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Fossil Evidence of the Avian Vocal Organ from the Mesozoic (PDF) LETTER doi:10.1038/nature19852 Fossil evidence of the avian vocal organ from the Mesozoic Julia A. Clarke1, Sankar Chatterjee2, Zhiheng Li1,3, Tobias Riede4, Federico Agnolin5,6, Franz Goller7, Marcelo P. Isasi5, Daniel R. Martinioni8, Francisco J. Mussel9 & Fernando E. Novas5 From complex songs to simple honks, birds produce sounds using a laryngeal sound source in frogs, reptiles or mammals, data from the unique vocal organ called the syrinx1,2. Located close to the heart at hyoid skeleton, skull and vertebral column have been proposed to the tracheobronchial junction, vocal folds or membranes attached to inform evolutionary changes in its position in hominoids16 and in modified mineralized rings vibrate to produce sound1–7. Syringeal bats17. However, neither direct fossil evidence nor indirect inferential components were not thought to commonly enter the fossil record6, approaches have so far been used to inform our understanding of the and the few reported fossilized parts of the syrinx are geologically origin of the syrinx. young8–11 (from the Pleistocene and Holocene (approximately 2.5 A three-dimensionally preserved syrinx in a partial skeleton of a million years ago to the present)). The only known older syrinx is Late Cretaceous fossil bird from Vega Island, Antarctic Peninsula an Eocene specimen that was not described or illustrated12. Data (MACN-PV 19.748 (MACN-Museo Argentino de Ciencias Naturales), on the relationship between soft tissue structures and syringeal Figs 1 and 2, Extended Data Figs 1, 2, 4–8, Supplementary Information, three-dimensional geometry are also exceptionally limited5. Here Supplementary Table 1 and Supplementary Fig. 1), is here referred to we describe the first remains, to our knowledge, of a fossil syrinx the species Vegavis iaai18 (Supplementary Information, Extended Data from the Mesozoic Era, which are preserved in three dimensions Figs 4 and 6). X-ray computed tomography (CT) was used to digitally in a specimen from the Late Cretaceous (approximately 66 to 69 extract syrinx remains from this fossil, as well as from the previously million years ago) of Antarctica. With both cranial and postcranial reported Eocene fossil anseriform specimen (Presbyornis sp12; USNM remains, the new Vegavis iaai specimen is the most complete to PAL 617185; (USNM-United States National Museum) Fig. 3, Extended be recovered from a part of the radiation of living birds (Aves). Data Fig. 8, Supplementary Table 4 and Supplementary Fig. 2). Enhanced-contrast X-ray computed tomography (CT) of syrinx Iodine-enhanced contrast CT (diceCT)19 data was acquired for 12 structure in twelve extant non-passerine birds, as well as CT imaging extant birds and one outgroup exemplar (Fig. 3, Extended Data Fig. 8, of the Vegavis and Eocene syrinxes, informs both the reconstruction Supplementary Information, Supplementary Tables 1 and 4) to inform of ancestral states in birds and properties of the vocal organ in the the placement of three displaced portions of the syrinx and inference of extinct species. Fused rings in Vegavis form a well-mineralized the location of sound-generating tissues (membranes or labia). These pessulus, a derived neognath bird feature, proposed to anchor data provide insight into the three-dimensional geometry of the syrinx enlarged vocal folds or labia5. Left-right bronchial asymmetry, as and the relationship between the structure of the mineralized rings seen in Vegavis, is only known in extant birds with two sets of vocal and soft tissue20. fold sound sources. The new data show the fossilization potential Nine elements of the mineralized rings of the syrinx in MACN-PV of the avian vocal organ and beg the question why these remains 19.748 are preserved adjacent to the cranial-most thoracic vertebrae, have not been found in other dinosaurs. The lack of other Mesozoic close to their position in life (Fig. 2a, b, coloured elements I–IX). Three tracheobronchial remains, and the poorly mineralized condition of these elements were preserved in articulation, whereas the remaining in archosaurian taxa without a syrinx, may indicate that a complex elements lay on either side of the thoracic vertebrae (Fig. 2b). Three syrinx was a late arising feature in the evolution of birds, well after are clearly bronchial elements (Fig. 2b elements V–VII, Extended Data the origin of flight and respiratory innovations. Fig. 7 and Supplementary Table 3). They are half rings, two of which In the mid-nineteenth century, T. H. Huxley named the unique vocal have slightly expanded ventral tips (Fig. 2c, Extended Data Fig. 7 and organ in birds as the syrinx1. He also recognized that birds were most Supplementary Fig. 1). The reduction of the medial aspect of bronchial closely related to dinosaurs. However, neither he nor most subsequent rings is the most consistent feature of an avian syrinx; in outgroup authors that studied the syrinx2–4 addressed its origin, early