Developmental and evolutionary origins of the vertebrate dentition: molecular controls for spatio-temporal organisation of tooth sites in osteichthyans

The rainbow trout (Oncorhynchus mykiss) as a developmental model surpasses both zebrafish and mouse for a more widespread distribution of teeth in the oro-pharynx as the basis for general vertebrate odontogenesis, one in which replacement is an essential requirement. Studies on the rainbow trout have led to the identification of the initial sequential appearance of teeth, through differential gene expression as a changing spatio-temporal pattern, to set in place the primary teeth of the first generation, and also to regulate the continuous production of replacement tooth families. Here we reveal gene expression data that address both the field and clone theories for patterning a polyphyodont osteichthyan dentition. These data inform how the initial pattern may be established through up-regulation at tooth loci from a broad odontogenic band. It appears that control and regulation of replacement pattern resides in the already primed dental epithelium at the sides of the predecessor tooth. A case is presented for the developmental changes that might have occurred during vertebrate evolution, for the origin of a separate successional dental lamina, by comparison with an osteichthyan tetrapod dentition (Ambystoma mexicanum). The evolutionary origins of such a permanent dental lamina are proposed to have occurred from the transient one demonstrated here in the trout. This has implications for phylogenies based on the homology of teeth as only those developed from a dental lamina. Utilising the data generated from the rainbow trout model, we propose this as a standard for comparative development and evolutionary theories of the vertebrate dentition.     

The taming of the shrew milk teeth

SUMMARY A characteristic feature of mammalian dentition is the evolutionary reduction of tooth number and replacement. Because mice do not replace teeth, here we used Sorex araneus , the common shrew, as a model to investigate the loss of tooth replacement. Historically, shrews have been reported to initiate the development of several, milk or deciduous teeth but these soon become rudimentary and only the replacement teeth erupt. Shrews thus offer a living example of a derived mammalian pattern where the deciduous tooth development is being suppressed. Based on histological and gene expression analyses of serial sections, we suggest that S. araneus has discernible tooth replacement only in the premolar 4 (P4) position. Both generations of teeth express Shh in the enamel knot and in the inner enamel epithelium. Nevertheless, the deciduous P4 (dP4) is reduced in size during embryogenesis and is eventually lost without becoming functional. Analysis of growth shows that P4 replaces the dP4 in a "double-wedge" pattern indicative of competitive replacement where the suppression of the deciduous tooth coincides with the initiation of its replacement. Because activator–inhibitor mechanisms have been implicated in adjacent mouse molars and in transgenic mice with continuous tooth budding, we suggest that evolutionary suppression of deciduous teeth may involve early activation of replacement teeth, which in turn begin to suppress their deciduous predecessors.     

Making teeth to order: conserved genes reveal an ancient molecular pattern in paddlefish (Actinopterygii)

Ray-finned fishes (Actinopterygii) are the dominant vertebrate group today (+30 000 species, predominantly teleosts), with great morphological diversity, including their dentitions. How dental morphological variation evolved is best addressed by considering a range of taxa across actinopterygian phylogeny; here we examine the dentition of Polyodon spathula (American paddlefish), assigned to the basal group Acipenseriformes. Although teeth are present and functional in young individuals of Polyodon, they are completely absent in adults. Our current understanding of developmental genes operating in the dentition is primarily restricted to teleosts; we show that shh and bmp4, as highly conserved epithelial and mesenchymal genes for gnathostome tooth development, are similarly expressed at Polyodon tooth loci, thus extending this conserved developmental pattern within the Actinopterygii. These genes map spatio-temporal tooth initiation in Polyodon larvae and provide new data in both oral and pharyngeal tooth sites. Variation in cellular intensity of shh maps timing of tooth morphogenesis, revealing a second odontogenic wave as alternate sites within tooth rows, a dental pattern also present in more derived actinopterygians. Developmental timing for each tooth field in Polyodon follows a gradient, from rostral to caudal and ventral to dorsal, repeated during subsequent loss of teeth. The transitory Polyodon dentition is modified by cessation of tooth addition and loss. As such, Polyodon represents a basal actinopterygian model for the evolution of developmental novelty: initial conservation, followed by tooth loss, accommodating the adult trophic modification to filter-feeding.     

