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Mummified precocial bird wings in mid-Cretaceous Burmese amber

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      Abstract

      Our knowledge of Cretaceous plumage is limited by the fossil record itself: compression fossils surrounding skeletons lack the finest morphological details and seldom preserve visible traces of colour, while discoveries in amber have been disassociated from their source animals. Here we report the osteology, plumage and pterylosis of two exceptionally preserved theropod wings from Burmese amber, with vestiges of soft tissues. The extremely small size and osteological development of the wings, combined with their digit proportions, strongly suggests that the remains represent precocial hatchlings of enantiornithine birds. These specimens demonstrate that the plumage types associated with modern birds were present within single individuals of Enantiornithes by the Cenomanian (99 million years ago), providing insights into plumage arrangement and microstructure alongside immature skeletal remains. This finding brings new detail to our understanding of infrequently preserved juveniles, including the first concrete examples of follicles, feather tracts and apteria in Cretaceous avialans.

      Abstract

      The plumage of Cretaceous birds has previously been described only from compression fossils and isolated feathers in amber. Here, Xing et al. describe two 99 million year old bird wings found preserved in amber, enabling new insight into the evolution of feather arrangement, pigmentation, and structure.

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      Most cited references 18

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      Development and evolutionary origin of feathers.

       Richard Prum (1999)
      Avian feathers are a complex evolutionary novelty characterized by structural diversity and hierarchical development. Here, I propose a functionally neutral model of the origin and evolutionary diversification of bird feathers based on the hierarchical details of feather development. I propose that feathers originated with the evolution of the first feather follicle-a cylindrical epidermal invagination around the base of a dermal papilla. A transition series of follicle and feather morphologies is hypothesized to have evolved through a series of stages of increasing complexity in follicle structure and follicular developmental mechanisms. Follicular evolution proceeded with the origin of the undifferentiated collar (stage I), barb ridges (stage II), helical displacement of barb ridges, barbule plates, and the new barb locus (stage III), differentiation of pennulae of distal and proximal barbules (stage IV), and diversification of barbule structure and the new barb locus position (stage V). The model predicts that the first feather was an undifferentiated cylinder (stage I), which was followed by a tuft of unbranched barbs (stage II). Subsequently, with the origin of the rachis and barbules, the bipinnate feather evolved (stage III), followed then by the pennaceous feather with a closed vane (stage IV) and other structural diversity (stages Va-f). The model is used to evaluate the developmental plausibility of proposed functional theories of the origin of feathers. Early feathers (stages I, II) could have functioned in communication, defense, thermal insulation, or water repellency. Feathers could not have had an aerodynamic function until after bipinnate, closed pennaceous feathers (stage IV) had evolved. The morphology of the integumental structures of the coelurisaurian theropod dinosaurs Sinosauropteryx and Beipiaosaurus are congruent with the model's predictions of the form of early feathers (stage I or II). Additional research is required to examine whether these fossil integumental structures developed from follicles and are homologous with avian feathers. J. Exp. Zool. (Mol. Dev. Evol.) 285:291-306, 1999. Copyright 1999 Wiley-Liss, Inc.
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        A Jurassic ceratosaur from China helps clarify avian digital homologies.

        Theropods have traditionally been assumed to have lost manual digits from the lateral side inward, which differs from the bilateral reduction pattern seen in other tetrapod groups. This unusual reduction pattern is clearly present in basal theropods, and has also been inferred in non-avian tetanurans based on identification of their three digits as the medial ones of the hand (I-II-III). This contradicts the many developmental studies indicating II-III-IV identities for the three manual digits of the only extant tetanurans, the birds. Here we report a new basal ceratosaur from the Oxfordian stage of the Jurassic period of China (156-161 million years ago), representing the first known Asian ceratosaur and the only known beaked, herbivorous Jurassic theropod. Most significantly, this taxon possesses a strongly reduced manual digit I, documenting a complex pattern of digital reduction within the Theropoda. Comparisons among theropod hands show that the three manual digits of basal tetanurans are similar in many metacarpal features to digits II-III-IV, but in phalangeal features to digits I-II-III, of more basal theropods. Given II-III-IV identities in avians, the simplest interpretation is that these identities were shared by all tetanurans. The transition to tetanurans involved complex changes in the hand including a shift in digit identities, with ceratosaurs displaying an intermediate condition.
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          A juvenile coelurosaurian theropod from China indicates arboreal habits.

          Here we report an unequivocal arboreal coelurosaur, Epidendrosaurus ningchengensis gen. et sp. nov. This juvenile coelurosaur's third manual digit is extremely elongated, distinctively different from that of other known dinosaurs and birds. It represents certainly a type of adaptation previously unreported from the Mesozoic although the exact function of the third manual digit is unclear. The relatively long forelimb, penultimate phalanx of manual digit II, and pedal penultimate phalanges, are interpreted as evidence for the arboreal habit of Epidendrosaurus. Because Epidendrosaurus is more similar to advanced birds in some arboreal features than to Archaeopteryx, we suggest that the initial appearance of tree-adaptation in theropods was probably not directly related to flight but to other functions, such as seeking food or escaping from predators. Electronic Supplementary Material is available if you access this article at http://dx.doi.org/10.1007/s00114-002-0353-8. On that page (frame on the left side), a link takes you directly to the supplementary material.
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            Author and article information

            Affiliations
            [1 ]State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences , Beijing 100083, China
            [2 ]School of the Earth Sciences and Resources, China University of Geosciences , Beijing 100083, China
            [3 ]Palaeontology, Royal Saskatchewan Museum , Regina, Saskatchewan, Canada S4P 2V7
            [4 ]Biology Department, University of Regina , Regina, Saskatchewan, Canada S4S 0A2
            [5 ]Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences , Beijing 100044, China
            [6 ]Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences , Beijing 100101, China
            [7 ]School of Earth Sciences, University of Bristol , Bristol BS8 1RJ, UK
            [8 ]Institute of Geology and Paleontology, Linyi University , Linyi 276000, China
            [9 ]Department of Exercise and Health Science, University of Taipei , Taipei 11153, China
            [10 ]Dinosaur Tracks Museum, University of Colorado Denver , Denver, Colorado 80217, USA
            [11 ]Institute of High Energy Physics, Chinese Academy of Science , Beijing 100049, China
            [12 ]P.O. Box 4680, Chongqing 400015, China
            Author notes
            [*]

            These authors contributed equally to this work.

            Journal
            Nat Commun
            Nat Commun
            Nature Communications
            Nature Publishing Group
            2041-1723
            28 June 2016
            2016
            : 7
            27352215
            4931330
            ncomms12089
            10.1038/ncomms12089
            Copyright © 2016, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.

            This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

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