Vertebrates have a vast array of epithelial appendages, including scales, feathers, and hair. The... more Vertebrates have a vast array of epithelial appendages, including scales, feathers, and hair. The developmental patterning of these diverse structures can be theoretically explained by Alan Turing's reaction-diffusion system. However, the role of this system in epithelial appendage patterning of early diverging lineages (com-pared to tetrapods), such as the cartilaginous fishes, is poorly understood. We investigate patterning of the unique tooth-like skin denticles of sharks, which closely relates to their hydrodynamic and protective functions. We demonstrate through simulation models that a Turing-like mechanism can explain shark den-ticle patterning and verify this system using gene expression analysis and gene pathway inhibition experiments. This mechanism bears remarkable similarity to avian feather patterning, suggesting deep homology of the system. We propose that a diverse range of vertebrate appendages, from shark denticles to avian feathers and mam-malian hair, use this ancient and conserved system, with slight genetic modulation accounting for broad variations in patterning.
Teeth and denticles belong to a specialized class of mineralizing epithelial appendages called od... more Teeth and denticles belong to a specialized class of mineralizing epithelial appendages called odontodes. Although homology of oral teeth in jawed vertebrates is well supported, the evolutionary origin of teeth and their relationship with other odontode types is less clear. We compared the cellular and molecular mechanisms directing development of teeth and skin denticles in sharks, where both odontode types are retained. We show that teeth and denticles are deeply homologous developmental modules with equivalent underlying odontode gene regulatory networks (GRNs). Notably, the expression of the epithelial progenitor and stem cell marker sex-determining region Y-related box 2 (sox2) was tooth-specific and this correlates with notable differences in odontode regenera-tive ability. Whereas shark teeth retain the ancestral gnathostome character of continuous successional regeneration, new denticles arise only asynchronously with growth or after wounding. Sox2+ putative stem cells associated with the shark dental lamina (DL) emerge from a field of epithelial progenitors shared with anterior-most taste buds, before establishing within slow-cycling cell niches at the (i) superficial taste/tooth junction (T/TJ), and (ii) deep suc-cessional lamina (SL) where tooth regeneration initiates. Furthermore, during regeneration, cells from the superficial T/TJ migrate into the SL and contribute to new teeth, demonstrating persistent contribution of taste-associated progenitors to tooth regeneration in vivo. This data suggests a trajectory for tooth evolution involving cooption of the odontode GRN from nonregenerating denticles by sox2+ progenitors native to the oral taste epithelium, facilitating the evolution of a novel regenerative module of odontodes in the mouth of early jawed vertebrates: the teeth. regeneration | stem cells | odontogenesis | chondrichthyes | evolutionary novelty T he evolutionary origin of teeth, a key vertebrate innovation, is a long-disputed question in vertebrate biology (1–3). Anatomical and developmental similarities between teeth and denti-cles, both consisting of basal bone, dentine, and a hypermineralized enamel-related tissue surrounding a pulp cavity, have long been recognized (4, 5). Despite these similarities, teeth in extant vertebrates are functionally, topographically, and organizationally distinct from the rest of the exoskeleton and considered a largely independent developmental module (6, 7). Current hypotheses posit that oral teeth evolved either from odontodes in the external dermal skeleton (outside-in) or deeper within the pharynx (inside-out) before their eventual cooption and elaboration in jaws of early gnathostomes (1, 3). However, neither the developmental genetic basis of this cooption event nor the evolutionary mechanisms underlying the elaboration and diversification of this peculiar odontode module are known. To resolve these outstanding questions, it is necessary to clearly differentiate true teeth from other odontode modules using reliable homology criteria. Successional regeneration, the iterative emergence of replacement odontodes within organized families (e.g., tooth-whorls) on the jaw margins characterizes the dentition of crown gnathostomes (Chondrichthyes (including acan-thodians) + Osteichthyes). Polarized rows of sequentially added oral odontodes occur earlier in the fossil record, including on pharyngeal arches of the jawless thelodont Loganellia (2, 8, 9) and in denti-tions of stem gnathostomes such as arthrodiran placoderms (10, 11). However, whether these patterned odontodes are ancestral to or convergent with true successional tooth whorls of crown gnathostomes is still unclear. Due to the secondary loss of polyphyodonty in most established vertebrate model organisms (e.g., mouse, chick, frog, zebrafish), developmental mechanisms regulating successional regeneration of oral teeth remain poorly understood. Correspondingly, how the evolutionary transformation between simple unidimensional addition of new odontodes into an expanding growth zone as seen in skin den-ticles and the complex successional regeneration of odontodes in a one-for-one or many-for-one family-structured pattern occurred is unknown. To resolve the evolutionary relationship between oral teeth and other odontodes and to develop a model describing the emergence of successional regeneration from simple nonsuccessional odontode addition, we compared the developmental genetic basis for successional regeneration of oral teeth with the development of other odontodes (skin denticles) using the emerging chondrichthyan model, the small-spotted catshark (Scyliorhinus canicula) (12, 13) (Fig. 1 A and B). Results Successional Regeneration is a Property Unique to Teeth Among Odontodes. We first compared developmental patterning of oral teeth with denticles in catsharks with a range of light microscopy and computed tomographic methods (Fig. 1 and Movie S1). The shark dentition, emerging from tightly constrained developmental fields on the anterior jaw margins (6, 14), includes adjoining tooth families embedded within a permanent epithelial dental lamina (DL) (Fig. 1 C–G). Each family is comprised of a developmental sequence of regenerating teeth, with the youngest tooth primordia Significance Oral teeth and skin denticles share a deep, 450-million-year-old, evolutionary relationship among vertebrates. We investigate how teeth evolved from simpler denticles using sharks as an evolutionary developmental model. The striking ability of shark teeth to regenerate rapidly and continuously is not shared by denticles, and we suggest that this difference is related to the tooth-specific expression of the stem cell factor sox2. We show that epithelial progenitors of the shark dentition share a remarkable developmental relationship with taste buds. We suggest that teeth arose by combining the gene regulatory network for producing simple denticles with that for producing the highly regenerative taste buds in the oral cavity.
