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.     

Ontogenetic Tooth Reduction in Stenopterygius quadriscissus (Reptilia: Ichthyosauria): Negative Allometry,Changes in Growth Rate,and Early Senescence of the Dental Lamina

We explore the functional, developmental, and evolutionary processes which are argued to produce tooth reduction in the extinct marine reptile Stenopterygius quadriscissus (Reptilia: Ichthyosauria). We analyze the relationship between mandible growth and tooth size, shape, and count, to establish an ontogenetic trend. The pattern in S. quadriscissus is consistent with hypotheses of tooth size reduction by neutral selection, and this unusual morphology (a functionally edentulous rostrum) was produced by a series of different evolutionary developmental changes that are known for other taxa showing tooth reduction and loss. Specifically, this species evolved functional edentulism by evolutionary changes in the growth allometry of the dentition and by altering growth rates through ontogeny. This observation supports previous hypotheses that S. quadriscissus underwent ontogenetic tooth reduction. Tooth reduction in S. quadriscissus may be caused by unique selective pressures resulting from prey choice and feeding behavior, expanding our current understanding of the mechanisms producing tooth reduction.     

Characteristics of dentition in gekkonid lizards of the genus <Emphasis Type="Italic">Teratoscincus</Emphasis> and other Gekkota (Sauria,Reptilia)

The dentition and tooth crown microstructure of gekkonids and eublepharids are examined. Scanning electron microscopy shows that the lingual surface of teeth in these lizards has one, two, or, occasionally, several cusps separated by grooves. The teeth of geckoes usually have two (lingual and labial) cusps in the apical region. With respect to the number of teeth, the majority of Gekkota fall into two groups. The first includes a few species with many teeth (50 or more) in the dentary and maxilla, the eublepharids Goniurosaurus and Aeluroscalabotes, and the gekkonid Cyrtopodion louisiadensis. The second group, comprising most of the species, is subdivided into two subgroups, species with 20–30 or 30–40 teeth in jaw bones. Teratoscincus belongs to the first subgroup of the second group.     

The plagiosaurid temnospondyl Plagiosuchus pustuliferus (Amphibia: Temnospondyli) from the Middle Triassic of Germany: anatomy and functional morphology of the skull

The cranial anatomy of the plagiosaurid temnospondyl Plagiosuchus pustuliferus, from the Middle Triassic of Germany, is described in detail on the basis of a newly discovered skull and mandibular material. The highly derived skull is characterized by huge orbitotemporal fenestrae, a reduction of the circumorbital bones – the prefrontal, postfrontal and (probably) postorbital are lost – and the expansion of the jugal to occupy most of the lateral skull margin. Ventrally the extremely long subtemporal vacuities correlate with the elongate adductor fossa of the mandible. The dentition is feebly developed on both skull and mandible. Ossified ?ceratobranchials and ‘branchial denticles’ indicate the presence of open gills clefts in life. The remarkably divergent cranial morphology of P. pustuliferus highlights the extraordinary cranial diversity within the Plagiosauridae, probably unsurpassed within the Temnospondyli. Specific structural aspects of the skull – including an extremely short marginal tooth row, feeble dentition and an elongated chamber for adductor musculature – together with evidence for a hyobranchial skeleton, suggests that P. pustuliferus utilized directed suction feeding for prey capture. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155 , 348–373.     

Variability in the number of tooth rows in the pharyngeal dentition of Barbus intermedius (Teleostei; Cyprinidae): genetic,hormonal and environmental factors

The variability of pharyngeal dentition in a natural population of B. intermedius and effects of genetic, hormonal and environmental factors on the number of tooth rows in the pharyngeal dentition in offspring from wild‐caught parents have been investigated. It was revealed that: (i) about 10% of fish from natural population have four‐rowed dentition instead of three‐rowed dentition characteristic for this species; (ii) the presence of the additional tooth row is not an abnormality of tooth replacement since it occurs symmetrically on both sides; (iii) occurrence of the fourth row of teeth is heritable since laboratory‐reared offspring from parents with four‐rowed dentition have the same dentition. Even if one of the parents had four‐rowed dentition the percentage of four‐rowed individuals in the progeny was significantly higher than in progeny from parents with normal (three rowed) dentition; (iv) the number of tooth rows appears to be hormonally controlled: high levels of thyroid hormone result in a decrease in the number of tooth rows to two. In contrast, deficiency of this hormone results in an increase to four rows; (v) no differences in the number of tooth rows were found in fish reared under 17°C, 24°C, 30°C and room temperature (20–26°C).     

