Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
Review
, 214 (4), 477-501

Loss of Teeth and Enamel in Tetrapods: Fossil Record, Genetic Data and Morphological Adaptations

Affiliations
Review

Loss of Teeth and Enamel in Tetrapods: Fossil Record, Genetic Data and Morphological Adaptations

Tiphaine Davit-Béal et al. J Anat.

Abstract

Since their recruitment in the oral cavity, approximately 450 million years ago, teeth have been subjected to strong selective constraints due to the crucial role that they play in species survival. It is therefore quite surprising that the ability to develop functional teeth has subsequently been lost several times, independently, in various lineages. In this review, we concentrate our attention on tetrapods, the only vertebrate lineage in which several clades lack functional teeth from birth to adulthood. Indeed, in other lineages, teeth can be absent in adults but be functionally present in larvae and juveniles, can be absent in the oral cavity but exist in the pharyngeal region, or can develop on the upper jaw but be absent on the lower jaw. Here, we analyse the current data on toothless (edentate) tetrapod taxa, including information available on enamel-less species. Firstly, we provide an analysis of the dispersed and fragmentary morphological data published on the various living taxa concerned (and their extinct relatives) with the aim of tracing the origin of tooth or enamel loss, i.e. toads in Lissamphibia, turtles and birds in Sauropsida, and baleen whales, pangolins, anteaters, sloths, armadillos and aardvark in Mammalia. Secondly, we present current hypotheses on the genetic basis of tooth loss in the chicken and thirdly, we try to answer the question of how these taxa have survived tooth loss given the crucial importance of this tool. The loss of teeth (or only enamel) in all of these taxa was not lethal because it was always preceded in evolution by the pre-adaptation of a secondary tool (beak, baleens, elongated adhesive tongues or hypselodonty) useful for improving efficiency in food uptake. The positive selection of such secondary tools would have led to relaxed functional constraints on teeth and would have later compensated for the loss of teeth. These hypotheses raise numerous questions that will hopefully be answered in the near future.

