Review
From snout to beak: the loss of teeth in birds

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All living birds are toothless, constituting by far the most diverse toothless vertebrate clade, and are striking examples of evolutionary success following tooth loss. In recent years, an unprecedented number of Mesozoic birds have been described, illustrating the evolution of dentition reductions. Simultaneously, major advances in experimental embryology have yielded new results concerning avian edentulism. Reviewing these lines of evidence, we propose hypotheses for its causes, with a prominent role for the horny beak during development. A horny beak and a muscular gizzard functionally ‘replaced’ dentition for food acquisition and processing, respectively. Together with edentulism itself, these features and others contributed to the later success of birds, as a result of their high performance or additional functionality working in concert in these complex organisms.

Section snippets

Tracking the roots of bird beak success

Food acquisition and processing are fundamental in all heterotrophs because they control the availability of energy required for maintenance, growth and reproduction. Therefore, the mechanism by which food is brought from the environment into the organism is of the most basic biological importance. In this context, it is interesting that, in tetrapods, essentially just two basic mechanisms have evolved to achieve this: dentition and a horny beak (rhamphotheca; see Glossary) together account for

Evo-devo insights

Three types of developmental event, which are not mutually exclusive, might have led to repeated dentition reduction and loss in birds. Here, we examine the evidence for each of these in turn.

Tooth loss in avian evolution

The developmental processes discussed above suggest probable mechanisms for tooth loss. However, to find out how tooth loss actually happened, how many times and with what phenotypes produced as a result of the underlying genetic changes, it is necessary to trace the evolution of bird dentitions through time, using the fossil record.

Crucial innovations for edentulism

Among the anatomical, physiological or behavioral innovations thought to have favored the viability of edentulism in birds 1, 10, 11, we examine first the evolution of the rhamphotheca (which also played a major role developmentally) in relation to dentition reduction. We then address the role of the muscular gizzard and, more indirectly, that of homeothermy and sustained active flight.

Tooth loss, rhamphothecae and gizzards in other tetrapods

Dentition reductions occurred in a limited number of tetrapod clades outside Aves, including total edentulism in 15 independent clades of extant or extinct groups (Figure 3). These reductions, partial or total, are relatively more common in archosaurs than in other tetrapods. The closer to Aves, the more frequent they are, and always concomitant with the acquisition of elements of rhamphotheca. Evidence of a muscular gizzard, intrinsically rare, is known at least in several clades of dinosaurs

Towards a model

We suggest that, despite the loss of dentition, a network of related innovations in complex interplay through natural selection has favored avian evolutionary diversification, in particular in the Neornithes. The acquisition of a muscular gizzard and of a rhamphotheca appear to have been crucial in allowing edentulism and making it viable. Food is stored in the crop, and hence continuously available even outside feeding activities. The muscular gizzard with ingested gastroliths efficiently

Concluding remarks

The concentration of independent dentition reductions, including edentulism, in early birds is unrivalled and attests to an early fragility in their odontogenetic program. Patterns of intermediate, partial stages of dentition reduction were diverse, as seen in the pterosaurs. The pattern occurring on the line to neornithine edentulism is congruent with recent developmental models of the rhamphotheca. The appearance of rhamphothecal elements probably had a crucial role in the arrest of

Prospects

There is a need to investigate the presence and extent of the rhamphotheca in different lineages of Mesozoic birds, and the evolution of its spatial relation with dentition. Comparisons at different levels with pterosaurs are required, as this group appears to share many characteristics with birds regarding dentition. Concerning avian dental evolution, preceding tooth losses, tooth size (generally millimetric) and shape appear to be very diverse across the different lineages [3]. These aspects

Acknowledgments

We thank H. Magloire, J-Y. Sire, E. ‘Dino’ Frey, B. Pain, V. Laudet, J. Burden and all members of the teeth evo-devo team at IGFL, for fruitful discussions and comments on earlier drafts. AL thanks the IFRO for financial support to this work in 2010. We also benefited from the CNRS grant PEPS 2010 (Projets Exploratoires/Premier Soutien) ‘Pouladents’. We thank G. Dyke and two anonymous reviewers for comments that improved the manuscript.

Glossary

Arcilineal
simple movement of the lower jaw relative to the upper jaw in which it closes or opens following an arc, and without longitudinal or transverse movements. This is the basal type of jaw movement in tetrapods, characteristic of Diapsida among reptiles, and the only one known in Aves. By contrast other tetrapods exhibit propalineal (caudo-rostral; e.g. turtles and tortoises) or transverse jaw movements, or both (e.g. mammals) [11].
Caruncle (also called the ‘egg tooth’)
keratinous tip of

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