First evidence of the tooth eruption sequence of the upper jaw in Hyaenodon (Hyaenodontidae,Mammalia) and new information on the ontogenetic development of its dentition

Juvenile material with the main focus on the upper jaw of the fossil predator Hyaenodon was evaluated to study the tooth eruption sequence and to examine the ontogeny of its dentition in detail. The comparison in size of milk to permanent teeth indicates a growth rate of 12–16 % in Hyaenodon. The thin section of a deciduous canine of a North American taxon shows four dental rings. Based on the knowledge of recent carnivores, this implies an age of 3–4 years in the last stage of tooth eruption and thus a long juvenile phase. The mandibles ascertained the most recent established tooth eruption sequence for North American and European species. For the first time ever, juvenile material from Asia is documented and interpreted. This study likewise shows a difference in the sequence of the upper jaw: the first upper premolar erupts before the first upper molar in North American species, whereas the European taxa show an earlier eruption of the first upper molar. This fact further confirms the divergence between the Hyaenodon lineages from North America and Europe.     

New observations on the anatomy and paleobiology of the Eocene requiem shark 2Eogaleus bolcensis (Carcharhiniformes,Carcharhinidae) from Bolca Lagerstätte,Italy

Here we provide new information about the anatomy of the extinct shark 2Eogaleus bolcensis from the early Eocene Bolca Konservat-Lagerstätte. The combination of morphological and dental characters of the three known articulated specimens and a single isolated tooth collected from the Pesciara and Monte Postale sites (e.g., head bulky with rounded snout, pectoral fins of semiplesodic type, cutting-clutching dentition, dermal denticles shell-shaped and of drag-reducing type, caudal fin accounting for one fourth of the entire body length, 135–153 vertebrae) supports the assignment of 2Eogaleus to the family Carcharhinidae and allows us to confirm definitively its distinct taxonomic status from the sympatric carcharhiniform, the triakid 2Galeorhinus cuvieri. Moreover, the analysis of the dermal denticle morphology and the size and maturity age estimates of the studied specimens provide new paleobiological information about 2Eogaleus, suggesting a close association of this small top predator with the tropical shallow-water marine context hypothesized for the Bolca paleobiotopes.     

Unique dentition of rhynchosaurs and their two-phase success as herbivores in the Triassic

Rhynchosaurs were key herbivores over much of the world in the Middle and Late Triassic, often dominating their faunas ecologically, and much of their success may relate to their dentition. They show the unique ankylothecodont mode of tooth implantation, with deep roots embedded in the bone of the jaw and low crowns that were rapidly worn down in use. During growth, the main area of oral food processing, located in the middle and posterior portions of the occlusal surfaces of the jaws, moved posteriorly relative to the anterior tips of the jaws, which curved up. As the maxilla and dentary grew by addition of new bone posteriorly, the dental lamina fed in new teeth at the back of the tooth rows. CT scanning of the holotype skull of Bentonyx sidensis from the Middle Triassic of England reveals previously concealed details of the dentition. Together with new dentary material from the same location, this has enabled us to examine the tooth replacement process and elucidate ontogenetic changes in dentition and jaw morphology as the animals aged. There were major changes in rhynchosaur anatomy and function through their evolutionary history, with the early forms of the Middle Triassic dying out before or during the Carnian Pluvial Episode (233–232 Ma), and the subclade Hyperodapedontinae, with broad skulls and adaptations to chop tough vegetation, subsequently diversifying worldwide in a successful ecological expansion until their global extinction 227–225 Ma.     