evolution archosaurs and other saurians, these rings are typically complete. or probable ancestral states. More recently, it was noted that given the Bronchial half rings in all extant Aves support a membranous medial distribution of the syrinx in living birds, it was possibly ancestral to bronchial wall or medial tympaniform membrane that contributes to the crown clade Aves6. The few hypotheses about non-avian dinosaur sound production21. In contrast to a rigid cartilaginous wall, a pliable vocal behaviour have focused on the possibility of a larynx-based medial bronchial non-muscular wall consisting of soft connective tissue sound source, the outgroup condition present in other tetrapods13, or and epithelium facilitates not only airflow-induced tissue vibration for speculated that most—those lacking an interclavicular air sac—might sound production, but also tissue adduction through the development have been mute13. Others did not focus on the sound source (larynx of a transmembraneous pressure differential. or syrinx), but on possible resonating chambers in the skull of some The spacing, shape and position of the tracheal and bronchial half- ornithischian dinosaurs14,15. Although there are also no fossils of the rings provides a good proxy for the location of the sound-generating 1Department of Geological Sciences, University of Texas at Austin, Austin, Texas 78756, USA. 2Museum of Texas Tech University, Box 43191, Lubbock, Texas 79409, USA. 3Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China. 4Department of Physiology, Midwestern University, 19555 N 59th Avenue, Glendale, Arizona 85308, USA. 5Conicet — Laboratorio de Anatomía Comparada y Evolución de los Vertebrados, Museo Argentino de Ciencias Naturales, Av. Ángel Gallardo 470, C1405DJR Buenos Aires, Argentina. 6Fundación de Historia Natural “Félix de Azara”, Universidad Maimónides, Hidalgo 775, C1405BDB Buenos Aires, Argentina. 7Department of Biology, University of Utah, 257 South 1400 East, Salt Lake City, Utah 84112, USA. 8Laboratorio de Geologia Andina, CADIC-Conicet, B.Houssay 200, CP V9410CAB Ushuaia, Tierra del Fuego, Argentina. 9Departamento de Ciencias Geológicas, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Autónoma de Buenos Aires, CP C1405DJR Buenos Aires, Argentina. 00 MONTH 2016 | VOL 000 | NATURE | 1 © 2016 Macmillan Publishers Limited, part of Springer Nature. All rights reserved. RESEARCH LETTER a b c d Figure 1 | The Vegavis iaai specimen showing the location of the syrinx. a–g, MACN-PV cm 19.748 (photographs (b, c, f, g) and X-ray computed tomography imaging (a, d, e, h)) cv pa pa comprises a pterygoid (pt), syrinx, the cervical (cv) and thoracic (tv) series and part of the caudal (cav) series, as well as the coracoid (co), hy? cav scapula (s), furcula (fu), carpometacarpus phII-2 f (cm), manual phalanges II:1 and II:2 in ri articulation (phII-2), femur (f), patella (pa), 1 cm pph pedal phalanges (pph), ribs (ri) and (hy?) a possible ceratobranchial element from the pt pt hyoid. Additional elements were prepared e f fu g h co co from the primary blocks (for example, caudal co mandible, coracoid, humerus, ulna, radius, radiale, ulnare, femur, tibiotarsus and fibula; see Supplementary Methods and Extended Data Syrinx Figs 1 and 2). tv tv s 1 cm tissues (labia or membranes)5. In the Vegavis syrinx, the sound produc- involved in sound production. One end of the paired bronchial ing tissues are just caudal to the tracheobronchial juncture (between half-rings is expanded and slightly bulbous (elements V–VII); this positions 0 and − 1 or positions − 1 and − 2 in Fig. 2c, Supplementary expansion is also seen in many neognath taxa with paired labia4,5 Table 3). Given the irregular shape of the preserved half-rings and their articulations, a sound source located deeper in the bronchi is highly unlikely. In extant galloanserines and Presbyornis, these tissues are a II–IV V 1 cm typically just below the tracheobronchial juncture (between position − 1 and − 2; Fig. 3, Extended Data Fig. 8, Supplementary Fig. 2 and co Supplementary Table 4). By contrast, in Gaviidae and Procellariformes, VI these tissues are located well below the juncture between positions − 3 tv and − 4 (Extended Data Fig. 8 and Supplementary Table 4). Whether this condition is more widespread in Neoaves, and possibly phyloge- netically informative, awaits denser taxon sampling. There is also b I no marked shift in diameter across the tracheobronchial juncture in VII Vegavis, although one is seen in these sampled neoavian taxa (Fig. 3 I and Extended Data Figs 7 and 8). IX c VIII IX VIII Vegavis has a distinct pessulus, a robust, ossified midline structure VII I II where the bronchial airways meet the trachea, thought by some to be 1 cm III IV 5 V key to anchoring larger vocal membranes or labia (Fig. 2 element III; VI VII Supplementary Table 3 and Supplementary Fig. 1). A well-mineralized LTM Asymmetry pessulus is here identified as a derived feature of Neognathae (Fig.
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