Figures

Fig. 1
Fig. 1
Simplified tetrapodan phylogeny with indication of toothless lineages (red lines), enamel-less lineages (blue lines) and lineages with enamel reduction and tooth reduction (green lines). Tetrapodan relationships after Murphy et al. (2001) and Hedges (2002).
Fig. 2
Fig. 2
Simplified phylogeny of Avialae (after Chiappe, 2002). Lineages with toothless taxa are in red. (A) Skull of Velociraptor. (B) Skull of Archaeopteryx lithographica. (C) Skull of Confuciusornis sanctus. (D) Comparison of the skulls ofC. sanctus and a pigeon (bottom). (E) Skull of Hesperornis regalis (after Marsh, 1880). (F) Ichthyornis dispar (after Marsh, 1883).
Fig. 3
Fig. 3
A shift in the positioning of the odontogenic epithelium relative to the dental competent mesenchyme could explain the loss of the ability to form teeth in the modern bird ancestor. Schematic drawings summarizing the chick tooth experiments. (A) Mouse molar developmental stages, from bud [embryonic day (E)12.5] to cap (E14.5) to bell (E16.5). The condensing mesenchyme around the bud stage tooth germ expresses Bmp4 and Msx1 and induces development of the enamel knot at the cap stage, which expresses signalling molecules such as Shh. The inner enamel epithelium forms the ameloblasts that form enamel, whereas the adjacent mesenchyme forms the odontoblasts that form dentine (see Caton & Tucker, 2009). (B) Chick development. At Hamburger & Hamilton (HH) stage 28 a bud-like thickening of the oral epithelium is observed. Expression of Bmp4 and Msx1 is not, however, associated with this region. No further tooth development is observed at later stages and the thickening regresses. Note that, at an earlier stage (stage 24), Bmp4 expression is epithelial and shifts into the mesenchyme at stage 28 (Francis-West et al. 1994). (C) When a bead impregnated with Bmp4 and Fgf4 is implanted into the chick epithelium, the expression of Bmp4 and Msx1 in the mesenchyme extends around the developing tooth bud. This leads to the extension and folding of the bud epithelium, and induction of Shh. No further progression of the tooth germs is observed, however (Chen et al. 2000). (D) When mouse mesenchyme is combined with chick epithelium (either by recombination of mandible tissue or by earlier neural crest grafts of mouse neural crest into a chick embryo), the chick epithelium induces Msx1 and Bmp4 in the mouse mesenchyme. The tooth germ progresses to the cap stage and forms an enamel knot-like structure expressing Shh. The mouse tissue differentiates into odontoblasts and forms a bell stage tooth germ. Tooth differentiation does not proceed beyond this stage and enamel is not deposited (Wang et al. 1998; Mitsiadis et al. 2003). (E) In the chick mutant talpid2 a shift in the positioning of the epithelium and mesenchyme has been described (indicated by dashed lines and arrows). The chick epithelium is able to induce expression of Bmp4 in the underlying mesenchyme and expresses Shh. The tooth germ develops by evagination, similar to that observed in alligator embryos. At later stages differentiated odontoblasts are identified by histology but no further differentiation occurs (Harris et al. 2006).
Fig. 4
Fig. 4
Simplified phylogeny of Batracia (after Marjanovic & Laurin, 2007). Red line: edentate toad lineage. It is worth noting that several species in various anuran lineages have also lost the ability to form teeth independently (not shown). †Extinct lineage.
Fig. 5
Fig. 5
Simplified turtle relationships (after Gaffney & Meylan, 1988; Rieppel, 1999; Joyce, 2007). Green lines: lineages with palatine teeth only; red lines: toothless lineages. (A) Skull of Proganochelys quenstedti (from Gaffney, 1990). (B) Dorsal view of the skull and beak of the snapping turtle (aquatic). (C) Skull and beak of a terrestrial turtle. †Extinct lineages.
Fig. 6
Fig. 6
(A and C) Lateral and ventral views of the skull of a primitive tetrapod, the parareptilian Procolophon. (B and D) Lateral and ventral views of the skull of Proganochelys quenstedti. (E) Ventral view of the skull of Kayentachelys aprix. Small dots represent teeth. M, maxillary; Pal, palatine; Pm, pre-maxillary; Pt, pterygoid; V, vomer. (A and C) From Carroll & Lindsay (1985). (B and D) From Gaffney (1990). (E) From Gaffney et al. (1987). Scale bars, 1 cm.
Fig. 7
Fig. 7
Lateral and ventral views of the skull of Monotremata. (A) The echidna, Tachyglossus aculeatus. (B) A fossil (adult) ornithorhynchid, Obdurodon dicksoni (after Musser & Archer, 1998). In this species the skull morphology is very similar to that in platypus (see Fig. 13), except for the presence of teeth in adults (two pre-molars and two or three molars). Scale bars: A, 1 cm; B, 2 cm.
Fig. 13
Fig. 13
Ornithorhynchus anatinus, the platypus. (A) Lateral view of the skull in a juvenile. (B) Lateral view of the skull in adult. (C) The three teeth (a small pre-molar and two molars) on the upper left maxilla of a juvenile. (D) The three opposite teeth on the lower left jaw. Bars: A and B, 1 cm; C and D, 1 mm.
Fig. 8
Fig. 8
Simplified phylogeny of Xenarthra and Afrotheria (after Hallström et al. 2007; Seiffert, 2007). Red lines: toothless lineages; blue lines: enamel-less lineages; green lines: enamel reduction. (A) Lateral view of the skull and detail of the upper cheek teeth of an aardvark, Orycteropus afer. (B) Ventral view of the skull and of the upper right jaw, and detail of extracted teeth of a nine-banded armadillo, Dasypus novemdelineatus. (C) Ventral view of the skull of a giant anteater, Myrmecophaga tridactyla. (D) Ventral view of the skull and detail of the upper jaw of a three-toed sloth. †Extinct lineages.
Fig. 9
Fig. 9
Simplified phylogeny of Pholidota (after McKenna & Bell, 1997; Nowak, 1999). Red lines: toothless lineages. (A) Dorsal view of the right dentary of a primitive palaeanodont (Eocene) showing the large canine (no incisors) and the alveoli for three pre-molars p2–p4 (p1 absent) and two molars. Modified after Rose et al. (2004). (B) Ventral view of the skull and lower jaw of a living pangolin, Manis javanica. Note the extremely narrow and weak blade-like mandible. †Extinct lineages. Scale bars: A, 1 mm; B, 1 cm.
Fig. 10
Fig. 10
Simplified phylogeny of Cetacea (after Uhen, 2002; Deméré et al. 2008). (A) Skull of an early archaeocete, Pakicetus from the early Eocene. (B) The toothed jaws of an odontocete, the orca Orcinus orca. (C) The edentulous jaw of a mysticete, the bowhead whale Balaena mysticetus. (D) Detail of a baleen plate of a gray whale Eschrichtius robustus. †Extinct lineages.
Fig. 11
Fig. 11
Histological evidence of embryonic teeth developing in the embryos of the baleen whale Balaenoptera physalus. Most tooth germs attain an advanced bell stage, until dentine deposition, and are then progressively resorbed. (A–D) Tooth morphogenesis and differentiation. (E and F) Resorption. (A) Cap stage. (B) Bell stage; dental epithelium starts to fold around dental papilla cells. (C) Advanced bell stage, in which the dental epithelium entirely surrounds the dental papilla. (D) A thin layer of dentine has been deposited; enamel is not identified. The arrows point to numerous capillary blood vessels located close to the dentine layer. (E) Initiation of resorption process. White arrows indicate osteoclasts. Black arrow points to blood vessels. (F) Advanced stage of resorption. Black arrows indicate the dentine; white arrow points to osteoclasts. Modified after Karlsen (1962). Bars: A, 50 µm; B, C, E and F, 100 µm; D, 500 µm.
Fig. 12
Fig. 12
Tooth developing in the nine-banded armadillo. Note the presence of a thin layer of enamel covering the orthodentine crown. Modified after Martin (1916).

Comment in

Similar articles

See all similar articles

Cited by 23 PubMed Central articles

See all "Cited by" articles

LinkOut - more resources

Feedback