The evolution of oral teeth is considered a major contributor to the overall success of jawed ver... more 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 lifelong regeneration. Perpetual regeneration of oral teeth has been either lost or highly reduced in many other lineages including important developmental model species, so cartilaginous fishes are uniquely suited for deep comparative analyses of tooth development and regeneration. Additionally, sharks and rays can offer crucial insights into the characters of the dentition in the ancestor of all jawed vertebrates. Despite this, tooth development and regeneration in chondrichthyans is poorly understood and remains virtually uncharacterized from a developmental genetic standpoint. Using the emerging chondrichthyan model, the catshark (Scyliorhinus spp.), we characterized the expression of genes homologous to those known to be expressed during stages of early dental competence, tooth initiation, morphogenesis, and regenera-tion in bony vertebrates. We have found that expression patterns of several genes from Hh, Wnt/β-catenin, Bmp and Fgf signalling pathways indicate deep conservation over $ 450 million years of tooth development and regeneration. We describe how these genes participate in the initial emergence of the shark dentition and how they are redeployed during regeneration of successive tooth generations. We suggest that at the dawn of the vertebrate lineage, teeth (i) were most likely continuously regenerative structures, and (ii) utilised a core set of genes from members of key developmental signalling pathways that were instrumental in creating a dental legacy redeployed throughout vertebrate evolution. These data lay the foundation for further experimental investigations utilizing the unique regenerative capacity of chondrichthyan models to answer evolutionary, developmental, and regenerative biological questions that are impossible to explore in classical models.
Classically the oral dentition with teeth regulated into a successional iterative order was thoug... more Classically the oral dentition with teeth regulated into a successional iterative order was thought to have evolved from the superficial skin denticles migrating into the mouth at the stage when jaws evolved. The canonical view is that the initiation of a pattern order for teeth at the mouth margin required development of a sub-epithelial, permanent dental lamina. This provided regulated tooth production in advance of functional need, as exemplified by the Chondrichthyes. It had been assumed that teeth in the Osteichthyes form in this way as in tetrapods. However, this has been shown not to be true for many osteichthyan fish where a dental lamina of this kind does not form, but teeth are regularly patterned and replaced. We question the evolutionary origin of pattern information for the dentition driven by new morphological data on spatial initiation of skin denticles in the catshark. We review recent gene expression data for spatio-temporal order of tooth initiation for Scyliorhinus canicula, selected teleosts in both oral and pharyngeal dentitions, and Neoceratodus forsteri. Although denticles in the chondrichthyan skin appear not to follow a strict pattern order in space and time, tooth replacement in a functional system occurs with precise timing and spatial order. We suggest that the patterning mechanism observed for the oral and pharyngeal dentition is unique to the vertebrate oro-pharynx and independent of the skin system. Therefore, co-option of a successional iterative pattern occurred in evolution not from the skin but from mechanisms existing in the oro-pharynx of now extinct agnathans.
In classical theory, teeth of vertebrate dentitions evolved from co-option of external skin denti... more 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 newdata frommicro-CT scanning, showing howthe ‘conein- 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 908 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 hondrichthyans, but differs in the crown reorientation and their enclosure directly between roots of predecessor saw-teeth. Schizorhiza saw-tooth development is decoupled fromthe jawteeth 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.
