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Branchial tooth plates have also been reported for the basal temnospondyl amphibian Colosteus scutellatus upper Carboniferous, Ma Hook, Interestingly, Schoch noted the coincidence between the loss of branchial denticles, considered to be homologous to teeth, and the loss of gill slits in temnospondyls Fig. Schoch suggested a functional explanation for the simultaneous loss of both branchial denticles and gill slits: Paleontologists indeed tend to use the presence of denticulated pieces of bone branchial ossicles, sensu Schoch, in temnospondyl amphibians as evidence for the presence of a cartilaginous branchial skeleton Boy, and open gill slits e.
Berman, ; Schoch, We propose that the simultaneous loss of gill slits and of pharyngeal denticles teeth is not just functionally but also developmentally related, as the loss of gill slits could prevent the invagination of odontogenic, or inductively competent, ectoderm. However, it is important to note that the presence of gill slits does not necessarily predict the development of branchial denticles.
For example, lungfish Dipnoi lack pharyngeal denticles. This is assumed to be a secondary loss, possibly related to the extensive evolution of the dentition during the early history of the group Ahlberg et al. The loss could be analogous to the loss of teeth on the different gill arches in teleosts.
Branchial denticulated plates branchial ossicles in the pre-metamorphosis stage of Onchiodon labyrinthicus , a temnospondyl amphibian from the lower Permian reproduced from Schoch, , Fig. Also significant to our hypothesis is that in no other tetrapods have pharyngeal teeth, or branchial denticles, ever been observed, despite the presence of pharyngeal endoderm, and despite the likely presence of segmentally arranged ectodermal—endodermal contacts. We speculate that such contacts are constituted solely of outpockets of endoderm abutting the ectoderm, and that without ectodermal invagination into the body, tooth development is not initiated.
This will be easy to test once a reliable marker for endoderm is available. In the urodele amphibian Ambystoma mexicanum , endodermally derived oral teeth are formed in close proximity to the invaginated ectoderm Soukup et al. In our view, the concomitant lack of gill slits and pharyngeal teeth in tetrapods is a strong argument for the ectodermal origin of teeth.
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- Evolutionary and developmental origins of the vertebrate dentition?
Even if the competence to form teeth had been transferred during evolution from ectoderm to endoderm, and the ectoderm would still be required as an inductive tissue, tooth formation would be blocked because of the loss of extensive contact between the two embryonic layers ectoderm and endoderm.
Given that the spiraculum, similar to other gill slits, could allow ectoderm to migrate inwards, it is interesting to note that Eusthenopteron retains denticles inside the spiracular canal Jarvik, Most tetrapod stem group members are now assumed to retain an open spiraculum Clack, Possibly, the rise of the tympanic membrane could have been the ultimate event that definitively sealed off this route for ectodermal migration.
The recent discussion in the literature of whether placoderms e. Again, for the reasons given above, we do not consider differences in patterning sufficient to justify an independent, endodermal origin of pharyngeal denticles. Our hypothesis revives the view of Nelson , , who assumed that small tooth plates were distributed over the entire surface of the oropharyngeal cavity early in gnathostome evolution, comparable to the distribution of placoid scales in elasmobranchs cf.
Reif, , and that these tooth plates, whether large or small, were freely located in the tissues. Subsequently, enlarged tooth plates may have appeared in areas of particular functional importance, and possibly first on the jaws. Although Nelson did not explicitly state that competent ectoderm entered the oropharyngeal cavity through the gill slits, he does refer to a relation between the presence or absence of gill slits and the presence or absence of tooth plates. Looking at the distribution of teeth both in actinopterygian and sarcopterygian lineages, it is clear that the number of tooth-bearing skeletal elements has been reduced during vertebrate evolution.
The dentition associated with the post-hyoid visceral arches was lost in early tetrapods, a loss formerly associated with the loss of respiratory function in the transition from aquatic to terrestrial life. We now believe that loss of the dentition on the visceral arches is only secondarily associated with the loss of their respiratory function and primarily associated with the loss of the gill slits see above.