Anatomy and cranial functional morphology of the small-bodied dinosaur Fruitadens haagarorum from the Upper Jurassic of the USA

Background

Heterodontosaurids are an important but enigmatic and poorly understood early radiation of ornithischian dinosaurs. The late-surviving heterodontosaurid Fruitadens haagarorum from the Late Jurassic (early Tithonian) Morrison Formation of the western USA is represented by remains of several small (<1 metre total body length, <1 kg body mass) individuals that include well-preserved but incomplete cranial and postcranial material. Fruitadens is hypothesized to represent one of the smallest known ornithischian dinosaurs.

Methodology/Principal Findings

We describe the cranial and postcranial anatomy of Fruitadens in detail, providing comparisons to all other known heterodontosaurid taxa. High resolution micro-CT data provides new insights into tooth replacement and the internal anatomy of the tooth-bearing bones. Moreover, we provide a preliminary functional analysis of the skull of late-surviving heterodontosaurids, discuss the implications of Fruitadens for current understanding of heterodontosaurid monophyly, and briefly review the evolution and biogeography of heterodontosaurids.

Conclusions/Significance

The validity of Fruitadens is supported by multiple unique characters of the dentition and hindlimb as well as a distinct character combination. Fruitadens shares highly distinctive appendicular characters with other heterodontosaurids, strengthening monophyly of the clade on the basis of the postcranium. Mandibular morphology and muscle moment arms suggest that the jaws of late-surviving heterodontosaurids, including Fruitadens, were adapted for rapid biting at large gape angles, contrasting with the jaws of the stratigraphically older Heterodontosaurus, which were better suited for strong jaw adduction at small gapes. The lack of wear facets and plesiomorphic dentition suggest that Fruitadens used orthal jaw movements and employed simple puncture-crushing to process food. In combination with its small body size, these results suggest that Fruitadens was an ecological generalist, consuming select plant material and possibly insects or other invertebrates.     

Evolution of tooth crown shape in Mesozoic birds,and its adaptive significance with respect to diet

Both the evolution of tooth morphology and the relationship between dental features and diet in toothed birds have long been studied. Here we quantify variation in tooth crown shape in 28 key Mesozoic bird species, and examine differences in dental morphology among birds belonging to different taxonomic groupings and inferred to have had different diets. Using geometric morphometric methods (GMM) and phylogenetic comparative methods (PCM), we found few clear differences in tooth crown shape between different taxonomic and ecological categories, and our analysis provides little support for many dietary inferences drawn in previous studies. However, the Solnhofen Archaeopteryx, Jeholornis, Protopteryx, Pengornis, Longipteryx, Tianyuornis, Mengciusornis, Ichthyornis and Hesperornis all were found to possess relatively specialized tooth crown shapes, perhaps reflecting specialized diets such as insectivory, granivory, piscivory and consumption of soft-shelled arthropods. Similarity in tooth crown shape across many Mesozoic birds may indicate the lack of dietary specialization, and the association between tooth form and diet may have been weakened in any case by ‘functional replacement’ of the dentition by a horny beak and, in many cases, gastroliths.     

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.     

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.     

WNT10A variants are associated with non-syndromic tooth agenesis in the general population

Tooth agenesis is the most common developmental dental anomaly. Absence of one or two permanent teeth is found in the majority of affected subjects. Very few patients suffer severe tooth agenesis. Recent studies revealed that WNT10A gene mutations caused syndromic and isolated severe tooth agenesis. In this study, to determine the contribution of WNT10A variants in different severities of tooth agenesis, we investigated the association between WNT10A variants and non-syndromic tooth agenesis in a Chinese population consisting of 505 tooth agenesis patients and 451 normal controls. Twenty-three novel non-synonymous variants were identified. WNT10A variants were detected in 15.8 % (75/474) of patients with 1–3 missing teeth and 51.6 % (16/31) of patients with 4 or more missing teeth. As compared with a frequency of 3.1 % in individuals with full dentition, variant allele frequencies were significantly elevated in both groups with tooth agenesis (p values of 1.00 × 10^?6 and 3.89 × 10^?23, respectively). Our findings showed that WNT10A variants were associated with non-syndromic tooth agenesis from mild to severe tooth agenesis, and the more severe tooth agenesis, the stronger association. Biallelic genotypes of WNT10A variants may have a pathogenic effect on tooth development. Presence of a single variant allele would be predisposing for causation with low penetrance. Together with WNT10A variant, there should be other genetic or environmental factors leading to biallelic variant-related variable clinical manifestations and single allele variant-related low penetrance. The frequent missing tooth positions in the WNT10A-related cases were consistent with that in the general population, suggesting WNT10A plays a critically important role in the etiology of general tooth agenesis.     