This study considers stem cells for odontogenic capability in biological tooth renewal in the bro... more This study considers stem cells for odontogenic capability in biological tooth renewal in the broad context of gnathostome dentitions and the derivation of them from oral epithelium. The location of the developmental site and cell dynamics of the dental lamina are parameters of a possible source for odontogenic epithelial stem cells, but the phylogenetic history is not known. Understanding the phylogenetic basis for stem cell origins throughout continuous tooth renewal in basal jawed vertebrates is the ultimate objective of this study. The key to understanding the origin and location of stem cells in the development of the dentition is sequestration of stem cells locally for programmed tooth renewal. We suggest not only the initial pattern differences in each dentate field but local control subsequently for tooth renewal within each family. The role of the specialized odontogenic epithelium (odontogenic band) is considered as that in which the stem cells reside and become partitioned. These regulate time, position and shape in sequential tooth production. New histological data for chondrichthyan fish show first a thickening of the oral epithelium (odontogenic band). After this, all primary and successive teeth are only generated deep to the oral epithelium from a dental lamina. In contrast, in osteichthyan fish the first teeth develop directly within the odontogenic band. In addition, successors are initiated at each tooth site in the predecessor tooth germ (without a dental lamina). We suggest that stem cells specified for each tooth family are set up and located in intermediate cells between the outer and inner dental epithelia. J. Exp. Zool. (Mol. Dev. Evol.) 312B:260– 280, 2009
Maintaining coral reef resilience against increasing anthropogenic disturbance is critical for ef... more Maintaining coral reef resilience against increasing anthropogenic disturbance is critical for effective reef management. Resilience is partially determined by how processes, such as herbivory and nutrient supply, affect coral recovery versus macroalgal proliferation following disturbances. However, the relative effects of herbivory versus nutrient enrichment on algal proliferation remain debated. Here, we manipulated herbivory and nutrients on a coral-dominated reef protected from fishing, and on an adjacent macroalgal-dominated reef subject to fishing and riverine discharge, over 152 days. On both reefs, herbivore exclusion increased total and upright macroalgal cover by 9-46 times, upright macroalgal biomass by 23-84 times, and cyanobacteria cover by 0-27 times, but decreased cover of encrusting coralline algae by 46-100% and short turf algae by 14-39%. In contrast, nutrient enrichment had no effect on algal proliferation, but suppressed cover of total macroalgae (by 33-42%) and ...
Shark and ray (elasmobranch) dentitions are well known for their multiple generations of teeth, w... more 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.
Ray-finned fishes (Actinopterygii) are the dominant vertebrate group today (þ30 000 species, pred... more Ray-finned fishes (Actinopterygii) are the dominant vertebrate group today (þ30 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 newdata 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.
In many non-mammalian vertebrates, adult dentitions result from cyclical rounds of tooth regenera... more In many non-mammalian vertebrates, adult dentitions result from cyclical rounds of tooth regeneration wherein simple unicuspid teeth are replaced by more complex forms. Therefore and by contrast to mammalian models, the numerical majority of vertebrate teeth develop shape during the process of replacement. Here, we exploit the dental diversity of Lake Malawi cichlid fishes to ask how vertebrates generally replace their dentition and in turn how this process acts to influence resulting tooth morphologies. First, we used immunohistochemistry to chart organogenesis of continually replacing cichlid teeth and discovered an epithelial down-growth that initiates the replacement cycle via a labial proliferation bias. Next, we identified sets of co-expressed genes from common pathways active during de novo, lifelong tooth replacement and tooth morphogenesis. Of note, we found two distinct epithelial cell populations, expressing markers of dental competence and cell potency, which may be responsible for tooth regeneration. Related gene sets were simultaneously active in putative signaling centers associated with the differentiation of replacement teeth with complex shapes. Finally, we manipulated targeted pathways (BMP, FGF, Hh, Notch, Wnt/β-catenin) in vivo with small molecules and demonstrated dose-dependent effects on both tooth replacement and tooth shape. Our data suggest that the processes of tooth regeneration and tooth shape morphogenesis are integrated via a common set of molecular signals. This linkage has subsequently been lost or decoupled in mammalian dentitions where complex tooth shapes develop in first generation dentitions that lack the capacity for lifelong replacement. Our dissection of the molecular mechanics of vertebrate tooth replacement coupled to complex shape pinpoints aspects of odontogenesis that might be re-evolved in the lab to solve problems in regenerative dentistry.
Proceedings of The National Academy of Sciences, 2010
Differences in brain region size among species are thought to arise late in development via adapt... more Differences in brain region size among species are thought to arise late in development via adaptive control over neurogenesis, as cells of previously patterned compartments proliferate, die, and/or differentiate into neurons. Here we investigate comparative brain development in ecologically distinct cichlid fishes from Lake Malawi and demonstrate that brains vary among recently evolved lineages because of early patterning. Divergence among rock-dwellers and sand-dwellers in the relative size of the telencephalon versus the thalamus is correlated with gene expression variation in a regulatory circuit (composed of six3, fezf2, shh, irx1b, and wnt1) known from model organisms to specify anterior-posterior (AP) brain polarity and position the shh-positive signaling boundary zona limitans intrathalamica (ZLI) in the forebrain. To confirm that changes in this coexpression network are sufficient to produce the differences we observe, we manipulated WNT signaling in vivo by treating rock-dwelling cichlid embryos with temporally precise doses of LiCl. Chemically treated rock-dwellers develop gene expression patterns, ZLIs, and forebrains distinct from controls and untreated conspecifics, but strongly resembling those of sand-dwellers. Notably, endemic Malawi rock- and sand-dwelling lineages are alternately fixed for an SNP in irx1b, a mediator of WNT signaling required for proper thalamus and ZLI. Together, these natural experiments in neuroanatomy, development, and genomics suggest that evolutionary changes in AP patterning establish ecologically relevant differences in the elaboration of cichlid forebrain compartments. In general, variation in developmental patterning might lay the foundations on which neurogenesis erects diverse brain architectures.