During metamorphosis, the palatines disappear from the upper jaw and are replaced by the extension of the vomers. In the lower jaw, the coronoids disappear and only the dentaries remain. The restriction of teeth to these skeletal elements can be easily explained by the fact that an ectodermal-endodermal contact necessary to allow these teeth to form, is established only through the mouth opening. By extension, this may explain the restricted oral distribution of teeth in sauropsids Edmund, and in mammals Thenius, Within the actinopterygians, the teleost fish, with 26 species representing approximately one third of all extant vertebrate species, display a prominent evolutionary trend in the loss of teeth from different visceral arches.
Representatives of basal teleostean lineages such as elopomorphs have tooth plates associated with all branchial arches. In contrast, advanced teleosts, such as acanthomorphs, usually retain teeth only on the mandibular and the posteriormost branchial arches Nelson, ; Vandewalle et al. In the ostariophysan lineage on the other hand, oral teeth have been lost in cypriniforms Stock, Instead, the cause of tooth loss is more likely to be found in changes in the molecular networks that regulate tooth initiation, under the selective pressure of regionalization of functions with respect to food processing and respiration.
However, at least one question that has been settled over the past years is whether and how teeth can develop in a Hox-expressing environment, as is the case for the post-mandibular arches in non-mammalians Prince et al.
Indeed, teeth in mammals develop on the mandibular arch only, which is a non-Hox expressing environment Rijli et al. It had previously been demonstrated that, at least in birds, Hox-gene expression and jaw formation are mutually exclusive Couly et al. This implies that, whereas a loss of Hox gene expression in the first branchial arch might have been required for jaws to form Rijli et al. The small number of papers published so far on expression patterns of developmental genes involved in tooth formation in non-mammalians have revealed both conserved and divergent patterns when compared to mammals Fraser et al.
A profound knowledge of the molecular networks and the genes involved is nevertheless imperative if we want to approach the question of ontogenetic and evolutionary tooth loss. To date, most of what is known about the evolutionary loss of teeth associated with certain branchial arches has been published by Stock and colleagues Stock et al. Next, using a zebrafish dlx2b: These authors concluded that preservation of oral enhancer function, unused for more than 50 million years, could be the result of pleiotropic function in the pharyngeal dentition. The above-mentioned findings raise the question of whether teeth can be re-acquired after having been lost in certain areas of the oropharyngeal cavity, or from certain bones.
The reappearance of a fourth row of pharyngeal teeth in the cyprinid fish Barbus paludinosus Golubtsov et al. Similar to the spontaneous reappearance of lost characters in individuals atavism , lost characters can reappear in entire taxa taxic atavism Stiassny, Additional examples of taxic atavisms from other taxa and other organ systems fins, muscles, skull bones are discussed by Raikow et al.
In an excellent review, this author analysed the various levels at which modules units that develop under semi-autonomous control can be identified in the vertebrate dentition, and discussed how these could be related to modularity in the genetic control of development. A final issue regarding the distribution of teeth in the oropharyngeal cavity that needs to be addressed concerns a developmental conundrum, which is the presence of extra-oral teeth. Within recent years, several teleost species have been described with denticles structurally identical to teeth, developed across extra-oral surfaces of the head.
Initially, these extra-oral elements were considered to be dermal denticles reminiscent of ancestral odontodes e. However, given the variety of species involved it became clear that these structures should be regarded as a novel activation of an existing tooth developmental programme in extra-oral locations and not merely as the reappearance of an ancestral character Sire, , see also Stock, We suggest that teeth may have arisen before the origin of jaws, as a result of the invasion of competent, odontode-forming ectoderm into the oropharyngeal cavity through the mouth and gill slits, to interact with neural crest-derived mesenchyme Hall, This hypothesis supports the homology between skin denticles odontodes and teeth.
