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Complete Ichthyornis skull illuminates mosaic assembly of the avian head

Abstract

The skull of living birds is greatly modified from the condition found in their dinosaurian antecedents. Bird skulls have an enlarged, toothless premaxillary beak and an intricate kinetic system that includes a mobile palate and jaw suspensorium. The expanded avian neurocranium protects an enlarged brain and is flanked by reduced jaw adductor muscles. However, the order of appearance of these features and the nature of their earliest manifestations remain unknown. The Late Cretaceous toothed bird Ichthyornis dispar sits in a pivotal phylogenetic position outside living groups: it is close to the extant avian radiation but retains numerous ancestral characters1,2,3. Although its evolutionary importance continues to be affirmed3,4,5,6,7,8, no substantial new cranial material of I. dispar has been described beyond incomplete remains recovered in the 1870s. Jurassic and Cretaceous Lagerstätten have yielded important avialan fossils, but their skulls are typically crushed and distorted9. Here we report four three-dimensionally preserved specimens of I. dispar—including an unusually complete skull—as well as two previously overlooked elements from the Yale Peabody Museum holotype, YPM 1450. We used these specimens to generate a nearly complete three-dimensional reconstruction of the I. dispar skull using high-resolution computed tomography. Our study reveals that I. dispar had a transitional beak—small, lacking a palatal shelf and restricted to the tips of the jaws—coupled with a kinetic system similar to that of living birds. The feeding apparatus of extant birds therefore evolved earlier than previously thought and its components were functionally and developmentally coordinated. The brain was relatively modern, but the temporal region was unexpectedly dinosaurian: it retained a large adductor chamber bounded dorsally by substantial bony remnants of the ancestral reptilian upper temporal fenestra. This combination of features documents that important attributes of the avian brain and palate evolved before the reduction of jaw musculature and the full transformation of the beak.

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Fig. 1: Full 3D reconstruction of the skull of I. dispar.
Fig. 2: Line drawings of the skull of I. dispar.
Fig. 3: Relationships of I. dispar and the origin of the avian beak.
Fig. 4: Derived brain shape and primitive temporal region of I. dispar.

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Acknowledgements

We thank M. Colbert, J. Maisano and the staff of the UTCT facility at The University of Texas at Austin, as well as G. Lin at the Harvard Center for Nanoscale Systems and A. Pritchard at Yale for CT scanning assistance. K. Zyskowski and G. Watkins-Colwell in the Division of Vertebrate Zoology at YPM assisted with extant comparative material. M. Fox, C. Norris and D. Brinkman facilitated the examination and scanning of YPM fossil material. This research was supported by Yale University, the Yale Peabody Museum of Natural History, the University of Bath, National Science Foundation Doctoral Dissertation Improvement Grant DEB 1500798, the Alexander Wetmore Memorial Research Award (American Ornithologists’ Union), a Yale Institute for Biospheric Studies Dissertation Improvement Grant, the Stephen J. Gould Award (Paleontological Society), an Evolving Earth Foundation Research Grant and a Frank M. Chapman Ornithological Research Grant (American Museum of Natural History).

Reviewer information

Nature thanks Z. Zhou and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author information

Authors and Affiliations

Authors

Contributions

D.J.F. and B.-A.S.B. conceived and directed the study and arranged logistics of specimen preparation and CT scanning. K.S. discovered the FHSM specimen and donated it to the museum. D.J.F., M.H. and B.-A.S.B. performed CT scans and processed CT data and M.H. assembled the skull reconstruction. M.H., D.J.F. and B.-A.S.B. scored characters and performed phylogenetic analyses. B.-A.S.B. and M.H. planned the main-text figures. M.H. and D.J.F. prepared the figures. D.J.F. wrote the supplementary anatomical descriptions and rendered the Supplementary Videos. D.B., L.E.W., K.S., D.E. and J.A.E. collected and prepared specimens for study, analysed morphology and edited the paper. B.-A.S.B., D.J.F. and M.H. wrote the paper. B.-A.S.B. and D.J.F. acquired funding.

Corresponding author

Correspondence to Bhart-Anjan S. Bhullar.

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Extended data figures and tables

Extended Data Fig. 1 Full 3D reconstruction of the skull of I. dispar in high resolution.

This is the same reconstruction as shown in Fig. 1, reproduced at a higher resolution to show details.

Extended Data Fig. 2 Reconstruction of the skull of I. dispar.

Material described in this paper is indicated in gold and previously described regions are indicated in grey. All elements are scaled to the size of the  FHSM VP-18702 specimen.

Extended Data Fig. 3 Reconstruction of the skull of I. dispar indicating the material represented by every known Ichthyornis specimen.

All elements are scaled to the size of the FHSM VP-18702 specimen. Specimen numbers in bold are those used in the reconstruction. Numbers in italics indicate preservation of the same element in additional specimens.

Extended Data Fig. 4 High-resolution line drawing of the skull of I. dispar.

This the same image as shown in Fig. 2, reproduced at a larger size to show details. All anatomical abbreviations are as indicated in Fig. 2. Solid lines indicate areas known from fossil specimens, and dashed lines indicate unknown areas reconstructed from other ornithuran birds.

Extended Data Fig. 5

Skull and jaw elements of I. dispar specimen BHI 6421.

Extended Data Fig. 6

Skull and jaw elements of I. dispar specimen FHSM VP-18702.

Extended Data Fig. 7

Skull and jaw elements of I. dispar specimen KUVP 119673.

Extended Data Fig. 8

Skull and jaw elements of I. dispar specimen ALMNH 3316.

Extended Data Fig. 9

Skull and jaw elements of I. dispar holotype YPM 1450 showing the nasal and lacrimal elements that have not previously been reported.

Extended Data Fig. 10

Skull and jaw elements of I. dispar specimens YPM 1728, YPM 1459, YPM 1775 and YPM 1749.

Supplementary information

Supplementary Information

This file contains supplementary text 1-9; which contains supplementary tree legends for 1-17, supplementary video legends 1-7, supplementary table 1 and supplementary figure 1

Reporting Summary

Supplementary Data

This file contains Supplementary Trees 1-17. (Tree legends can be found in the Supplementary Information)

Video 1: FHSM 18702, premaxillary beak and articulated rostral maxilla as they were preserved, with palatine attached

Video 2: FHSM 18702, neurocranium

Video 3: FHSM 18702, complete jugal

41586_2018_53_MOESM7_ESM.mov

Video 4: YPM 1450, nasal and lacrimal. Partial nasal and lacrimal are attached as they were discovered in the reanalysis of YPM 1450

Video 5: ALMNH 3316, rostral tip of premaxillae

Video 6: BHI 6421, quadrate, quadratojugal, and two postdentary complexes

Video 7: ALMNH 3316, five fragments of the maxilla showing tooth alveoli and medially positioned occlusal fossae

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Field, D.J., Hanson, M., Burnham, D. et al. Complete Ichthyornis skull illuminates mosaic assembly of the avian head. Nature 557, 96–100 (2018). https://doi.org/10.1038/s41586-018-0053-y

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