Maintaining coral reef resilience against increasing anthropogenic disturbance is critical for ef... more Maintaining coral reef resilience against increasing anthropogenic disturbance is critical for effective reef management. Resilience is partially determined by how processes, such as herbivory and nutrient supply, affect coral recovery versus macroalgal proliferation following disturbances. However, the relative effects of herbivory versus nutrient enrichment on algal proliferation remain debated. Here, we manipulated herbivory and nutrients on a coral-dominated reef protected from fishing, and on an adjacent macroalgal-dominated reef subject to fishing and riverine discharge, over 152 days. On both reefs, herbivore exclusion increased total and upright macroalgal cover by 9–46 times, upright macroalgal biomass by 23–84 times, and cyanobacteria cover by 0–27 times, but decreased cover of encrusting coralline algae by 46–100% and short turf algae by 14–39%. In contrast, nutrient enrichment had no effect on algal proliferation, but suppressed cover of total macroalgae (by 33–42%) and cyanobacteria (by 71% on the protected reef) when herbivores were excluded. Herbivore exclusion, but not nutrient enrichment, also increased sediment accumulation, suggesting a strong link between herbivory, macroalgal growth, and sediment retention. Growth rates of the corals Porites cylindrica and Acropora millepora were 30–35% greater on the protected versus fished reef, but nutrient and herbivore manipulations within a site did not affect coral growth. Cumulatively, these data suggest that herbivory rather than eutrophication plays the dominant role in mediating macroalgal proliferation, that macroalgae trap sediments that may further suppress herbivory and enhance macroalgal dominance, and that corals are relatively resistant to damage from some macroalgae but are significantly impacted by ambient reef condition.
Vertebrates have a vast array of epithelial appendages, including scales, feathers, and hair. The... more Vertebrates have a vast array of epithelial appendages, including scales, feathers, and hair. The developmental patterning of these diverse structures can be theoretically explained by Alan Turing's reaction-diffusion system. However, the role of this system in epithelial appendage patterning of early diverging lineages (com-pared to tetrapods), such as the cartilaginous fishes, is poorly understood. We investigate patterning of the unique tooth-like skin denticles of sharks, which closely relates to their hydrodynamic and protective functions. We demonstrate through simulation models that a Turing-like mechanism can explain shark den-ticle patterning and verify this system using gene expression analysis and gene pathway inhibition experiments. This mechanism bears remarkable similarity to avian feather patterning, suggesting deep homology of the system. We propose that a diverse range of vertebrate appendages, from shark denticles to avian feathers and mam-malian hair, use this ancient and conserved system, with slight genetic modulation accounting for broad variations in patterning.
Teeth and denticles belong to a specialized class of mineralizing epithelial appendages called od... more Teeth and denticles belong to a specialized class of mineralizing epithelial appendages called odontodes. Although homology of oral teeth in jawed vertebrates is well supported, the evolutionary origin of teeth and their relationship with other odontode types is less clear. We compared the cellular and molecular mechanisms directing development of teeth and skin denticles in sharks, where both odontode types are retained. We show that teeth and denticles are deeply homologous developmental modules with equivalent underlying odontode gene regulatory networks (GRNs). Notably, the expression of the epithelial progenitor and stem cell marker sex-determining region Y-related box 2 (sox2) was tooth-specific and this correlates with notable differences in odontode regenera-tive ability. Whereas shark teeth retain the ancestral gnathostome character of continuous successional regeneration, new denticles arise only asynchronously with growth or after wounding. Sox2+ putative stem cells associated with the shark dental lamina (DL) emerge from a field of epithelial progenitors shared with anterior-most taste buds, before establishing within slow-cycling cell niches at the (i) superficial taste/tooth junction (T/TJ), and (ii) deep suc-cessional lamina (SL) where tooth regeneration initiates. Furthermore, during regeneration, cells from the superficial T/TJ migrate into the SL and contribute to new teeth, demonstrating persistent contribution of taste-associated progenitors to tooth regeneration in vivo. This data suggests a trajectory for tooth evolution involving cooption of the odontode GRN from nonregenerating denticles by sox2+ progenitors native to the oral taste epithelium, facilitating the evolution of a novel regenerative module of odontodes in the mouth of early jawed vertebrates: the teeth. regeneration | stem cells | odontogenesis | chondrichthyes | evolutionary novelty T he evolutionary origin of teeth, a key vertebrate innovation, is a long-disputed question in vertebrate biology (1–3). Anatomical and developmental similarities between teeth and denti-cles, both consisting of basal bone, dentine, and a hypermineralized enamel-related tissue surrounding a pulp cavity, have long been recognized (4, 5). Despite these similarities, teeth in extant vertebrates are functionally, topographically, and organizationally distinct from the rest