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Comparative phylogeny of tooth replacement modes in toothed vertebrate clades. A. the shark dentition (elasmobranchs) continuously regenerates throughout life (polyphyodont) with a many-for-one mechanism (many teeth made in advance of function for each functional tooth position in the jaw). B. Bony fishes offer a diverse range of tooth replacement mechanisms, with continuous replacement with a one-for-one system (e.g. cichlid fishes, in B (Fraser et al., 2013); one replacement tooth made in advance of function for each functional position), although a many-for-one system is observed in many bony fish species. C. Reptiles show a range of diverse mechanisms for tooth replacement with a continuous polyphyodont system in some species e.g. the snake, in C (with some species showing a more restricted dentition without replacement (monophyodont; e.g. chamealeon; Buchtová et al. 2013). D. The mammalian dentition also offers a range of diverse replacement or renewal phenotypes from monophyodont mammals e.g. mice, where the only regenerative potential is observed in the continuously growing incisor (Di), and molars are never replaced. In most mammals the dentition is diphyodont with two tooth generations e.g. humans (D). A phylogenetic reduction of tooth generations are generally observed toward more higher vertebrates i.e. mammals.
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The evolution of oral teeth is considered a major contributor to the overall success of jawed vertebrates. This is especially apparent in cartilaginous fishes including sharks and rays, which develop elaborate arrays of highly specialized teeth, organized in rows and retain the capacity for life-long regeneration. Perpetual regeneration of oral tee...
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... consistent with an OB and comparable to those in chondrichthyans[3], teleosts[1,34], ...
Teeth have been a prominent feature of most vertebrates for 400 million years, and the core regulatory network underlying embryonic tooth formation is deeply conserved from fishes to amniotes. In frogs, however, odontogenesis is delayed, occurring instead during the postembryonic metamorphosis. Nearly all adult frogs have teeth on the upper jaw and lack lower jaw dentition, but a single species re-evolved mandibular teeth. Developmental-genetic mechanisms that underlie tooth formation in frogs are poorly understood, including whether an ancestral program is partially retained in the lower jaw that could facilitate the evolutionary reappearance of lost mandibular teeth. Using a developmental series of an unconventional model species, we assessed 1) if the gene network underlying odontogenic competence is conserved in the late-forming teeth of frogs; 2) if unique keratinized mouthparts, which function as an alternative feeding tool in anuran larvae, impede tooth induction; and 3) if transient tooth rudiments form in the anuran mandible. The tooth development network is conserved in the frog upper jaw, which displays dental expression patterns comparable to those of other vertebrates. There is, however, no evidence of tooth development in the mandible. Teeth emerge before keratinized mouthparts degenerate, but their location may be spatially constrained by keratin, and gene expression patterns of keratinized mouthparts and teeth overlap. We hypothesize that the novel mouthparts of tadpoles did not arise de novo but instead originated by partially co-opting the developmental program that typically mediates true tooth development.
... The teeth of chondrichthyans are their most important feature for capturing and processing prey and to keep long functionality, teeth are constantly replaced in modern sharks [41][42][43]. This polyphyodonty (constant replacement of teeth) is plesiomorphic within chondrichthyans [39,107,108]. Tooth replacement can be achieved in two different ways. Either the post-functional tooth is retained and moves beneath the skin on the outside of the head as exhibited by cladodonts [44], or the teeth are shed and replaced, as by neoselachians [41][42][43]. ...
Devonian ctenacanth chondrichthyans reached body sizes similar to modern great white sharks and therefore might have been apex predators of the Devonian seas. However, very little is known about the diet and feeding behaviours of these large ancestral sharks. To reconstruct their ecological properties, teeth of the large Famennian (Late Devonian) chondrichthyan Ctenacanthus concinnus from the Anti-Atlas, Morocco, were analysed. The teeth show strong tooth wear with deep horizontal as well as vertical scratches. Dental microwear texture analysis, a well-established method for the reconstruction of diet and commonly used in terrestrial vertebrates, was applied for the first time, to our knowledge, to Palaeozoic vertebrates in this study. Furthermore, finite element analysis was performed to test the biomechanical properties of the teeth. By combining both analyses, as well as palaeoenvironmental data and tooth morphology, we demonstrate that the results from only one method can be insufficient and misleading. Ctenacanthus concinnus most likely was an opportunistic feeder like many modern sharks. Direct evidence and the results of our analyses suggest that Ctenacanthus fed on ectocochleate cephalopods, other chondrichthyans and further vertebrates using a combination of head movements including lateral head shaking to cut large prey items.
