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Abstract

Tooth replacement rates of polyphyodont cartilaginous and bony fishes are hard to determine because of a lack of obvious patterning and maintaining specimens long enough to observe replacement. Pulse-chase is a fluorescent technique that differentially colours developing mineralized tissue. We present in situ tooth replacement rate and position data for the oral and pharyngeal detentions of Ophiodon elongatus (Pacific lingcod). We assessed over 10 000 teeth, in 20 fish, and found a daily replacement rate of about two teeth (3.6% of the dentition). The average tooth is in the dental battery for 27 days. The replacement was higher in the lower pharyngeal jaw (LPJ). We found no difference between replacement rates of feeding and non-feeding fish, suggesting feeding was not a driver of tooth replacement. Lingcod teeth have both a size and location fate; smaller teeth at one spot will not grow into larger teeth, even if a large tooth nearby is lost. We also found increased rates of replacement at the posterior of the LPJ relative to the anterior. We propose that lingcod teeth do not migrate in the jaw as they develop; their teeth are fated in size and location, erupting in their functional position.

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Vertebrate dentitions are often collapsed into a few discrete categories, obscuring both potentially important functional differences between them and insight into their evolution. The terms homodonty and heterodonty typically conflate tooth morphology with tooth function, and require context-dependent subcategories to take on any specific meaning. Qualifiers like incipient, transient, or phylogenetic homodonty attempt to provide a more rigorous definition but instead highlight the difficulties in categorizing dentitions. To address these issues, we recently proposed a method for quantifying the function of dental batteries based on the estimated stress of each tooth (inferred using surface area) standardized for jaw out-lever (inferred using tooth position). This method reveals a homodonty-heterodonty functional continuum where small and large teeth work together to transmit forces to a prey item. Morphological homodonty or heterodonty refers to morphology, whereas functional homodonty or heterodonty refers to transmission of stress. In this study, we use Halichoeres wrasses to explore how functional continuum can be used in phylogenetic analyses by generating two continuous metrics from the functional homodonty-heterodonty continuum. Here we show that functionally heterodont teeth have evolved at least three times in Halichoeres wrasses. There are more functionally heterodont teeth on upper jaws than on lower jaws, but functionally heterodont teeth on the lower jaws bear significantly more stress. These nuances, which have functional consequences, would be missed by binning entire dentitions into discrete categories. This analysis points out areas worth taking a closer look at from a mechanical and developmental point of view with respect to the distribution and type of heterodonty seen in different jaws and different areas of jaws. These data, on a small group of wrasses, suggest continuous dental variables can be a rich source of insight into the evolution of fish feeding mechanisms across a wider variety of species.
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Fitness is in part determined by the success of prey capture, often achieved in marine piscivores using teeth to capture and process prey. In ram feeding piscivores, a pattern of monognathic heterodonty has been observed where tooth size either increases posteriorly (Scomberomorus maculatus), or anteriorly (Carcharhinus limbatus), with exceptions such as Trichiurus lepturus and Sphyraena barracuda which have large anterior fangs. Tooth size and placement, as related to prey capture, was examined in Atlantic Spanish Mackerel (S. maculatus), Great Barracuda (S. barracuda), Atlantic Cutlassfish (T. lepturus), and the Blacktip shark (C. limbatus) by quantifying tooth occlusion along the jaw. Percent gape at occlusion in S. maculatus decreased anteriorly in a linear fashion, indicating occlusion from posterior to anterior. Therefore, prey initially contact the posterior teeth with high puncture pressure during high velocity strikes, capitalizing the region of greatest bite force. For S. barracuda and T. lepturus, posterior teeth and premaxillary fangs occlude at similar percent gapes (within 10%). The premaxillary fangs are likely used for initial capture due to the high angular velocity of the anterior section of the jaw and then for cutting, due to their laterally compressed shape. In C. limbatus all teeth occluded within a narrow range of 1.4–8.8% gape, indicating that all teeth meet at almost complete jaw closure. Simultaneous puncture of teeth prevents prey escape while maximizing the cutting area during head shaking. Thus, various tooth size and dentition patterns may yield similar success in prey capture, serving the same function.
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Tooth replacement in piranhas is unusual: all teeth on one side of the head are lost as a unit, then replaced simultaneously. We used histology and microCT to examine tooth-replacement modes across carnivorous piranhas and their herbivorous pacu cousins (Serrasalmidae) and then mapped replacement patterns onto a molecular phylogeny. Pacu teeth develop and are replaced in a manner like piranhas. For serrasalmids, unilateral tooth replacement is not an "all or nothing" phenomenon; we demonstrate that both sides of the jaws have developing tooth rows within them, albeit with one side more mineralized than the other. All serrasalmids (except one) share unilateral tooth replacement, so this is not an adaptation for carnivory. All serrasalmids have interlocking teeth; piranhas interdigitate lateral tooth cusps with adjacent teeth, forming a singular saw-like blade, whereas lateral cusps in pacus clasp together. For serrasalmids to have an interlocking dentition, their teeth need to develop and erupt at the same time. We propose that interlocking mechanisms prevent tooth loss and ensure continued functionality of the feeding apparatus. Serrasalmid dentitions are ubiquitously heterodont, having incisiform and molariform dentitions reminiscent of mammals. Finally, we propose that simultaneous tooth replacement be considered as a synapomorphy for the family.
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Much of the basic information about individual organ development comes from studies using model species. Whereas conservation of gene regulatory networks across higher taxa supports generalizations made from a limited number of species, generality of mechanistic inferences remains to be tested in tissue culture systems. Here, using mammalian tooth explants cultured in isolation, we investigate self-regulation of patterning by comparing developing molars of the mouse, the model species of mammalian research, and the bank vole. A distinct patterning difference between the vole and the mouse molars is the alternate cusp offset present in the vole. Analyses of both species using 3D reconstructions of developing molars and jaws, computational modeling of cusp patterning, and tooth explants cultured with small braces show that correct cusp offset requires constraints on the lateral expansion of the developing tooth. Vole molars cultured without the braces lose their cusp offset, and mouse molars cultured with the braces develop a cusp offset. Our results suggest that cusp offset, which changes frequently in mammalian evolution, is more dependent on the 3D support of the developing jaw than other aspects of tooth shape. This jaw–tooth integration of a specific aspect of the tooth phenotype indicates that organs may outsource specific aspects of their morphology to be regulated by adjacent body parts or organs. Comparative studies of morphologically different species are needed to infer the principles of organogenesis.
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The squaliform sharks represent one of the most speciose shark clades. Many adult squaliforms have blade-like teeth, either on both jaws or restricted to the lower jaw, forming a continuous, serrated blade along the jaw margin. These teeth are replaced as a single unit and successor teeth lack the alternate arrangement present in other elasmobranchs. Micro-CT scans of embryos of squaliforms and a related outgroup (Pristiophoridae) revealed that the squaliform dentition pattern represents a highly modified version of tooth replacement seen in other clades. Teeth of Squalus embryos are arranged in an alternate pattern, with successive tooth rows containing additional teeth added proximally. Asynchronous timing of tooth production along the jaw and tooth loss prior to birth cause teeth to align in oblique sets containing teeth from subsequent rows; these become parallel to the jaw margin during ontogeny, so that adult Squalus has functional tooth rows comprising obliquely stacked teeth of consecutive developmental rows. In more strongly heterodont squaliforms, initial embryonic lower teeth develop into the oblique functional sets seen in adult Squalus, with no requirement to form, and subsequently lose, teeth arranged in an initial alternate pattern.
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Teeth are a classic model system of organogenesis, as repeated and reciprocal epithelial and mesenchymal interactions pattern placode formation and outgrowth. Less is known about the developmental and genetic bases of tooth development and replacement in polyphyodonts, vertebrates with continual tooth replacement. Here we leverage natural variation in the threespine stickleback fish Gasterosteus aculeatus to investigate the developmental genetic bases of tooth development and replacement. We find that two derived freshwater stickleback populations have both convergently evolved more ventral pharyngeal teeth through heritable genetic changes. In both populations, evolved tooth gain manifests late in development. Using pulse-chase vital dye labeling to mark newly forming teeth in adult fish, we find that both high-toothed freshwater populations have accelerated tooth replacement rates relative to low-toothed ancestral marine fish. Despite the similar evolved phenotype of more teeth and an accelerated adult replacement rate, the timing of tooth number divergence and the spatial patterns of newly formed adult teeth are different in the two populations, suggesting distinct developmental mechanisms. Using genome-wide linkage mapping in marine-freshwater F2 genetic crosses, we find that the genetic basis of evolved tooth gain in the two freshwater populations is largely distinct. Together our results support a model where increased tooth number and an accelerated tooth replacement rate have evolved convergently in two independently derived freshwater stickleback populations using largely distinct developmental and genetic mechanisms. © 2015. Published by The Company of Biologists Ltd.