of the exoskeleton and considered a largely independent developmental module (6, 7). Current hypotheses posit that oral teeth evolved either from odontodes in the external dermal skeleton (outside-in) or deeper within the pharynx (inside-out) before their eventual cooption and elaboration in jaws of early gnathostomes (1, 3). However, neither the developmental genetic basis of this cooption event nor the evolutionary mechanisms underlying the elaboration and diversification of this peculiar odontode module are known. To resolve these outstanding questions, it is necessary to clearly differentiate true teeth from other odontode modules using reliable homology criteria. Successional regeneration, the iterative emergence of replacement odontodes within organized families (e.g., tooth-whorls) on the jaw margins characterizes the dentition of crown gnathostomes (Chondrichthyes (including acan-thodians) + Osteichthyes). Polarized rows of sequentially added oral odontodes occur earlier in the fossil record, including on pharyngeal arches of the jawless thelodont Loganellia (2, 8, 9) and in denti-tions of stem gnathostomes such as arthrodiran placoderms (10, 11). However, whether these patterned odontodes are ancestral to or convergent with true successional tooth whorls of crown gnathostomes is still unclear. Due to the secondary loss of polyphyodonty in most established vertebrate model organisms (e.g., mouse, chick, frog, zebrafish), developmental mechanisms regulating successional regeneration of oral teeth remain poorly understood. Correspondingly, how the evolutionary transformation between simple unidimensional addition of new odontodes into an expanding growth zone as seen in skin den-ticles and the complex successional regeneration of odontodes in a one-for-one or many-for-one family-structured pattern occurred is unknown. To resolve the evolutionary relationship between oral teeth and other odontodes and to develop a model describing the emergence of successional regeneration from simple nonsuccessional odontode addition, we compared the developmental genetic basis for successional regeneration of oral teeth with the development of other odontodes (skin denticles) using the emerging chondrichthyan model, the small-spotted catshark (Scyliorhinus canicula) (12, 13) (Fig. 1 A and B). Results Successional Regeneration is a Property Unique to Teeth Among Odontodes. We first compared developmental patterning of oral teeth with denticles in catsharks with a range of light microscopy and computed tomographic methods (Fig. 1 and Movie S1). The shark dentition, emerging from tightly constrained developmental fields on the anterior jaw margins (6, 14), includes adjoining tooth families embedded within a permanent epithelial dental lamina (DL) (Fig. 1 C–G). Each family is comprised of a developmental sequence of regenerating teeth, with the youngest tooth primordia Significance Oral teeth and skin denticles share a deep, 450-million-year-old, evolutionary relationship among vertebrates. We investigate how teeth evolved from simpler denticles using sharks as an evolutionary developmental model. The striking ability of shark teeth to regenerate rapidly and continuously is not shared by denticles, and we suggest that this difference is related to the tooth-specific expression of the stem cell factor sox2. We show that epithelial progenitors of the shark dentition share a remarkable developmental relationship with taste buds. We suggest that teeth arose by combining the gene regulatory network for producing simple denticles with that for producing the highly regenerative taste buds in the oral cavity.
The evolution of oral teeth is considered a major contributor to the overall success of jawed ver... more 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 lifelong regeneration. Perpetual regeneration of oral teeth has been either lost or highly reduced in many other lineages including important developmental model species, so cartilaginous fishes are uniquely suited for deep comparative analyses of tooth development and regeneration. Additionally, sharks and rays can offer crucial insights into the characters of the dentition in the ancestor of all jawed vertebrates. Despite this, tooth development and regeneration in chondrichthyans is poorly understood and remains virtually uncharacterized from a developmental genetic standpoint. Using the emerging chondrichthyan model, the catshark (Scyliorhinus spp.), we characterized the expression of genes homologous to those known to be expressed during stages of early dental competence, tooth initiation, morphogenesis, and regenera-tion in bony vertebrates. We have found that expression patterns of several genes from Hh, Wnt/β-catenin, Bmp and Fgf signalling pathways indicate deep conservation over $ 450 million years of tooth development and regeneration. We describe how these genes participate in the initial emergence of the shark dentition and how they are redeployed during regeneration of successive tooth generations. We suggest that at the dawn of the vertebrate lineage, teeth (i) were most likely continuously regenerative structures, and (ii) utilised a core set of genes from members of key developmental signalling pathways that were instrumental in creating a dental legacy redeployed throughout vertebrate evolution. These data lay the foundation for further experimental investigations utilizing the unique regenerative capacity of chondrichthyan models to answer evolutionary, developmental, and regenerative biological questions that are impossible to explore in classical models.
