Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
, 114 (41), 10930-10935

Heterochronic Truncation of Odontogenesis in Theropod Dinosaurs Provides Insight Into the Macroevolution of Avian Beaks

Affiliations

Heterochronic Truncation of Odontogenesis in Theropod Dinosaurs Provides Insight Into the Macroevolution of Avian Beaks

Shuo Wang et al. Proc Natl Acad Sci U S A.

Erratum in

Abstract

Beaks are innovative structures characterizing numerous tetrapod lineages, including birds, but little is known about how developmental processes influenced the macroevolution of these important structures. Here we provide evidence of ontogenetic vestigialization of alveoli in two lineages of theropod dinosaurs and show that these are transitional phenotypes in the evolution of beaks. One of the smallest known caenagnathid oviraptorosaurs and a small specimen of the Early Cretaceous bird Sapeornis both possess shallow, empty vestiges of dentary alveoli. In both individuals, the system of vestiges connects via foramina with a dorsally closed canal homologous to alveoli. Similar morphologies are present in Limusaurus, a beaked theropod that becomes edentulous during ontogeny; and an analysis of neontological and paleontological evidence shows that ontogenetic reduction of the dentition is a relatively common phenomenon in vertebrate evolution. Based on these lines of evidence, we propose that progressively earlier postnatal and embryonic truncation of odontogenesis corresponds with expansion of rostral keratin associated with the caruncle, and these progenesis and peramorphosis heterochronies combine to drive the evolution of edentulous beaks in nonavian theropods and birds. Following initial apomorphic expansion of rostral keratinized epithelia in perinatal toothed theropods, beaks appear to inhibit odontogenesis as they grow postnatally, resulting in a sequence of common morphologies. This sequence is shifted earlier in development through phylogeny until dentition is absent at hatching, and odontogenesis is inhibited by beak formation in ovo.

Keywords: Caenagnathidae; Sapeornis; beak evolution; ontogenetic edentulism; tooth reduction.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Dinosaurian and crocodilian dentaries illustrated by CT data, showing the presence of the alveolar canal and other alveolar vestiges. (A) Dorsal view and (B) coronal section of Caenagnathasia sp. (IVPP V20377). (C) Dorsal view of rostral dentary of cf. Chirostenotes TMP 2012.12.12, and (Inset) entire mandible. Photographs in Fig. 1C are reproduced with permission from ref. . Copyright 2008 Canadian Science Publishing or its licensors. (D) Mirror symmetry of right dentary of Sapeornis chaoyangensis (LPM B00015) in lingual view showing vestigial alveoli and foramina present on the dorsolingual aspect of the dentary. (E–K) Coronal dentary sections of (E) S. chaoyangensis (LPM B00015), (F) subadult Limusaurus inextricabilis (IVPP V15923), (G) juvenile L. inextricabilis (IVPPV15301), (H) extant Alligator sinensis (IVPP 1361), (I) extant Pavo sp. (IVPP 1032), (J) Confuciusornis sp. (IVPP V23275), and (K) Khaan mckennai (IGM 100/973). av, alveolar vestige; mc, mandibular canal (V3); mf, Meckelian foramen; mg, Meckelian groove; sd, supradentary; t, tooth. White stars, swollen ridge present on the lingual aspect of the dentary; red arrows, lingual groove; white arrows, foramina piercing the lingual groove on the medial aspect of the dentary; dashed lines in A and D mark the positions of the slices shown in B and E, respectively; light yellow dashed lines in F and G mark the dentary; orange dashed line in G marks a replacement tooth present inside an enclosed dentary alveolus. (Not to scale.)
Fig. 2.
Fig. 2.
Development of chicken beak keratin. (A–C) Sagittal sections of the snout showing expression patterns of beak keratin in wild type chicken: (A) E7, (B) E12, and (C) E20. Inset in A shows whole-mount in situ hybridization of beak keratin, and red arrows in A–C mark beak keratin expression in E7 egg tooth, and E12 and E20 upper and lower beaks. (D–F) Sagittal sections of the snout showing expression patterns of beak keratin in developing chicken with molecular perturbation: (D) control; (E) BMP4 overexpression; and (F) noggin overexpression. (G and H) Stereophotos showing ectopic expression of beak keratin caused by BMP4 overexpression: (G) control (left lateral view); (H) ectopic expression of beak keratin on face (left lateral view); (I) coronal section of the snout in H showing in situ hybridization of beak keratin. Dashed line in H marks the position of the slice shown in I. Red arrows mark positions where normal keratin is present, green arrows mark the anteroposterior length of the keratin expression domain in the upper beak, and blue arrows mark ectopic expression of beak keratin on the face. et, egg tooth; lb, lower beak; ub, upper beak. (Scale bars, 1 mm.)
Fig. 3.
Fig. 3.
Summary of evidence for a macroevolutionary model of edentulism in vertebrates. (A) Evidence from extant nonavian vertebrate lineages with complete or near edentulism, showing phylogenetic and trophic diversity of ontogenetic tooth loss. (B) Evidence from select theropod dinosaur lineages focusing on Coelurosauria and showing independent evolution of adult edentulism at least seven times (–7). ?, hypothesized state/partial evidence; B, baleen; Bb, barbels; DR, sexually dimorphic reduction pattern; E, electroreception; F, filtration; G, gastric mill/ gizzard; H, expanded hypapophyses; R, rhamphotheca; S, suction feeding; Sw, sword; T, projectile tongue. (Taxon silhouettes not to scale.)
Fig. 4.
Fig. 4.
Transformations involved in theropod tooth reduction. Right lateral view of the head (Left) and transverse view of the dentary (Right). (A) Normal tooth development and tooth replacement with apomorphic keratinized rhamphotheca covering only the rostral-most portion of the jaws. (B) Tooth replacement is impeded by external closure and/or constriction of alveoli and regional tooth reduction occurs. (C) As the keratinized rhamphotheca enlarges, the remaining teeth are either functionally reduced or redundant. (D) Edentulous beak completely covered by rhamphotheca. Green, mandibular canal; yellow, alveolus and alveolar canal; orange, tooth. (Not to scale)

Similar articles

See all similar articles

Cited by 4 articles

Publication types

LinkOut - more resources

Feedback