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Research Article

Origin of the avian predentary and evidence of a unique form of cranial kinesis in Cretaceous ornithuromorphs

View ORCID ProfileAlida M. Bailleul, Zhiheng Li, Jingmai O’Connor, and Zhonghe Zhou
PNAS December 3, 2019 116 (49) 24696-24706; first published November 18, 2019 https://doi.org/10.1073/pnas.1911820116
Alida M. Bailleul
aKey Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, 100044 Beijing, China;
bCenter for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, 100044 Beijing, China
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  • ORCID record for Alida M. Bailleul
  • For correspondence: alida.bailleul@ivpp.ac.cn zhouzhonghe@ivpp.ac.cn
Zhiheng Li
aKey Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, 100044 Beijing, China;
bCenter for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, 100044 Beijing, China
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Jingmai O’Connor
aKey Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, 100044 Beijing, China;
bCenter for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, 100044 Beijing, China
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Zhonghe Zhou
aKey Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, 100044 Beijing, China;
bCenter for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, 100044 Beijing, China
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  • For correspondence: alida.bailleul@ivpp.ac.cn zhouzhonghe@ivpp.ac.cn
  1. Contributed by Zhonghe Zhou, October 14, 2019 (sent for review July 11, 2019; reviewed by Anthony Herrel and Adam K. Huttenlocker)

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Significance

The avian predentary is a small, rarely preserved skeletal structure found only in toothed Mesozoic ornithuromorph birds. The origin and function of this enigmatic bone is poorly understood. Based on skeletal tissue identification in a specimen of the Early Cretaceous Yanornis martini, we propose developmental, structural, and functional hypotheses for this element. It consists of trabecular bone with a caudal articular surface for the dentary covered by cartilage. Tissue mechanobiology suggests this contact was kinetic, representing a previously unknown type of avian cranial kinesis. We hypothesize that the avian predentary was a biomechanically induced sesamoid that coevolved with an edentulous portion of the premaxilla, together representing a successful morphotype that combined a small beak with a proprioceptive system.

Abstract

The avian predentary is a small skeletal structure located rostral to the paired dentaries found only in Mesozoic ornithuromorphs. The evolution and function of this enigmatic element is unknown. Skeletal tissues forming the predentary and the lower jaws in the basal ornithuromorph Yanornis martini are identified using computed-tomography, scanning electron microscopy, and histology. On the basis of these data, we propose hypotheses for the development, structure, and function of this element. The predentary is composed of trabecular bone. The convex caudal surface articulates with rostromedial concavities on the dentaries. These articular surfaces are covered by cartilage, which on the dentaries is divided into 3 discrete patches: 1 rostral articular cartilage and 2 symphyseal cartilages. The mechanobiology of avian cartilage suggests both compression and kinesis were present at the predentary–dentary joint, therefore suggesting a yet unknown form of avian cranial kinesis. Ontogenetic processes of skeletal formation occurring within extant taxa do not suggest the predentary originates within the dentaries, nor Meckel’s cartilage. We hypothesize that the predentary is a biomechanically induced sesamoid that arose within the soft connective tissues located rostral to the dentaries. The mandibular canal hosting the alveolar nerve suggests that the dentary teeth and predentary of Yanornis were proprioceptive. This whole system may have increased foraging efficiency. The Mesozoic avian predentary apparently coevolved with an edentulous portion of the premaxilla, representing a unique kinetic morphotype that combined teeth with a small functional beak and persisted successfully for ∼60 million years.

  • predentary
  • birds
  • sesamoid
  • kinesis
  • proprioception

Footnotes

  • ↵1To whom correspondence may be addressed. Email: alida.bailleul{at}ivpp.ac.cn or zhouzhonghe{at}ivpp.ac.cn.
  • Author contributions: A.M.B., Z.L., J.O., and Z.Z. designed research; A.M.B., Z.L., J.O., and Z.Z. performed research; Z.Z. contributed new reagents/analytic tools; A.M.B. and Z.L. collected the data; A.M.B., Z.L., J.O., and Z.Z. analyzed data; and A.M.B. and J.O. wrote the paper.

  • Reviewers: A.H., Muséum National d’Histoire Naturelle; and A.K.H., University of Southern California.

  • The authors declare no competing interest.

  • Data deposition: We have deposited large computed tomography data in the Open Science Framework, OSF, https://osf.io/q9xsp/.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1911820116/-/DCSupplemental.

Published under the PNAS license.

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Origin of the avian predentary and evidence of a unique form of cranial kinesis in Cretaceous ornithuromorphs
Alida M. Bailleul, Zhiheng Li, Jingmai O’Connor, Zhonghe Zhou
Proceedings of the National Academy of Sciences Dec 2019, 116 (49) 24696-24706; DOI: 10.1073/pnas.1911820116

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Origin of the avian predentary and evidence of a unique form of cranial kinesis in Cretaceous ornithuromorphs
Alida M. Bailleul, Zhiheng Li, Jingmai O’Connor, Zhonghe Zhou
Proceedings of the National Academy of Sciences Dec 2019, 116 (49) 24696-24706; DOI: 10.1073/pnas.1911820116
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