Classically the oral dentition with teeth regulated into a successional iterative order was thoug... more Classically the oral dentition with teeth regulated into a successional iterative order was thought to have evolved from the superficial skin denticles migrating into the mouth at the stage when jaws evolved. The canonical view is that the initiation of a pattern order for teeth at the mouth margin required development of a sub-epithelial, permanent dental lamina. This provided regulated tooth production in advance of functional need, as exemplified by the Chondrichthyes. It had been assumed that teeth in the Osteichthyes form in this way as in tetrapods. However, this has been shown not to be true for many osteichthyan fish where a dental lamina of this kind does not form, but teeth are regularly patterned and replaced. We question the evolutionary origin of pattern information for the dentition driven by new morphological data on spatial initiation of skin denticles in the catshark. We review recent gene expression data for spatio-temporal order of tooth initiation for Scyliorhinus canicula, selected teleosts in both oral and pharyngeal dentitions, and Neoceratodus forsteri. Although denticles in the chondrichthyan skin appear not to follow a strict pattern order in space and time, tooth replacement in a functional system occurs with precise timing and spatial order. We suggest that the patterning mechanism observed for the oral and pharyngeal dentition is unique to the vertebrate oro-pharynx and independent of the skin system. Therefore, co-option of a successional iterative pattern occurred in evolution not from the skin but from mechanisms existing in the oro-pharynx of now extinct agnathans.
In classical theory, teeth of vertebrate dentitions evolved from co-option of external skin denti... more 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 newdata frommicro-CT scanning, showing howthe ‘conein- 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 908 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 hondrichthyans, but differs in the crown reorientation and their enclosure directly between roots of predecessor saw-teeth. Schizorhiza saw-tooth development is decoupled fromthe jawteeth 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.
This study considers stem cells for odontogenic capability in biological tooth renewal in the bro... more This study considers stem cells for odontogenic capability in biological tooth renewal in the broad context of gnathostome dentitions and the derivation of them from oral epithelium. The location of the developmental site and cell dynamics of the dental lamina are parameters of a possible source for odontogenic epithelial stem cells, but the phylogenetic history is not known. Understanding the phylogenetic basis for stem cell origins throughout continuous tooth renewal in basal jawed vertebrates is the ultimate objective of this study. The key to understanding the origin and location of stem cells in the development of the dentition is sequestration of stem cells locally for programmed tooth renewal. We suggest not only the initial pattern differences in each dentate field but local control subsequently for tooth renewal within each family. The role of the specialized odontogenic epithelium (odontogenic band) is considered as that in which the stem cells reside and become partitioned. These regulate time, position and shape in sequential tooth production. New histological data for chondrichthyan fish show first a thickening of the oral epithelium (odontogenic band). After this, all primary and successive teeth are only generated deep to the oral epithelium from a dental lamina. In contrast, in osteichthyan fish the first teeth develop directly within the odontogenic band. In addition, successors are initiated at each tooth site in the predecessor tooth germ (without a dental lamina). We suggest that stem cells specified for each tooth family are set up and located in intermediate cells between the outer and inner dental epithelia. J. Exp. Zool. (Mol. Dev. Evol.) 312B:260– 280, 2009
Maintaining coral reef resilience against increasing anthropogenic disturbance is critical for ef... more Maintaining coral reef resilience against increasing anthropogenic disturbance is critical for effective reef management. Resilience is partially determined by how processes, such as herbivory and nutrient supply, affect coral recovery versus macroalgal proliferation following disturbances. However, the relative effects of herbivory versus nutrient enrichment on algal proliferation remain debated. Here, we manipulated herbivory and nutrients on a coral-dominated reef protected from fishing, and on an adjacent macroalgal-dominated reef subject to fishing and riverine discharge, over 152 days. On both reefs, herbivore exclusion increased total and upright macroalgal cover by 9-46 times, upright macroalgal biomass by 23-84 times, and cyanobacteria cover by 0-27 times, but decreased cover of encrusting coralline algae by 46-100% and short turf algae by 14-39%. In contrast, nutrient enrichment had no effect on algal proliferation, but suppressed cover of total macroalgae (by 33-42%) and ...
Shark and ray (elasmobranch) dentitions are well known for their multiple generations of teeth, w... more 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.
Ray-finned fishes (Actinopterygii) are the dominant vertebrate group today (þ30 000 species, pred... more Ray-finned fishes (Actinopterygii) are the dominant vertebrate group today (þ30 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 newdata 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.
