.
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            An integrative approach to understanding bird origins.

            Recent discoveries of spectacular dinosaur fossils overwhelmingly support the hypothesis that birds are descended from maniraptoran theropod dinosaurs, and furthermore, demonstrate that distinctive bird characteristics such as feathers, flight, endothermic physiology, unique strategies for reproduction and growth, and a novel pulmonary system originated among Mesozoic terrestrial dinosaurs. The transition from ground-living to flight-capable theropod dinosaurs now probably represents one of the best-documented major evolutionary transitions in life history. Recent studies in developmental biology and other disciplines provide additional insights into how bird characteristics originated and evolved. The iconic features of extant birds for the most part evolved in a gradual and stepwise fashion throughout archosaur evolution. However, new data also highlight occasional bursts of morphological novelty at certain stages particularly close to the origin of birds and an unavoidable complex, mosaic evolutionary distribution of major bird characteristics on the theropod tree. Research into bird origins provides a premier example of how paleontological and neontological data can interact to reveal the complexity of major innovations, to answer key evolutionary questions, and to lead to new research directions. A better understanding of bird origins requires multifaceted and integrative approaches, yet fossils necessarily provide the final test of any evolutionary model.
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              Leanchoilia guts and the interpretation of three-dimensional structures in Burgess Shale-type fossils

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                Author and article information

                Contributors
                maria.mcnamara@ucc.ie
                zhangfucheng@lyu.edu.cn
                xu.xing@ivpp.ac.cn
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                25 May 2018
                25 May 2018
                2018
                : 9
                : 2072
                Affiliations
                [1 ]ISNI 0000000123318773, GRID grid.7872.a, School of Biological, Earth and Environmental Sciences, , University College Cork, ; North Mall, Cork, T23 TK30 Ireland
                [2 ]ISNI 0000 0004 1763 3680, GRID grid.410747.1, Institute of Geology and Paleontology, , Linyi University, ; Shuangling Road, Linyi City, Shandong 276005 China
                [3 ]ISNI 0000 0004 1936 7603, GRID grid.5337.2, School of Earth Sciences, , University of Bristol, ; Queen’s Road, Bristol, BS8 1RJ UK
                [4 ]ISNI 0000 0001 0768 2743, GRID grid.7886.1, UCD School of Earth Sciences, , University College Dublin, ; Dublin, D04 N2E5 Ireland
                [5 ]ISNI 0000000123318773, GRID grid.7872.a, Department of Anatomy and Neuroscience, , University College Cork, ; Western Road, Cork, T12 XF62 Ireland
                [6 ]ISNI 0000 0001 2171 1133, GRID grid.4868.2, School of Biological and Chemical Sciences, , Queen Mary University of London, ; Mile End Rd., London, E1 4NS UK
                [7 ]ISNI 0000000096069301, GRID grid.10837.3d, School of Physical Sciences, , The Open University, ; Walton Hall, Milton Keynes, MK7 6AA UK
                [8 ]ISNI 0000 0000 9404 3263, GRID grid.458456.e, Institute of Vertebrate Paleontology and Paleoanthropology, ; 142 Xizhimenwai St., 100044 Beijing, China
                Author information
                http://orcid.org/0000-0003-0968-4624
                http://orcid.org/0000-0002-4045-8265
                http://orcid.org/0000-0002-4323-1824
                Article
                4443
                10.1038/s41467-018-04443-x
                5970262
                29802246
                b6314b06-3c6b-43d3-a684-8d365ac9fa43
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 30 November 2017
                : 23 April 2018
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