Phylogenetic memory of developing mammalian dentition

Structures suppressed during evolution can be retraced due to atavisms and vestiges. Atavism is an exceptional emergence of an ancestral form in a living individual. In contrast, ancestral vestige regularly occurs in all members of an actual species. We surveyed data about the vestigial and atavistic teeth in mammals, updated them by recent findings in mouse and human embryos, and discussed their ontogenetic and evolutionary implications. In the mouse incisor and diastema regions, dental placodes are transiently distinct being morphologically similar to the early tooth primordia in reptiles. Two large vestigial buds emerge in front of the prospective first molar and presumably correspond to the premolars eliminated during mouse evolution. The incorporation of the posterior premolar vestige into the lower first molar illustrates the putative mechanism of evolutionary disappearance of the last premolar in the mice. In mutant mice, devious development of the ancestral tooth primordia might lead to their revivification and origin of atavistic supernumerary teeth. Similarity in the developmental schedule between three molars in mice and the respective third and fourth deciduous premolar and the first molar in humans raises a question about putative homology of these teeth. The complex patterning of the vestibular and dental epithelium in human embryos is reminiscent of the pattern of "Zahnreihen" in lower vertebrates. A hypothesis was presented about the developmental relationship between the structures at the external aspect of the dentition in mammals (oral vestibule, pre-lacteal teeth, paramolar cusps/teeth), the tooth glands in reptiles, and the earliest teeth in lower vertebrates.     

Ontogeny and homology of the dentition in dasyurid marsupials: Development inSminthopsis virginiae

Histological analysis of an ontogenetic series of the dasyurid marsupial,Sminthopsis virginiae, from birt to 60 days old, was undertaken to assess the developmental homologies of the deciduous and successional teeth. This period covers the time from the initiation of all teeth as epithelial buds up until the time of early eruption of some teeth. In addition, two older specimens, aged 81 and 97 days, were examined to provide additional information on the state of differentiation of the unerupted third premolar. In the postcanine dentition, only a single tooth position, dP3, was characterized by the later development of a replacing successional tooth (P3), following developmental pathways identical to those in eutherian mammals. In contrast, the anterior dentition is characterized by the formation of rudimentary, nonerupting deciduous incisors and canines, and by the accelerated development of normal, erupting successional incisors and canines in both jaws. Comparison of relative developmental stages for each tooth position throughout its preeruptive ontogeny suggests thatheterochrony (both developmental acceleration and retardation) has played an important role in the evolutionary history of the dasyurid dentition. Differing aspects of this phenomenon are identified and discussed for the anterior dentition, the anterior two premolars, P3, and the lower molars. Further evidence is presented to corroborate the identification of the anterior two premolars in the adult as dP1 and dP2, based on the relative retardation of their initiation and their lack of successor tooth germs. This developmental heterochrony has probably occurred in all three-premolared marsupials.     

Innervation of the human upper primary dentition: Implications for understanding tooth initiation and rethinking growth and eruption patterns

Recent comparisons of humans with apes and early fossil hominids have prompted renewed interest in the study of sequences of dental growth and development. Such comparisons, however, rely on certain assumptions about tooth development and dental homology and the biological reality of distinguishing “deciduous” from “permanent” teeth. In light of earlier suggestions by Schwartz that there might be a correlation between nerves and the stem progenitors of tooth classes, and thus between nerve branch number and number of tooth classes, we studied a large sample of ～ 3 month fetuses to elucidate the nature of nerve branching patterns and the development of the primary dentition (i.e., the “deciduous” incisors, canine, and molars, and the first “permanent” molar). Contrary to expectation, variation in nerve branch patterning was the rule. If nerve fibers do have a role in tooth development, it can only be at the time of initiation, with definitive innervation occurring late in tooth development. In taking into consideration the entire span of tooth development—from initiation to innervation to eruption—and the process by which successional teeth arise (each from the external dental epithelium of a predecessor tooth), we suggest that dividing tooth growth and eruption into patterns of the “deciduous” teeth vs. those of the “permanent” is artificial and that a more meaningful approach would be the study of the entire dentition.     

