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From snout to beak: the loss of teeth in birds

2011; Elsevier BV; Volume: 26; Issue: 12 Linguagem: Inglês

10.1016/j.tree.2011.09.004

1872-8383

Antoine Louchart, Laurent Viriot,

Turtle Biology and Conservation

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. 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. 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]. keratinous tip of the rostrum present on embryos of many oviparous vertebrates, which helps to open the egg, and which disappears after hatching. anatomical direction from the side of the tail (posterior) to that of the rostrum (anterior). the quasi-impossibility for a developmentally lost complex structure to reappear homologously later in evolution. the whole set of influences of epithelial cells on cells of the underlying mesenchyme at specific locations during development, and which progressively shape organs such as teeth. Enamel derives from the epithelium and dentine from the mesenchyme. Epithelium and mesenchyme successively and reciprocally interact with each other via several signal molecules, which induce reactions on competent cells. The nature, dosage, sequential timing and precise location of action of these signal molecules are crucial parameters that regulate precise tooth morphogenesis, differentiation and mineralization of the dental tissues. The networks of odontogenetic signalling pathways are complex, and involve mechanisms of modulation, inhibition, coexpression and others, between molecules. total absence of teeth in an organism (essentially in jaws, and also other locations for some more basal groups of vertebrates). incompletely formed teeth that erupt first in the development, for instance in alligators, where they are rapidly resorbed during embryonic development and replaced by the following generation of teeth. As in most other reptiles, every tooth is then replaced after some time by a newly formed underlying tooth, and again repeatedly during the whole life of the organism (i.e. continuous dental replacement) [15]. the ability of an organism to maintain a constant body temperature regardless of the external conditions. The opposite is poikilothermy, in which the body temperature of an organism varies considerably, essentially as a consequence of variation in external conditions. in skulls, the ability of bone parts to move relative to others, generally without an articulation and, in birds, often through a flexible plate of bone (synostosis). Kinetic skulls are the most widespread forms in vertebrates, and occur in all modern birds. In the latter, kinesis often exists at several levels of the rostrum and mandible. in dental development, these are experiments hybridizing oral epithelium and mesenchyme of these two taxa to examine how teeth develop. They enable researchers to decipher the role of each of these tissues at various developmental stages, and their interaction steps. a powerful organ containing and processing food, predominantly in birds, and unknown in other extant tetrapods. The rare, disputed occurrences of ingested grit (also called gastroliths, or gizzard stones) in some lizards and crocodiles are ambiguous [41]. Also called gastric mill, the gizzard is situated after the crop and the true stomach. It grinds food with the help of ingested grit. Secondary losses of this function have occurred, for instance, in nectarivores and meat-eaters [10]. the monophyletic group constituting all modern birds within the class Aves (birds). They are all toothless. By contrast, many Mesozoic birds had teeth in at least parts of their jaws [2,3]. Based on current evidence, the last birds bearing teeth became extinct close to the Cretaceous–Paleogene (K–P) boundary, 65.5 Ma [4]. Only toothless Neornithes survived the K–P crisis, and later became exceptionally diverse during the Cenozoic. As Neornithes comprises 94% of the approximately 10 500 toothless extant tetrapods, they are the best example of successful diversification following tooth loss among all vertebrates. the limit between the inner part (oral) of a jaw (rostrum or mandible) and its outer part (aboral) at the opening of the jaws. a hard sheath of keratin covering the beak bones of both jaws, and forming the horny beak in birds and other beaked tetrapods. The rhamphotheca entirely covers the outer and part of the inner surfaces of the jaw bones in all Neornithes. These sheaths consist of a heavily keratinized stratum corneum, the outer layer of the integument epithelium, and comprise hydroxyapatite crystals that enhance their hardness [37]. The rhamphotheca grows internally continuously and is abraded externally through use. the ability of an organism to maintain active flight (generally flapping) over long periods of time.