In many non-mammalian vertebrates, adult dentitions result from cyclical rounds of tooth regenera... more In many non-mammalian vertebrates, adult dentitions result from cyclical rounds of tooth regeneration wherein simple unicuspid teeth are replaced by more complex forms. Therefore and by contrast to mammalian models, the numerical majority of vertebrate teeth develop shape during the process of replacement. Here, we exploit the dental diversity of Lake Malawi cichlid fishes to ask how vertebrates generally replace their dentition and in turn how this process acts to influence resulting tooth morphologies. First, we used immunohistochemistry to chart organogenesis of continually replacing cichlid teeth and discovered an epithelial down-growth that initiates the replacement cycle via a labial proliferation bias. Next, we identified sets of co-expressed genes from common pathways active during de novo, lifelong tooth replacement and tooth morphogenesis. Of note, we found two distinct epithelial cell populations, expressing markers of dental competence and cell potency, which may be responsible for tooth regeneration. Related gene sets were simultaneously active in putative signaling centers associated with the differentiation of replacement teeth with complex shapes. Finally, we manipulated targeted pathways (BMP, FGF, Hh, Notch, Wnt/β-catenin) in vivo with small molecules and demonstrated dose-dependent effects on both tooth replacement and tooth shape. Our data suggest that the processes of tooth regeneration and tooth shape morphogenesis are integrated via a common set of molecular signals. This linkage has subsequently been lost or decoupled in mammalian dentitions where complex tooth shapes develop in first generation dentitions that lack the capacity for lifelong replacement. Our dissection of the molecular mechanics of vertebrate tooth replacement coupled to complex shape pinpoints aspects of odontogenesis that might be re-evolved in the lab to solve problems in regenerative dentistry.
Proceedings of The National Academy of Sciences, 2010
Differences in brain region size among species are thought to arise late in development via adapt... more Differences in brain region size among species are thought to arise late in development via adaptive control over neurogenesis, as cells of previously patterned compartments proliferate, die, and/or differentiate into neurons. Here we investigate comparative brain development in ecologically distinct cichlid fishes from Lake Malawi and demonstrate that brains vary among recently evolved lineages because of early patterning. Divergence among rock-dwellers and sand-dwellers in the relative size of the telencephalon versus the thalamus is correlated with gene expression variation in a regulatory circuit (composed of six3, fezf2, shh, irx1b, and wnt1) known from model organisms to specify anterior-posterior (AP) brain polarity and position the shh-positive signaling boundary zona limitans intrathalamica (ZLI) in the forebrain. To confirm that changes in this coexpression network are sufficient to produce the differences we observe, we manipulated WNT signaling in vivo by treating rock-dwelling cichlid embryos with temporally precise doses of LiCl. Chemically treated rock-dwellers develop gene expression patterns, ZLIs, and forebrains distinct from controls and untreated conspecifics, but strongly resembling those of sand-dwellers. Notably, endemic Malawi rock- and sand-dwelling lineages are alternately fixed for an SNP in irx1b, a mediator of WNT signaling required for proper thalamus and ZLI. Together, these natural experiments in neuroanatomy, development, and genomics suggest that evolutionary changes in AP patterning establish ecologically relevant differences in the elaboration of cichlid forebrain compartments. In general, variation in developmental patterning might lay the foundations on which neurogenesis erects diverse brain architectures.
Maintaining coral reef resilience against increasing anthropogenic disturbance is critical for ef... more Maintaining coral reef resilience against increasing anthropogenic disturbance is critical for effective reef management. Resilience is partially determined by how processes, such as herbivory and nutrient supply, affect coral recovery versus macroalgal proliferation following disturbances. However, the relative effects of herbivory versus nutrient enrichment on algal proliferation remain debated. Here, we manipulated herbivory and nutrients on a coral-dominated reef protected from fishing, and on an adjacent macroalgal-dominated reef subject to fishing and riverine discharge, over 152 days. On both reefs, herbivore exclusion increased total and upright macroalgal cover by 9–46 times, upright macroalgal biomass by 23–84 times, and cyanobacteria cover by 0–27 times, but decreased cover of encrusting coralline algae by 46–100% and short turf algae by 14–39%. In contrast, nutrient enrichment had no effect on algal proliferation, but suppressed cover of total macroalgae (by 33–42%) and cyanobacteria (by 71% on the protected reef) when herbivores were excluded. Herbivore exclusion, but not nutrient enrichment, also increased sediment accumulation, suggesting a strong link between herbivory, macroalgal growth, and sediment retention. Growth rates of the corals Porites cylindrica and Acropora millepora were 30–35% greater on the protected versus fished reef, but nutrient and herbivore manipulations within a site did not affect coral growth. Cumulatively, these data suggest that herbivory rather than eutrophication plays the dominant role in mediating macroalgal proliferation, that macroalgae trap sediments that may further suppress herbivory and enhance macroalgal dominance, and that corals are relatively resistant to damage from some macroalgae but are significantly impacted by ambient reef condition.