Conservation and divergence of Bmp2a, Bmp2b, and Bmp4 expression patterns within and between dentitions of teleost fishes

The diversity of tooth location in teleost fishes provides an excellent system for comparing genetic divergence between teeth in different species (phylogenetic homologs) with divergence between teeth within one species (iterative homologs). We have chosen to examine the expression of three members of the bone morphogenetic protein (Bmp) family because they are known to play multiple roles in tooth development and evolution in tetrapod vertebrates. We characterized expression of Bmp2a, Bmp2b, and Bmp4 during the development of oral and pharyngeal dentitions in three species of teleost fishes, the zebrafish (Danio rerio), Mexican tetra (Astyanax mexicanus), and Japanese medaka (Oryzias latipes). We found that expression in teleosts is generally highly conserved, with minor differences found among both iteratively homologous and phylogenetically homologous teeth. Expression of orthologous genes differs in several ways between the teeth of teleost fishes and those of the mouse, but between these vertebrate groups the summed expression pattern of Bmp genes is highly conserved. Significantly, the toothless oral region of the zebrafish lacks Bmp expression domains found in teleosts with oral teeth, implicating these genes in evolutionary tooth loss. We conclude that Bmp expression has been largely conserved in vertebrate tooth development over evolutionary time, and that loss of Bmp expression is correlated with region-specific loss of the dentition in a major group of fishes.     

Early development and replacement of the stickleback dentition

Teeth have long served as a model system to study basic questions about vertebrate organogenesis, morphogenesis, and evolution. In nonmammalian vertebrates, teeth typically regenerate throughout adult life. Fish have evolved a tremendous diversity in dental patterning in both their oral and pharyngeal dentitions, offering numerous opportunities to study how morphology develops, regenerates, and evolves in different lineages. Threespine stickleback fish (Gasterosteus aculeatus) have emerged as a new system to study how morphology evolves, and provide a particularly powerful system to study the development and evolution of dental morphology. Here, we describe the oral and pharyngeal dentitions of stickleback fish, providing additional morphological, histological, and molecular evidence for homology of oral and pharyngeal teeth. Focusing on the ventral pharyngeal dentition in a dense developmental time course of lab‐reared fish, we describe the temporal and spatial consensus sequence of early tooth formation. Early in development, this sequence is highly stereotypical and consists of seventeen primary teeth forming the early tooth field, followed by the first tooth replacement event. Comparing this detailed morphological and ontogenetic sequence to that described in other fish reveals that major changes to how dental morphology arises and regenerates have evolved across different fish lineages. J. Morphol. 277:1072–1083, 2016. © 2016 Wiley Periodicals, Inc.     

Size and morphology of the permanent dentition in prehistoric Ohio Valley Amerindians.

Metric and morphological characterizations of the permanent teeth from a total of 155 prehistoric Amerindians are presented. The individuals represent samples from three Ohio Valley burial complexes (considered together as the Late Diffuse group): Glacial Kame, Adena and Ohio Hopewell. Metric data include common measures of central tendency and dispersion. From these measures estimates and analyses of the magnitude of sexual dimorphism and relative variability are presented as well as analyses of the patterns of these estimates. Forty morphological characters are also tabulated. The results indicate a number of provisional hypotheses: the generally larger tooth size of the Late Archaic Indian Knoll when compared to the Late Diffuse groups is consistent with the hypothesis of mitigated selective pressures in more technologically advanced groups; although tooth size is smaller in the Late Diffuse groups, dental morphology is as complex, or more so when compared to the Indian Knoll group. Since morphology and size do not covary exactly the biocultural forces resulting in smaller tooth size do not seem to act as strongly on dental morphology; odontological differences within the Late Diffuse arise primarily between the Glacial Kame-Adena and the Ohio Hopewell. These differences correspond to major biocultural changes in this area; although provisional hypotheses concerning odontological variability are erected, hypotheses concerning evolutionary trends must await the discovery of evolving lineages within these groups; similarities are noted among all compared groups including the pattern and magnitude of sexual dimorphism and relative variability. These parameters may be similar for all eastern Amerindians during this period; finally, the morphology of the deciduous dentition, which generally predicts that of the permanent teeth, is found to be less complex than the permanent teeth. This may be the result of a selective disadvantage for the individuals in the deciduous dentition sample which is reflected in the dentition.     

Development and Evolution of Dentition Pattern and Tooth Order in the Skates And Rays (Batoidea; Chondrichthyes)

Shark and ray (elasmobranch) dentitions are well known for their multiple generations of teeth, with isolated teeth being common in the fossil record. However, how the diverse dentitions characteristic of elasmobranchs form is still poorly understood. Data on the development and maintenance of the dental patterning in this major vertebrate group will allow comparisons to other morphologically diverse taxa, including the bony fishes, in order to identify shared pattern characters for the vertebrate dentition as a whole. Data is especially lacking from the Batoidea (skates and rays), hence our objective is to compile data on embryonic and adult batoid tooth development contributing to ordering of the dentition, from cleared and stained specimens and micro-CT scans, with 3D rendered models. We selected species (adult and embryonic) spanning phylogenetically significant batoid clades, such that our observations may raise questions about relationships within the batoids, particularly with respect to current molecular-based analyses. We include developmental data from embryos of recent model organisms Leucoraja erinacea and Raja clavata to evaluate the earliest establishment of the dentition. Characters of the batoid dentition investigated include alternate addition of teeth as offset successional tooth rows (versus single separate files), presence of a symphyseal initiator region (symphyseal tooth present, or absent, but with two parasymphyseal teeth) and a restriction to tooth addition along each jaw reducing the number of tooth families, relative to addition of successor teeth within each family. Our ultimate aim is to understand the shared characters of the batoids, and whether or not these dental characters are shared more broadly within elasmobranchs, by comparing these to dentitions in shark outgroups. These developmental morphological analyses will provide a solid basis to better understand dental evolution in these important vertebrate groups as well as the general plesiomorphic vertebrate dental condition.     

Gene deployment for tooth replacement in the rainbow trout (Oncorhynchus mykiss): a developmental model for evolution of the osteichthyan dentition

Repeated tooth initiation occurs often in nonmammalian vertebrates (polyphyodontism), recurrently linked with tooth shedding and in a definite order of succession. Regulation of this process has not been genetically defined and it is unclear if the mechanisms for constant generation of replacement teeth (secondary dentition) are similar to those used to generate the primary dentition. We have therefore examined the expression pattern of a sub-set of genes, implicated in tooth initiation in mouse, in relation to replacement tooth production in an osteichthyan fish (Oncorhynchus mykiss). Two epithelial genes pitx2, shh and one mesenchymal bmp4 were analyzed at selected stages of development for O. mykiss. pitx2 expression is upregulated in the basal outer dental epithelium (ODE) of the predecessor tooth and before cell enlargement, on the postero-lingual side only. This coincides with the site for replacement tooth production identifying a region responsible for further tooth generation. This corresponds with the expression of pitx2 at focal spots in the basal oral epithelium during initial (first generation) tooth formation but is now sub-epithelial in position and associated with the dental epithelium of each predecessor tooth. Co-incidental expression of bmp4 and aggregation of the mesenchymal cells identifies the epithelial-mesenchymal interactions and marks initiation of the dental papilla. These together suggest a role in tooth site regulation by pitx2 together with bmp4. Conversely, the expression of shh is confined to the inner dental epithelium during the initiation of the first teeth and is lacking from the ODE in the predecessor teeth, at sites identified as those for replacement tooth initiation. Importantly, these genes expressed during replacement tooth initiation can be used as markers for the sites of "set-aside cells," the committed odontogenic cells both epithelial and mesenchymal, which together can give rise to further generations of teeth. This information may show how initial pattern formation is translated into secondary tooth replacement patterns, as a general mechanism for patterning the vertebrate dentition. Replacement of the marginal sets of teeth serves as a basis for discussion of the evolutionary significance, as these dentate bones (dentary, premaxilla, maxilla) form the restricted arcades of oral teeth in many crown-group gnathostomes, including members of the tetrapod stem group.     