Introduction
Our hypothesis is based on 1 the assumption that endoderm alone, together with neural crest, cannot form teeth, given that — with one exception — supposedly endodermally derived teeth were never observed to develop without the nearby presence of ectoderm in extant species; 2 the observation that pharyngeal teeth are present only in species known to possess gill slits, and disappear from the pharyngeal region in early tetrapods concomitant with the closure of gill slits, and 3 the assumption that the dental lamina sensu Reif, is not a prerequisite for tooth development, although it may have facilitated tooth formation in advance of need.
One of the primary advantages of our hypothesis is that it can be tested on paleontological data it predicts a correlation between the presence of pharyngeal teeth and gill slits and developmental data in extant species by challenging endoderm alone to make teeth in association with neural crest-derived mesenchyme. In addition, it may serve as a guide for further developmental research, such as a search for an ectodermal signal necessary for pharyngeal tooth development. The authors acknowledge the insightful comments of two anonymous referees.
National Center for Biotechnology Information , U. Journal List J Anat v. Accepted Dec This article has been cited by other articles in PMC. Open in a separate window. Evolutionary modifications in the distribution of teeth A prominent evolutionary trend towards tooth reduction Looking at the distribution of teeth both in actinopterygian and sarcopterygian lineages, it is clear that the number of tooth-bearing skeletal elements has been reduced during vertebrate evolution.
The case of extra-oral teeth A final issue regarding the distribution of teeth in the oropharyngeal cavity that needs to be addressed concerns a developmental conundrum, which is the presence of extra-oral teeth. Acknowledgments The authors acknowledge the insightful comments of two anonymous referees.
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Lamprey Hox genes and the origin of jaws. Determination of the identity of the derivatives of the cephalic neural crest: Loss of teeth and enamel in tetrapods: Fossil record, genetic data and morphological adaptations. The differentiation of neural crest cells into visceral cartilages and odontoblasts in Amblystoma , and a re-examination of the germ-layer theory.
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Contribution of foregut endoderm to tooth initiation of mandibular incisor in rat embryos. Transgenic analysis of Dlx regulation in fish tooth development reveals evolutionary retention of enhancer function despite organ loss. Fgf signaling is required for zebrafish tooth development. Tooth development is independent of a Hox patterning programme. Oxford Monographs on Geology and Geophysics Homologies and evolutionary transitions in early vertebrate history. Basic Structure and Evolution of Vertebrates. Johanson Z, Smith MM. Placoderm fishes, pharyngeal denticles, and the vertebrate dentition.
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Major Events in Early Vertebrate Evolution
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Return of a lost structure in the evolution of the felid dentition.
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The cellular expression of eve1 suggests its requirement for the differentiation of the ameloblasts, and for the initiation and morphogenesis of the first tooth in the zebrafish Danio rerio. Evolution and development of teeth. Bock GR, Cardew G, editors. The oldest articulated chondrichthyan from the early Devonian period. It could be through conference attendance, group discussion or directed reading to name just a few examples. We provide a free online form to document your learning and a certificate for your records. Already read this title? Please accept our apologies for any inconvenience this may cause.
Add to Wish List. Toggle navigation Additional Book Information. Description Table of Contents. Summary A multi-author volume Major Events in Early Vertebrate Evolution examines the origin and early evolution of the backboned animals vertebrates -the group which comprises all fishes, amphibians, reptiles, birds and mammals, including ourselves. This volume draws together evidence from fossils, genes, and developmental biology the study of how embryos grow and develop to answer questions such as: The authors are all experts of international standing in their respective fields, and present some of their own recent findings in conjunction with reviews of the latest work in this fast-moving and fascinating area of biology.
Table of Contents 1. Holland and Nicholas D. The Cambrian Origin of Vertebrates M. Paul Smith, Ivan J. Sansom and Karen D. Origin of a Mineralized Skeleton Philip C. Donoghue and Richard J. The Relationship of Lampreys to Hagfishes: The evolution of Vertebrate Dentitions: