Bony pseudoteeth of extinct pelagic birds (Aves, Odontopterygiformes) formed through a response of bone cells to tooth-specific epithelial signals under unique conditions

Abstract

Modern birds (crown group birds, called Neornithes) are toothless; however, the extinct neornithine Odontopterygiformes possessed bone excrescences (pseudoteeth) which resembled teeth, distributed sequentially by size along jaws. The origin of pseudoteeth is enigmatic, but based on recent evidence, including microanatomical and histological analyses, we propose that conserved odontogenetic pathways most probably regulated the development of pseudodentition. The delayed pseudoteeth growth and epithelium keratinization allowed for the existence of a temporal window during which competent osteoblasts could respond to oral epithelial signaling, in place of the no longer present odontoblasts; thus, bony pseudoteeth developed instead of true teeth. Dynamic morphogenetic fields can explain the particular, sequential size distribution of pseudoteeth along the jaws of these birds. Hence, this appears as a new kind of deep homology, by which ancient odontogenetic developmental processes would have controlled the evolution of pseudodentition, structurally different from a true dentition, but morphologically and functionally similar.

Figure 1

Schematic reconstruction of the pseudodentition of a four-ranked pseudotoothed bird. (a) Left view of reconstructed beak and head. The rostrum and most of the mandible are represented with the rhamphotheca (keratinized epithelium; in yellow) covering the jaw bones, except for a small area of the mandible to show the underlying bone. (b) Magnification of the bony cores of two adjacent pseudoteeth (the larger is a PT2, the smaller is a PT4) of Pelagornis mauretanicus (AaO-PT-B), in lateral x-ray microtomographic view. (c) Structure of the pseudoteeth bony cores in (a), shown in parasagittally truncated x-ray microtomographic view. (d and e) (double frame), true tooth of the Cretaceous bird Hesperornis regalis (YPM.1206B) for comparison with pseudoteeth (in volume and parasagittally truncated synchrotron x-ray microtomographic views, respectively). Proportions based on data from Pelagornis species such as P. mauretanicus. Views in inserts are reversed, except (c), in order to fit a left mandibular placement in lateral view. The real position (left vs. right, rostral vs. mandibular) of the P. mauretanicus pseudoteeth and the H. regalis tooth, shown in inserts (b–e), is indeterminate^,. Distribution of PT1s to PT4s is indicated along part of the rostrum. b, bone; c, crown; d, dentin; e, enamel; mjb, main jaw bone; pc, pulp cavity; r, root; rh, rhamphotheca. Scale bars, main frame 2 cm, inserts (b–e) 2 mm.

Figure 2

Hypotheses for the phylogenetic position of pseudotoothed birds (Odontopterygiformes). The three hypotheses of phylogenetic placement of the Odontopterygiformes are shown in orange: basal within Anseriformes (1), sister to crown Galloanserae (2), or sister to crown Neognathae (3). Squares indicate the probable position of main innovations related to jaws: acquisition of streptognathism and loss of mandibular symphysis (red square in Hesperornithiformes and Ichthyornithiformes, violet squares in Odontopterygiformes), loss of teeth on the line to Neornithes (blue square), and acquisition of pseudoteeth in Odontopterygiformes (green squares). The horizontal dashed line indicates approximate position of the Cretaceous-Paleogene extinction event.

Figure 3

Proposed model of pseudotooth development compared with that of a tooth. Schematized transverse jaw section across a pseudotooth (A) and across a true tooth (B). In (A) the developing pseudotooth is shown at a growth stage approximately equivalent to that of stage 6 in Fig. 4. In (B) the developing tooth is shown schematically at “late bell” stage. In both instances epithelial-mesenchymal interactions are indicated, with the different categories of involved tissues, and their direction of growth. Thickness of tissues is exaggerated for convenience of visibility, especially for the mesenchyme.

Figure 4

Proposed model of pseudodentition development. The differential growth of the differently ranked pseudoteeth is shown in eight stages, in the parasagittal section of a jaw for all pseudoteeth. For convenience of visibility, tissue thicknesses are exaggerated, ~10 × (bone, epithelium) and ~100 × (mesenchyme). Epithelial-mesenchymal interactions between the basal epithelium cells and the periosteal osteoblasts start when the intervening space becomes lower than ~100 µm (Stage 2). This interaction ends when epithelial cells become keratinized (Stage 8).