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to have evolved from the superficial skin denticles migrating into the mouth at the stage when
jaws evolved. The canonical view is that the initiation of a pattern order for teeth at the mouth
margin required development of a sub-epithelial, permanent dental lamina. This provided regulated
tooth production in advance of functional need, as exemplified by the Chondrichthyes. It had been
assumed that teeth in the Osteichthyes form in this way as in tetrapods. However, this has been
shown not to be true for many osteichthyan fish where a dental lamina of this kind does not form,
but teeth are regularly patterned and replaced. We question the evolutionary origin of pattern
information for the dentition driven by new morphological data on spatial initiation of skin
denticles in the catshark. We review recent gene expression data for spatio-temporal order of
tooth initiation for Scyliorhinus canicula, selected teleosts in both oral and pharyngeal dentitions,
and Neoceratodus forsteri. Although denticles in the chondrichthyan skin appear not to follow a
strict pattern order in space and time, tooth replacement in a functional system occurs with
precise timing and spatial order. We suggest that the patterning mechanism observed for the oral
and pharyngeal dentition is unique to the vertebrate oro-pharynx and independent of the skin
system. Therefore, co-option of a successional iterative pattern occurred in evolution not from the
skin but from mechanisms existing in the oro-pharynx of now extinct agnathans.
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 908 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 hondrichthyans, but differs in the crown reorientation and their enclosure directly between roots of predecessor saw-teeth. Schizorhiza saw-tooth development is decoupled fromthe jawteeth 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.
not known. Understanding the phylogenetic basis for stem cell origins throughout continuous tooth renewal in basal jawed vertebrates is the ultimate objective of this study. The key to understanding the origin and location of stem cells in the development of the dentition is sequestration of stem cells
locally for programmed tooth renewal. We suggest not only the initial pattern differences in each dentate field but local control subsequently for tooth renewal within each family. The role of the specialized odontogenic epithelium (odontogenic band) is considered as that in which the stem cells reside and become partitioned. These regulate time, position and shape in sequential tooth production. New histological data for chondrichthyan fish show first a thickening of the oral
epithelium (odontogenic band). After this, all primary and successive teeth are only generated deep to the oral epithelium from a dental lamina. In contrast, in osteichthyan fish the first teeth develop directly within the odontogenic band. In addition, successors are initiated at each tooth site in the predecessor tooth germ (without a dental lamina). We suggest that stem cells specified for each tooth family are set up and located in intermediate cells between the outer and inner dental epithelia.
J. Exp. Zool. (Mol. Dev. Evol.) 312B:260– 280, 2009
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 newdata 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.
to have evolved from the superficial skin denticles migrating into the mouth at the stage when
jaws evolved. The canonical view is that the initiation of a pattern order for teeth at the mouth
margin required development of a sub-epithelial, permanent dental lamina. This provided regulated
tooth production in advance of functional need, as exemplified by the Chondrichthyes. It had been
assumed that teeth in the Osteichthyes form in this way as in tetrapods. However, this has been
shown not to be true for many osteichthyan fish where a dental lamina of this kind does not form,
but teeth are regularly patterned and replaced. We question the evolutionary origin of pattern
information for the dentition driven by new morphological data on spatial initiation of skin
denticles in the catshark. We review recent gene expression data for spatio-temporal order of
tooth initiation for Scyliorhinus canicula, selected teleosts in both oral and pharyngeal dentitions,
and Neoceratodus forsteri. Although denticles in the chondrichthyan skin appear not to follow a
strict pattern order in space and time, tooth replacement in a functional system occurs with
precise timing and spatial order. We suggest that the patterning mechanism observed for the oral
and pharyngeal dentition is unique to the vertebrate oro-pharynx and independent of the skin
system. Therefore, co-option of a successional iterative pattern occurred in evolution not from the
skin but from mechanisms existing in the oro-pharynx of now extinct agnathans.
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 908 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 hondrichthyans, but differs in the crown reorientation and their enclosure directly between roots of predecessor saw-teeth. Schizorhiza saw-tooth development is decoupled fromthe jawteeth 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.
not known. Understanding the phylogenetic basis for stem cell origins throughout continuous tooth renewal in basal jawed vertebrates is the ultimate objective of this study. The key to understanding the origin and location of stem cells in the development of the dentition is sequestration of stem cells
locally for programmed tooth renewal. We suggest not only the initial pattern differences in each dentate field but local control subsequently for tooth renewal within each family. The role of the specialized odontogenic epithelium (odontogenic band) is considered as that in which the stem cells reside and become partitioned. These regulate time, position and shape in sequential tooth production. New histological data for chondrichthyan fish show first a thickening of the oral
epithelium (odontogenic band). After this, all primary and successive teeth are only generated deep to the oral epithelium from a dental lamina. In contrast, in osteichthyan fish the first teeth develop directly within the odontogenic band. In addition, successors are initiated at each tooth site in the predecessor tooth germ (without a dental lamina). We suggest that stem cells specified for each tooth family are set up and located in intermediate cells between the outer and inner dental epithelia.
J. Exp. Zool. (Mol. Dev. Evol.) 312B:260– 280, 2009
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 newdata 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.