... Like mammals, sharks exhibit conspicuous tooth morphological variation at different scales, from single tooth to dentition levels. Interestingly, this is not a recently evolved pattern, as heterodont arrangements of multicuspid teeth are described among the earliest sharks 19 .Albeit less studied as mammals, shark odontogenesis shares many central features with the former class, involving conserved regulatory pathways and developmental mechanisms [20][21][22] , besides notable differences 20,23 . Such deep similarities across long phylogenetic distances point towards a kernel of developmental mechanisms capable of generating highly diverse dental morphologies both between and within individuals, which has been explored experimentally and computationally [23][24][25] . ...
Sharks are notorious for their exceptional dental diversity, which is frequently used as a proxy for ecological function. However, functional inferences from morphology need to consider morphological features across different organizational scales, from small cusplets to patterns at the level of the entire jaw. Here, we deploy a set of classic and novel morphometric approaches to quantify morphological features ranging from sub-dental features to whole dentitions within a large ensemble of species encompassing all extant orders of sharks. We then correlate these measures with habitat, feeding and body size traits and track their variation as a function of genetic distance, a measure of trait adaptability. Intriguingly, sharks tend to either explore tooth-level or dentition-level complexity, resulting in two distinct groups with key differences in tooth symmetry, graduality of heterodont change, and depth of habitat. Overall, we find that intermediate levels of resolution, namely monognathic heterodonty in comparison with dignathic heterodonty and tooth-level shape descriptors, show the strongest predictive power for ecological traits, while exhibiting low phylogenetic signal, which suggests a more dynamic adaptability on shorter evolutionary timescales. This raises macro-evolutionary interpretations about the evolvability of nested modular phenotypic structures, with
likely important implications for paleo-ecological inferences from sequentially homologous traits.
... (Raja clavata; Fig. 1) are comparable to tooth development of other vertebrates. Indeed, the development of diverse epithelial appendages appears to be governed by a core set of genes (i.e., an odontode gene regulatory network; Tucker and Fraser, 2014;Debiais-Thibaud et al., 2015;Rasch et al., 2016Cooper et al., 2017, Berio andDebiais-Thibaud, 2019). ...
... This epithelial placode is characterized by the expression of genes such as shh (Fig. 5), paired-like homeodomain 1 (pitx1) and paired-like homeodomain 2 (pitx2) (Tucker and Fraser, 2014;Smith et al., 2009;Rasch et al., 2016). Neural crest cells presumably from either the cranial (i.e. ...
... denticles) contribute to the mesenchyme (Gillis et al., 2017), which condenses underneath and around the epithelial placode upon the expression of mesenchymal genetic markers such as β-catenin (ctnnb1), lymphoid enhancer binding factor 1 (lef1), paired box 9 (pax9), pitx2, and bmp4 (Fraser et al., 2010). Continuation of epithelial-mesenchymal interactions involving the Hedgehog (Hh), FGF and BMP pathways, within the placode, leads to proliferation of cells within the epithelium and mesenchyme causing outgrowth of the developing odontode ( Fig. 4B and F ;Fraser et al., 2010;Martin et al., 2016;Rasch et al., 2016;Cooper et al., 2018;Debiais--Thibaud et al., 2015). This marks the early stages of morphogenesis. ...
... In the herbivorous mammals, the dental adaptations to accessible eating regimens also archived, for example, a morphological transformation of a finish edge course of action or biting muscle size to amplify biting adequacy (Clauss et al. 2008;Fritz et al. 2009;Kaiser et al. 2010). The development of teeth is extremely planned in: mice (Balic and Thesleff 2015), fish (Rasch et al. 2016), or reptiles (Whitlock and Richman 2013). Bertin et al. 2018 explore recent research on tooth implantation, attachment, and replacement in amniotes, revealing evolutionary and developmental mechanisms and providing insights into tooth structure and function diversity across different species. ...
The study reveals a lack of histomorphogenesis in New Zealand white rabbit teeth. The teeth development was examined through sequential histological segments in 24 rabbits from prenatal ages (E19, E21, E23, E25, and E28), neonates (E30), and postnatal age (1 week and 2 weeks); (three animal specimens at each age stage). Rabbit teeth first appeared at 19 days of prenatal life (E19) as an ectodermal epithelial thickening on each side of the mouth opening. At E21, the bud of upper incisor tooth appeared as an epithelial bud, which composed of many condensed epithelium cells, was simply identified from the larger with less condensed vestibular lamina, and was surrounded by mesenchymal connective tissue while the lower incisor took the cap stage. At (E23), tooth regular construction is formed from enamel, dentine, and pulp cavity. Peg incisor appearance (supplementary and assistant incisors) is visible at the lingual surface of the upper major incisor. Teeth prenatal development went through successive stages like initiation, bud, cap, late bell, maturation, and crown stages. The first initiation phase of tooth formation was seen as ectodermal epithelial cell collection at (E19). Bud stage saw on upper incisor tooth, while in cap structure in lower incisor teeth at (E19). A cap-formed tooth is composed of the enamel organ and fundamentally dense mesenchymal tissue. Enamel organs are segmented into three distinct layers: the external tooth enamel epithelial, the internal tooth enamel epithelial, and finally the stellate reticular layer. The cement layer covered teeth all around on enamel on both the labial and lingual sides while not contacting the dentine on the lateral side, forming enamel space. Teeth develop consistently all through life; they have expanded enamel thickness; they are diphyodont teeth; they have two continuous dentitions; they are deciduous and perpetual, with long crown teeth and an open root.
... Whether regeneration is cyclic and programmed, or brought on by injury or wear, nearly all types of epithelial appendages undergo whole-organ regeneration (Cox et al., 2018;Finger and Barlow, 2021;Lin et al., 2013Lin et al., , 2021Plikus et al., 2008;Rocchi et al., 2021). Despite stark differences in their basic compositions as mature organs, different epithelial appendages demonstrate numerous developmental and genetic similarities, in some cases suggesting deep homology or even direct homology between subsets of these organs (Aman et al., 2018;Benton et al., 2019;Bloomquist et al., 2019;Debiais-Thibaud et al., 2011;Di-Poï and Milinkovitch, 2016;Fraser et al., 2010;Huysseune et al., 2009Huysseune et al., , 2022Martin et al., 2016;Pispa and Thesleff, 2003;Rasch et al., 2016;Sharpe, 2001;Sire et al., 2009;Wu et al., 2004). Given that most epithelial appendages exhibit whole-organ regeneration, we parsimoniously hypothesize that these regenerative processes are driven by shared genetic networks. ...
Most vertebrate species undergo tooth replacement throughout adult life. This process is marked by the shedding of existing teeth and the regeneration of tooth organs. However, little is known about the genetic circuitry regulating tooth replacement. Here, we tested whether fish orthologs of genes known to regulate mammalian hair regeneration have effects on tooth replacement. Using two fish species that demonstrate distinct modes of tooth regeneration, threespine stickleback (Gasterosteus aculeatus) and zebrafish (Danio rerio), we found that transgenic overexpression of four different genes changed tooth replacement rates in the direction predicted by a hair regeneration model: Wnt10a and Grem2a increased tooth replacement rate, whereas Bmp6 and Dkk2 strongly inhibited tooth formation. Thus, similar to known roles in hair regeneration, Wnt and BMP signals promote and inhibit regeneration, respectively. Regulation of total tooth number was separable from regulation of replacement rates. RNA sequencing of stickleback dental tissue showed that Bmp6 overexpression resulted in an upregulation of Wnt inhibitors. Together, these data support a model in which different epithelial organs, such as teeth and hair, share genetic circuitry driving organ regeneration.
... The sequential addition model presumed that the dental pattern is determined by an ancient regulatory network (Jernvall and Thesleff, 2000;Smith, 2003;Fraser et al. 2004Fraser et al. , 2009Smith et al. 2015;Rasch et al. 2016Rasch et al. , 2020 that is repeatedly deployed in multiple organs, including various epithelial appendages such as teeth, scales, feathers, hairs, glands, intestinal crypt villi and sensory organs (see Chapter 3 and 7). This conserved gene network, as has been tested thoroughly in sharks, not only mediates the morphogenesis and patterning of teeth, but also makes dermal odontodes to order (Cooper et al., 2018), as well as regulating the patterned rows of taste buds and ampullae of Lorenzini (Cooper et al. 2023). ...
n-situ tooth replacement is a major innovation of osteichthyans, but how it evolved remains elusive. Classic models have attempted to analyze the regulation of the alternate tooth replacement relying on untested assumptions. The idealized models, however, cannot explain the large number of deviations of normal and abnormal dental development in the reality, such as the gap-filling phenomenon that causes the split or fusion of tooth families. This chapter will summarize the process components that are shared by all the odontodes. Spatiotemporal developmental shifts between teeth and the underlying skeleton are one of the key factors. Such shifts create the potential for transitioning between various dental patterns and growth modes and for producing a great diversity of dentitions simply by heterochrony. As an example, the frequent initiation of teeth coupled with the space constraint of bone could have given rise to in-situ tooth replacement, without fundamental modifications at the molecular level.
... In the herbivorous mammals, the dental adaptations to accessible eating regimens also archived, for example, a morphological transformation of a nish edge course of action or biting muscle size to amplify biting adequacy [7][8][9]. The development of teeth is extremely planned in; mice [10], sh [11], or reptiles [12]. Concerning substitution [13]. ...
The study reveals that New Zealand white rabbit teeth do not exhibit histomorphogenesis. The teeth development was examined in 28 rabbits from prenatal ages (E19, E23, E25, and E28), neonates (E30), and postnatal age (one and fourteen days). Rabbit teeth first appeared at 19 days of prenatal life as an ectodermal epithelial thickening on each side of the mouth opening. At E23, tooth regular construction is framed from enamel, dentine, and pulp cavity. The peg incisor appearance is visible on the lingual surface of the upper major incisor. Teeth prenatal development went through successive stages like initiation, bud, cap, late bell, maturation, and crown stages. The teeth are composed of the enamel organ and dense mesenchymal tissue. Teeth develop consistently throughout life, having expanded enamel thickness, being diphyodont teeth, having two continuous dentitions, being deciduous and perpetual, with long crown teeth and an open root.
... Downregulation of Sox2 and Runx2 and activation of WNT signalling in the dental epithelium leads to the production of supernumerary teeth associated with the expansion of the dental lamina [151][152][153]. The heterochronic persistence of the dental lamina is observed in non-mammalian polyphyodonts [154,155] and could represent the underlying cause of the extremely rare cases of polyphyodonty in mammals [156,157]. ...
Mammals possess impressive craniofacial variation that mirrors their adaptation to diverse ecological niches, feeding behaviour, physiology and overall lifestyle. The spectrum of craniofacial geometries is established mainly during embryonic development. The formation of the head represents a sequence of events regulated on genomic, molecular, cellular and tissue level, with each step taking place under tight spatio-temporal control. Even minor variations in timing, position or concentration of the molecular drivers and the resulting events can affect the final shape, size and position of the skeletal elements and the geometry of the head. Our knowledge of craniofacial development increased substantially in the last decades, mainly due to research using conventional vertebrate model organisms. However, how developmental differences in head formation arise specifically within mammals remains largely unexplored. This review highlights three evolutionary mechanisms acknowledged to modify ontogenesis: heterochrony, heterotopy and heterometry. We present recent research that links changes in developmental timing, spatial organization or gene expression levels to the acquisition of species-specific skull morphologies. We highlight how these evolutionary modifications occur on the level of the genes, molecules and cellular processes, and alter conserved developmental programmes to generate a broad spectrum of skull shapes characteristic of the class Mammalia.
This article is part of the theme issue ‘The mammalian skull: development, structure and function’.
... In addition, teeth and denticles are documented across most of the vertebrate phylum (9)(10)(11), offering an opportunity to link developmental and phenotypic variation to macroevolutionary trends. However, the vast majority of studies has focused on mammalian tooth development, where many relevant genetic pathways and the mechanisms of their interaction with different tissues have hence been described (12)(13)(14)(15). ...
... However, the vast majority of studies has focused on mammalian tooth development, where many relevant genetic pathways and the mechanisms of their interaction with different tissues have hence been described (12)(13)(14)(15). Recently, research has begun unveiling features of tooth development in elasmobranchs, one of the phylogenetically most distant clades from mammals to exhibit important tooth variation (10,(16)(17)(18). Studying their dentitions might even provide a glimpse on how teeth emerged from ancestral, more general forms of ectodermal appendages, as elasmobranch integuments are covered by an array of tooth-like denticles (19). ...
Developmental complexity stemming from the dynamic interplay between genetic and biomechanic factors canalizes the ways genotypes and phenotypes can change in evolution. As a paradigmatic system, we explore how changes in developmental factors generate typical tooth shape transitions. Since tooth development has mainly been researched in mammals, we contribute to a more general understanding by studying the development of tooth diversity in sharks. To this end, we build a general, but realistic, mathematical model of odontogenesis. We show that it reproduces key shark-specific features of tooth development as well as real tooth shape variation in small-spotted catsharks Scyliorhinus canicula. We validate our model by comparison with experiments in vivo. Strikingly, we observe that developmental transitions between tooth shapes tend to be highly degenerate, even for complex phenotypes. We also discover that the sets of developmental parameters involved in tooth shape transitions tend to depend asymmetrically on the direction of that transition. Together, our findings provide a valuable base for furthering our understanding of how developmental changes can lead to both adaptive phenotypic change and trait convergence in complex, phenotypically highly diverse, structures.