Expression of Dlx genes during the development of the zebrafish pharyngeal dentition: evolutionary implications

In order to investigate similarities and differences in genetic control of development among teeth within and between species, we determined the expression pattern of all eight Dlx genes of the zebrafish during development of the pharyngeal dentition and compared these data with that reported for mouse molar tooth development. We found that (i) dlx1a and dlx6a are not expressed in teeth, in contrast to their murine orthologs, Dlx1 and Dlx6; (ii) the expression of the six other zebrafish Dlx genes overlaps in time and space, particularly during early morphogenesis; (iii) teeth in different locations and generations within the zebrafish dentition differ in the number of genes expressed; (iv) expression similarities and differences between zebrafish Dlx genes do not clearly follow phylogenetic and linkage relationships; and (v) similarities and differences exist in the expression of zebrafish and mouse Dlx orthologs. Taken together, these results indicate that the Dlx gene family, despite having been involved in vertebrate tooth development for over 400 million years, has undergone extensive diversification of expression of individual genes both within and between dentitions. The latter type of difference may reflect the highly specialized dentition of the mouse relative to that of the zebrafish, and/or genome duplication in the zebrafish lineage facilitating a redistribution of Dlx gene function during odontogenesis.     

Involvement of the Reck tumor suppressor protein in maternal and embryonic vascular remodeling in mice

Background

The accessibility of the developing zebrafish pharyngeal dentition makes it an advantageous system in which to study many aspects of tooth development from early initiation to late morphogenesis. In mammals, hedgehog signaling is known to be essential for multiple stages of odontogenesis; however, potential roles for the pathway during initiation of tooth development or in later morphogenesis are incompletely understood.

Results

We have identified mRNA expression of the hedgehog ligands shha and the receptors ptc1 and ptc2 during zebrafish pharyngeal tooth development. We looked for, but did not detect, tooth germ expression of the other known zebrafish hedgehog ligands shhb, dhh, ihha, or ihhb, suggesting that as in mammals, only Shh participates in zebrafish tooth development. Supporting this idea, we found that morphological and gene expression evidence of tooth initiation is eliminated in shha mutant embryos, and that morpholino antisense oligonucleotide knockdown of shha, but not shhb, function prevents mature tooth formation. Hedgehog pathway inhibition with the antagonist compound cyclopamine affected tooth formation at each stage in which we applied it: arresting development at early stages and disrupting mature tooth morphology when applied later. These results suggest that hedgehog signaling is required continuously during odontogenesis. In contrast, over-expression of shha had no effect on the developing dentition, possibly because shha is normally extensively expressed in the zebrafish pharyngeal region.

Conclusion

We have identified previously unknown requirements for hedgehog signaling for early tooth initiation and later morphogenesis. The similarity of our results with data from mouse and other vertebrates suggests that despite gene duplication and changes in the location of where teeth form, the roles of hedgehog signaling in tooth development have been largely conserved during evolution.     

Early development of rostrum saw-teeth in a fossil ray tests classical theories of the evolution of vertebrate dentitions

In classical theory, teeth of vertebrate dentitions evolved from co-option of external skin denticles into the oral cavity. This hypothesis predicts that ordered tooth arrangement and regulated replacement in the oral dentition were also derived from skin denticles. The fossil batoid ray Schizorhiza stromeri (Chondrichthyes; Cretaceous) provides a test of this theory. Schizorhiza preserves an extended cartilaginous rostrum with closely spaced, alternating saw-teeth, different from sawfish and sawsharks today. Multiple replacement teeth reveal unique new data from micro-CT scanning, showing how the ‘cone-in-cone’ series of ordered saw-teeth sets arrange themselves developmentally, to become enclosed by the roots of pre-existing saw-teeth. At the rostrum tip, newly developing saw-teeth are present, as mineralized crown tips within a vascular, cartilaginous furrow; these reorient via two 90° rotations then relocate laterally between previously formed roots. Saw-tooth replacement slows mid-rostrum where fewer saw-teeth are regenerated. These exceptional developmental data reveal regulated order for serial self-renewal, maintaining the saw edge with ever-increasing saw-tooth size. This mimics tooth replacement in chondrichthyans, but differs in the crown reorientation and their enclosure directly between roots of predecessor saw-teeth. Schizorhiza saw-tooth development is decoupled from the jaw teeth and their replacement, dependent on a dental lamina. This highly specialized rostral saw, derived from diversification of skin denticles, is distinct from the dentition and demonstrates the potential developmental plasticity of skin denticles.     

Dental ontogeny of a white shark embryo

Unlike most viviparous vertebrates, lamniform sharks develop functional teeth during early gestation. This feature is considered to be related to their unique reproductive mode where the embryo grows to a large size via feeding on nutritive eggs in utero. However, the developmental process of embryonic teeth is largely uninvestigated. We conducted X‐ray microcomputed tomography to observe the dentitions of early‐, mid‐, and full‐term embryos of the white shark Carcharodon carcharias (Lamniformes, Lamnidae). These data reveal the ontogenetic change of embryonic dentition of the species for the first time. Dentition of the early‐term embryos (∼45 cm precaudal length, PCL) is distinguished from adult dentition by 1) the presence of microscopic teeth in the distalmost region of the paratoquadrate, 2) a fang‐like crown morphology, and 3) a lack of basal concavity of the tooth root. The “intermediate tooth” of early‐term embryos is almost the same size as the adjacent teeth, suggesting that lamnoid‐type heterodonty (lamnoid tooth pattern) has not yet been established. We also discovered that mid‐term embryos (∼80 cm PCL) lack functional dentition. Previous studies have shown that the maternal supply of nutritive eggs in lamnoid sharks ceases during mid‐ to late‐gestation. Thus, discontinuation of functional tooth development is likely associated with the completion of the oophagous (egg‐eating) phase. Replacement teeth in mid‐term embryos include both embryonic and adult‐type teeth, suggesting that the embryo to adult transition in dental morphology occurs during this period. J. Morphol. 278:215–227, 2017. © 2016 Wiley Periodicals,Inc.     

Adaptation to hard-object feeding in sea otters and hominins

The large, bunodont postcanine teeth in living sea otters (Enhydra lutris) have been likened to those of certain fossil hominins, particularly the ’robust’ australopiths (genus Paranthropus). We examine this evolutionary convergence by conducting fracture experiments on extracted molar teeth of sea otters and modern humans (Homo sapiens) to determine how load-bearing capacity relates to tooth morphology and enamel material properties. In situ optical microscopy and x-ray imaging during simulated occlusal loading reveal the nature of the fracture patterns. Explicit fracture relations are used to analyze the data and to extrapolate the results from humans to earlier hominins. It is shown that the molar teeth of sea otters have considerably thinner enamel than those of humans, making sea otter molars more susceptible to certain kinds of fractures. At the same time, the base diameter of sea otter first molars is larger, diminishing the fracture susceptibility in a compensatory manner. We also conduct nanoindentation tests to map out elastic modulus and hardness of sea otter and human molars through a section thickness, and microindentation tests to measure toughness. We find that while sea otter enamel is just as stiff elastically as human enamel, it is a little softer and tougher. The role of these material factors in the capacity of dentition to resist fracture and deformation is considered. From such comparisons, we argue that early hominin species like Paranthropus most likely consumed hard food objects with substantially higher biting forces than those exerted by modern humans.     

