Evo-devo of the diversification and loss of dentition in Birds – PIAFS

The fossils that represent, on the one hand the teeth of birds, and on the other hand the more recent bony pseudoteeth, are excessively rare (moreover the pseudoteeth are fragile and are often badly preserved). It is therefore impossible (or exceptional) to be able to make thin sections, in order to observe the internal microstructure and histology. Therefore, we mainly use 3D imaging technologies that allow us to visualize the interior of these fossils through variations in density, without altering them in any way. This consists of conventional x-ray microtomography; and also (particularly for teeth, which are denser and smaller) synchrotron x-ray microtomography which is more efficient, with higher intensity, more parallel beams and at less dispersed wavelengths; the latter therefore makes it possible to “break through” structures in denser materials, and also to give higher resolutions (smaller voxel sizes). The 3D images obtained are analyzed in 3D imaging using specialized software. To complete this, we also make surface observations of bird tooth enamel by SEM imaging (scanning electron microscopy) and confocal imaging. In addition, we make some thin sections of histology in fragments of bony pseudoteeth of Odontopterygiformes.

Our synthetic review revealed that tooth loss occurred many times in different lineages in birds during the Cretaceous, as did partial dentition reductions, which occurred in very diverse ways. Dental reductions were closely accompanied by the expansion of the horny beak on the jaws. Several traits such as this beak expansion, indirectly related to dentition loss, may have aided the evolutionary success of post-K-Pg crisis birds; the diversity and adaptability of the beak shapes of modern birds seem to be illustrative of this (Louchart & Viriot 2011). We were able to show precisely that in the different toothed birds: the attachment is completely thecodont by gomphosis (even if in Hesperornis the implantation is located in a long groove, a probable autapomorphy), and the dental replacement is lingual via a resorption pit in the root. Among the latest toothed birds closest to modern birds, the microstructure and morphology differ greatly between Ichthyornis and Hesperornis. But in both cases there is a reduction in enamel thickness and complexity, which could be a trend in tooth reduction. Hesperornis shows a high dentin growth rate compared to non-avian dinosaurs (Dumont et al. 2016). We have described an Archaeopterygidae tooth in the Lower Cretaceous of France, the first documented occurrence outside Germany and other than Late Jurassic (Louchart & Pouech 2017). Concerning the bony pseudoteeth of Odontopterygiformes, we described for the first time their precise histology: among other things, the bone is fibrolamellar and strongly remodeled secondarily, and the pseudoteeth are just outgrowths of the jaws. Among two hypotheses, several factors make us favor this one: they develop late, when the jaws have almost reached their adult dimensions. This would suggest that the young were dependent (altricial) (Louchart et al. 2013). We then developed a model that could explain the development of these pseudodentitions, and a body of evidence shows that it was probably derived from odontogenetic developmental bases (formation of real teeth), inherited from their ancestors. Still competent osteoblasts could, instead of absent odontoblasts, respond to epithelial signaling, inducing conical growth. Thus, morphogenesis would have “used” bone instead of dentin; and the epithelium, which will keratinize, will not form enamel, the enamel genes having become pseudogenes already in the Neornithes. Finally, dynamic zones of inhibition may explain the particular sequential distribution of pseudoteeth according to their size along the jaw (Louchart et al. 2018).

This research has therefore made it possible, among other things, to understand more precisely the nature of the dentitions of Mesozoic birds and their losses, as well as the nature of the pseudodentitions of the extraordinary Cenozoic Odontopterygiformes. They revealed a particular form of homology between these two structures, teeth and pseudoteeth, despite the different tissues involved (final tissues: dentin and enamel vs. bone and keratinized epithelium). Future research in different fields may test or refine these hypotheses. For example, searches for new fossils will be important: (i) at the base of the line that led to the Neornithes, in the late Cretaceous, to better specify the age of the loss of the dentition, (ii) at the base of the pseudotoothed birds, potentially around the K-Pg limit (and including anteriorly). Thus, new discoveries could «reduce« the known time elapsed between the loss of dentition and the first pseudoteeth, time during which an odontogenic potential could have been preserved and remained activatable, but diverted to different tissues (today this interval as known – between ca. 115 Ma and ca. 60 Ma – spans about 55 million years; Louchart et al. 2018). The model features zones of inhibition centered on the tip of the cone of each developing pseudotooth, homologous to an «enamel knot«, and also features the reduction of each radius of inhibition over time, allowing pseudoteeth to emerge between two larger (earlier) pseudoteeth sequentially, when the latter are completing their growth. This could explain this «wave« distribution of pseudoteeth along the jaws. It would be interesting in the future to study the teeth of certain fishes (e.g., saw sharks of the genus Pristiophorus, and Cynodontidae and Erythrinidae fishes), which present the same wave distribution but with real teeth (Louchart et al. 2018), in order to seek the materialization (though with thrue teeth) of such fields of inhibition, the latter remaining largely theoretical.

—Louchart, A., Buffrénil, V. de, Bourdon, E., Dumont, M., Viriot, L., & Sire, J. Y. (2018). Bony pseudoteeth of extinct pelagic birds (Aves, Odontopterygiformes) formed through a response of bone cells to tooth-specific epithelial signals under unique conditions. Scientific Reports, 8(1), 12952. DOI : doi.org/10.1038/s41598-018-31022-3
—Louchart, A., & Pouech, J. (2017). A tooth of Archaeopterygidae (Aves) from the Lower Cretaceous of France extends the spatial and temporal occurrence of the earliest birds. Cretaceous Research, 73, 40-46. DOI : doi.org/10.1016/j.cretres.2017.01.004
—Dumont, M., Tafforeau, P., Bertin, T., Bhullar, B. A., Field, D., Schulp, A., Strilisky, B., Thivichon-Prince, B., Viriot, L., & Louchart, A. (2016). Synchrotron imaging of dentition provides insights into the biology of Hesperornis and Ichthyornis, the “last” toothed birds. BMC Evolutionary Biology, 16, 1-28. DOI : doi.org/10.1186/s12862-016-0753-6
—Louchart, A., Sire, J. Y., Mourer-Chauviré, C., Geraads, D., Viriot, L., & De Buffrenil, V. (2013). Structure and growth pattern of pseudoteeth in Pelagornis mauretanicus (Aves, Odontopterygiformes, Pelagornithidae). PLoS One, 8(11), e80372. DOI : doi.org/10.1371/journal.pone.0080372
—Louchart, A., Viriot, L., & Dubois, A. (2013). The use of the prefix Pan-and other problems in zoological family-series nomenclature. Zootaxa, 3750(2), 197-200. DOI : doi.org/10.11646/zootaxa.3750.2.9
—Louchart, A., & Viriot, L. (2011). From snout to beak: the loss of teeth in birds. Trends in Ecology & Evolution, 26(12), 663-673. DOI : doi.org/10.1016/j.tree.2011.09.004

The appearance of a dentition in Vertebrates has been a key-innovation in their evolution. It was followed by a tremendous diversification with modifications in number, shape, structure, implantation, growth, and replacement of teeth. These are studied especially in mammals, and also in fossil groups such as non-avian dinosaurs. Birds today stand alone with their lack of teeth. But between 146 and 65.5 million years before present, many groups of birds were toothed, at least partly. The fossil record of these taxa is exceptional and growing rapidly. In parallel, recent experiments have produced rudiments of teeth in mutant chicken embryos. In our project, we wish for the first time to investigate the phenotypes of teeth and dentitions in Mesozoic birds, and in experimental embryos, and to compare them with those of other archosaurs, and other tetrapods. We also wish to decipher the pathways and mechanisms of dental reductions and losses in birds, through an evo-devo approach. Third, we will investigate the nature and ontogenetic origin of the structures known as pseudo-teeth or bony teeth in two groups of extinct Cenozoic birds, which can shed new light on the evolution and loss of teeth in the entire class.