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.     

Development of the pharyngeal teeth in the big head,Aristichthys nobilis (Cyprinidae)

The development of pharyngeal dentition was observed in the big head,Aristichthys nobilis, which is one of the hypophthalmichthyines of the cyprinids. This fish has the C-type larval dentition, in which no teeth ever occur at the position An3, and in which the first tooth at the position An2 is on the third replacement wave. So the positions Pol, Ce0, Ani and An2 in the larval dentition correspond to the positions A4, A3, A2 and A1 in the adult dentition, respectively. The initial tooth at each position is a conical one. The conical teeth are then changed to ones bearing a narrow grinding surface with a hook at the tip and some denticles on the margins. These teeth are of theLeuciscus stage. Tn the following teeth, the grinding surface is expanded, and the denticles are increased in number and distributed on not only the margins but also the whole grinding surface. These teeth bearing a very broad grinding surface characterize the hypophthalmichthyines. At the positions A2 to A4, the teeth become the hypophthalmichthyine type in the larval period. But the tooth at the position A1 becomes the hypophthalmichthyine type in the juvenile period. The morphological change of teeth in this species is simple although their teeth are highly specialized. We think that this phenomenon gives a hint on their phylogeny.     

Tooth germ initiation patterns in a developing dentition: An in vivo study of Xenopus laevis tadpoles

The transparency of soft tissue in Xenopus laevis tadpoles and the anterior‐posterior orientation of their developing tooth germs in the upper jaw offer a unique opportunity for the in vivo charting of the first 15–20 days of the developing dentition. Twenty‐two X. laevis tadpoles were anesthetized daily and their mouths opened to record the first appearance, position, and development of tooth germs in the upper jaw. The initiation patterns revealed considerable variability between animals, and even between the jaw quadrants in the same animal. This variability appears within a structural boundary and the results are consistent with the presence of an odontogenic band. The final length of dental rows far exceeded the jaw growth for each quadrant during the recording period. This in vivo investigation underlines the limits of cross‐sectional studies, and in particular the assumption that tooth germs initiate at the same position in the dental row. The tooth germ initiation patterns in this study did not align with the predictions of standard models for the development of the dentition—Zahnreihen, Clone, and New Progress Zone theories.     

Differences in developmental potential predict the contrasting patterns of dental diversification in characiform and cypriniform fishes

Morphological diversification during adaptive radiation may depend on factors external or internal to the lineage. We provide evidence for the latter in characiform fishes (tetras and piranhas), which exhibit extensive dental diversity. Phylogenetic character mapping supported regain of lost teeth as contributing to this diversity. To test for latent potential for dentition that would facilitate its evolutionary expansion, we overexpressed a tooth initiation signal, the tumour necrosis factor pathway ligand ectodysplasin, in a model characiform, the Mexican tetra (Astyanax mexicanus). This manipulation resulted in extensive ectopic dentition, in contrast with its previously reported limited effect in the zebrafish (Danio rerio). Tooth location in the order Cypriniformes, to which the zebrafish belongs, is much more restricted than in characiforms, a pattern that may be explained by differences in the retention of ancestral developmental potential. Our results suggest that differences in evolvability between lineages may lead to contrasting patterns of diversification.     

Über die Bezahnung desOrthacanthus (Chondrichthyes: Xenacanthida; Oberkarbon - Unterperm)

The following features of the Permo-Carbonif erous xenacanthid sharkOrthacanthus sen- ckenhergianus are described for the first time:

—The blood and nerve supply system of the tooth root is comprised of two parallel, labio-lingually arranged main channels connected with a mesio-distally directed cavity below the crown. The nutrition of the median cuspule is separated from this vascular system.

—The dentition can be divided into symphyseal teeth, anterior teeth, lateral teeth, and posterior teeth. They vary in height and inclination of the cusps. No difference in dentition between upper and lower jaw can be shown.