Plate-like permanent dental laminae of upper jaw dentition in adult gobiid fish, Sicyopterus japonicus

Sicyopterus japonicus (Teleostei, Gobiidae) possesses a unique upper jaw dentition different from that known for any other teleosts. In the adults, many (up to 30) replacement teeth, from initiation to attachment, are arranged orderly in a semicircular-like strand within a capsule of connective tissue on the labial side of each premaxillary bone. We have applied histological, ultrastructural, and three-dimensional imaging from serial sections to obtain insights into the distribution and morphological features of the dental lamina in the upper jaw dentition of adult S. japonicus. The adult fish has numerous permanent dental laminae, each of which is an infolding of the oral epithelium at the labial side of the functional tooth and forms a thin plate-like structure with a wavy contour. All replacement teeth of a semicircular-like strand are connected to the plate-like dental lamina by the outer dental epithelium and form a tooth family; neighboring tooth families are completely separated from each other. The new tooth germ directly buds off from the ventro-labial margin of the dental lamina, whereas no distinct free end of the dental lamina is present, even adjacent to this region. Cell proliferation concentrated at the ventro-labial margin of the dental lamina suggests that this region is the site for repeated tooth initiation. During tooth development, the replacement tooth migrates along a semicircular-like strand and eventually erupts through the dental lamina into the oral epithelium at the labial side of the functional tooth. This unique thin plate-like permanent dental lamina and the semicircular-like strand of replacement teeth in the upper jaw dentition of adult S. japonicus probably evolved as a dental adaptation related to the rapid replacement of teeth dictated by the specialized feeding habit of this algae-scraping fish.     

Tooth morphology of Notosuchus terrestris (Notosuchia: Mesoeucrocodylia): New evidence and implications

Notosuchia is a large and diverse group of Crocodyliforms, characterized, among other features, by a heterodont dentition. New information on the tooth anatomy of Notosuchus terrestris is presented, based on well-preserved specimens from the Late Cretaceous of Patagonia (southern Argentina). This allows a complete characterization of its dental anatomy (composed by incisiviform, caniniform, and molariform teeth) that includes autapomorphic features and derived features shared with Sphagesaurus and Mariliasuchus. This includes the extensive wear facets in molariforms, indicative of tooth–tooth occlusion and a sharp keel that bears rounded denticles. Notosuchus also shares with Mariliasuchus the presence of a tooth with a transitional morphology located at the premaxilla–maxilla contact and the absence of interalveolar septa in the entire premaxillary and maxillary dentition.     

Vertebrate dentitions at the origin of jaws: when and how pattern evolved

New evidence shows that teeth evolved with a greater degree of independence from jaws than previously considered. Pharyngeal denticles occur in jawless fish and also in early gnathostomes and precede jaw teeth in phylogeny. Many of these denticles form joined polarized sets on each branchial arch; these resemble whorl-shaped tooth sets on the jaws of stem and crown gnathostomes and are proposed as homologous units. Therefore, the source of patterning of these pharyngeal denticle and tooth sets is conserved from jawless conditions. It is proposed that developmental regulatory systems, responsible for all such tooth patterns on the jaws, are co-opted from the pharyngeal region and not from the skin as classically understood. This strongly implicates embryonic endoderm as opposed to ectoderm in the genetic control of dentition patterning. New interpretations of ontogenetic data on patterning dentitions of extant sharks are proposed, together with those of osteichthyan fish. Two entirely fossil groups, placoderms and acanthodians, at the base of gnathostome phylogeny are reassessed on the basis of a new model. It is concluded that within stem group and crown group gnathostomes several different strategies, unique to each taxon, were adopted to produce different developmental models of dentition patterning from pharyngeal denticles. One shared developmental pattern is that of initiation from primordial tooth sites, independently in each dentate zone of the jaws. The new model is proposed as a framework for data on evolutionary developmental genetics.