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Fossil evidence of the avian vocal organ from the Mesozoic

Abstract

From complex songs to simple honks, birds produce sounds using a unique vocal organ called the syrinx1,2. Located close to the heart at the tracheobronchial junction, vocal folds or membranes attached to modified mineralized rings vibrate to produce sound1,2,3,4,5,6,7. Syringeal components were not thought to commonly enter the fossil record6, and the few reported fossilized parts of the syrinx are geologically young8,9,10,11 (from the Pleistocene and Holocene (approximately 2.5 million years ago to the present)). The only known older syrinx is an Eocene specimen that was not described or illustrated12. Data on the relationship between soft tissue structures and syringeal three-dimensional geometry are also exceptionally limited5. Here we describe the first remains, to our knowledge, of a fossil syrinx from the Mesozoic Era, which are preserved in three dimensions in a specimen from the Late Cretaceous (approximately 66 to 69 million years ago) of Antarctica. With both cranial and postcranial remains, the new Vegavis iaai specimen is the most complete to be recovered from a part of the radiation of living birds (Aves). Enhanced-contrast X-ray computed tomography (CT) of syrinx structure in twelve extant non-passerine birds, as well as CT imaging of the Vegavis and Eocene syrinxes, informs both the reconstruction of ancestral states in birds and properties of the vocal organ in the extinct species. Fused rings in Vegavis form a well-mineralized pessulus, a derived neognath bird feature, proposed to anchor enlarged vocal folds or labia5. Left-right bronchial asymmetry, as seen in Vegavis, is only known in extant birds with two sets of vocal fold sound sources. The new data show the fossilization potential of the avian vocal organ and beg the question why these remains have not been found in other dinosaurs. The lack of other Mesozoic tracheobronchial remains, and the poorly mineralized condition in archosaurian taxa without a syrinx, may indicate that a complex syrinx was a late arising feature in the evolution of birds, well after the origin of flight and respiratory innovations.

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Figure 1: The Vegavis iaai specimen showing the location of the syrinx.
Figure 2: Syrinx elements in Vegavis iaai (MACN-PV 19.748) from X-ray computed tomography data.
Figure 3: Comparison of the Cretaceous Vegavis and Eocene Presbyornis syrinxes to extant avian exemplars showing the optimization of major traits present in the fossil and arising during the origin of living birds.

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Acknowledgements

This project was funded by the Gordon and Betty Moore Foundation (grant GBMF4498; J.A.C., T.R. and F.G.), as well as the National Science Foundation (OPP ANT-1141820, OPP 0927341 and EAR 1355292; J.A.C.), C. Burke and the Agencia Nacional de Promoción Científica y Técnica (PICT 2010-066; F.E.N). The Instituto Antártico Argentino (IAA), G. M. Robles, W. J. Zinsmeister and especially C. A. Rinaldi, E. B. Olivero, and the Fuerza Aérea Argentina provided key support for fieldwork in 1993.

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Authors

Contributions

D.R.M. and F.J.M. collected the fossil specimen and contributed geological data. M.P.I. and S.C. contributed to the fossil specimen preparation and study. T.R., F.G., Z.L. and J.A.C. designed the study of the syrinx and collected primary data. Z.L. designed the enhanced contrast CT protocol and collected extant CT data. J.A.C. discovered the fossil syrinx remains and designed the project with F.E.N., S.C., T.R. and F.G. J.A.C., Z.L., F.A., F.E.N., T.R., F.G. and S.C. conducted morphological study of the specimen.

Corresponding author

Correspondence to Julia A. Clarke.

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The authors declare no competing financial interests.

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Nature thanks P. O’Connor and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Extended data figures and tables

Extended Data Figure 1 Photographs of elements from the new Vegavis iaai specimen from Vega Island, Antarctica (MACN-PV 19.748) prepared from the primary block.

ad, Coracoid(a), caudal vertebra (b), (from top to bottom) distal radius, ulna with radiale in articulation, radiale and ulnare, and manual phalanx III:1 (c), pedal phalanx (d), scapula (e), femur (f), tibiotarsus (g). Scale bar, 1 cm.

Extended Data Figure 2 Images from X-ray computed tomography of selected elements of the new Vegavis iaai specimen (MACN-PV 19.748).

a, Coracoid (acr, acrocoracoid; gl, glenoid facet; pp, procoracoid process; scc, scapular cotyla). b, Proximal tibia (cnc, cranial cnemial crest). c, Pterygoid (bpt, basipterygoid articular facet; pat, palatine articular facet; qut, quadrate articular facet). d, Fibula (fi). e, Radialae and ulnare. f, Caudal mandible. g, Proximal humerus (dep, depression; dc, deltopectoral crest; ci, captal incisure; fo, fossa). h, Femur (os, ovoid scar). Scale bar, 1 cm.

Extended Data Figure 3 Polarornis gregorii holotype specimen from Seymour Island, Antarctic Peninsula.

The specimen was damaged during original preparation and the existence of the previously described braincase and quadrate as well as morphologies from the skull and tibial shaft cannot be confirmed.

Extended Data Figure 4 Comparison of elements in common between the Polarornis gregorii holotype specimen from Seymour Island (top) and the new specimen of Vegavis iaai (MACN-PV 19.748) (bottom).

a, b, Tibiotarsus (a) and femur (b). The asterisk indicates the prominent muscular ridge on the femur present in the Vegavis iaai holotype and the newly referred specimen (MACN-PV 19.748), but not seen in the Polarornis holotype. Scale bar, 1 cm.

Extended Data Figure 5 Comparison of select elements in common between the Vegavis iaai holotype and the new specimen (MACN-PV 19.748).

Top, the circular depression on the proximal femur used in the diagnosis of Vegavis seen in the new specimen18. Bottom, the humeral crest (lateral to the capital ridge) also mentioned in that diagnosis of Vegavis iaai are shown. Although both of these characters show a complex distribution in Aves, and are not restricted to the species, their combination is unique.

Extended Data Figure 6 The pterygoid in Vegavis iaai specimen MACN-PV 19.748 (right) compared to that of Gavia immer (left) highlighting the prominent basipterygoid facet in the Vegavis iaai referred specimen.

See also Fig. 1, Extended Data Fig. 2 and Supplementary Information. Scale bar, 1 cm.

Extended Data Figure 7 Vegavis iaai (MACN-PV 19.748) syrinx with position-based identities labelled.

See also Fig. 2 and Supplementary Table 3.

Extended Data Figure 8 Morphological comparison of the syrinx in the fossils and enhanced contrast CT images of avian and outgroup exemplars. Key features discussed in the text are illustrated.

The numbers (−1, 0, 1) reference the position schema described in the main text, Supplementary Information, Supplementary Tables 3 and 4, Extended Data Fig. 7. Enlarged images are available at http://www.jsg.utexas.edu/syrinx-evolution/ and this image website is also available at Data Dryad as a zipped file at http://dx.doi.org/10.5061/dryad.50n8j.

Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary Tables 1-4 and additional references. (PDF 702 kb)

Supplementary Figures

This file contains Supplementary Figures 1-2. (PDF 262 kb)

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Clarke, J., Chatterjee, S., Li, Z. et al. Fossil evidence of the avian vocal organ from the Mesozoic. Nature 538, 502–505 (2016). https://doi.org/10.1038/nature19852

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