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Organisms that are durophagous, hard prey consumers, have a diversity of tooth forms. To determine why we see this variation, we tested whether some tooth forms break shells better than others. We measured the force needed with three series of aluminium tooth models, which varied in concavity and the morphology of a stress concentrating cusp, to break a shell. We created functionally identical copies of two intertidal snail shells: the thicker shelled Nucella ostrina and the more ornamented Nucella lamellosa using a three-dimensional printer. In this way, we reduced variation in material properties between test shells, allowing us to test only the interaction of the experimental teeth with the two shell morphologies. We found that for all tooth shapes, thicker shells are harder to break than the thinner shells and that increased ornamentation has no discernible effect. Our results show that for both shell morphologies, domed and flat teeth break shells better than cupped teeth, and teeth with tall or skinny cusps break shells best. While our results indicate that there is an ideal tooth form for shell breaking, we do not see this shape in nature. This suggests a probable trade-off between tooth function and the structural integrity of the tooth.
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The mode of tooth development displayed in Chondrichthyans (sharks, rays and holocephalans), one of frequent tooth replacement, was possible once a dental lamina had evolved, and since 1982 this has been known as the odontode regulation theory after Reif. Today, Reif's concepts need to be transformed into those of modern biology, the crosstalk between epithelium and mesenchyme, for the regulation of timing, spacing and shape of vertebrate teeth. Although Reif's proposed 'primordial tissue' may be the only site of progenitor cells, to restrict odontogenic potential to time-specific sites (protogerms), as has been suggested in the sequential addition tooth (SAT) model, very little data are available. Here, his model of alternate tooth replacement files has been interpreted as an integrated tooth addition unit of two adjacent files (SAT) unit for alternate replacement of teeth, regulated by putative, precisely timed gene expression for activation and inhibition. We have provided new data on patterns of tooth succession in dentitions of extant sharks and rays to compare with those of Reif. Using a phylogeny combined from molecular and morphological data, it is suggested that the alternate tooth addition and replacement model is derived within Chondrichthyes, and diversified from single file tooth addition of the stem chondrichthyans.
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Teleost fishes comprise approximately half of all living vertebrates. The extreme range of diversity in teleosts is remarkable, especially, extensive morphological variation in their jaws and dentition. Some of the most unusual dentitions are found among members of the highly derived teleost order Tetraodontiformes, which includes triggerfishes, boxfishes, ocean sunfishes, and pufferfishes. Adult pufferfishes (Tetraodontidae) exhibit a distinctive parrot-like beaked jaw, forming a cutting edge, unlike in any other group of teleosts. Here we show that despite novelty in the structure and development of this "beak," it is initiated by formation of separate first-generation teeth that line the embryonic pufferfish jaw, with timing of development and gene expression patterns conserved from the last common ancestor of osteichthyans. Most of these first-generation larval teeth are lost in development. Continuous tooth replacement proceeds in only four parasymphyseal teeth, as sequentially stacked, multigenerational, jaw-length dentine bands, before development of the functional beak. These data suggest that dental novelties, such as the pufferfish beak, can develop later in ontogeny through modified continuous tooth addition and replacement. We conclude that even highly derived morphological structures like the pufferfish beak form via a conserved developmental bauplan capable of modification during ontogeny by subtle respecification of the developmental module.
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The majority of studies on the evolution and function of feeding in sharks have focused primarily on the movement of cranial components and muscle function, with little integration of tooth properties or function. As teeth are subjected to sometimes extreme loads during feeding, they undergo stress, strain, and potential failure. As attributes related to structural strength such as material properties and overall shape may be subjected to natural selection, both prey processing ability and structural parameters must be considered to understand the evolution of shark teeth. In this study, finite element analysis was used to visualize stress distributions of fossil and extant shark teeth during puncture, unidirectional draw (cutting), and holding. Under the loading and boundary conditions here, which are consistent with bite forces of large sharks, shark teeth are structurally strong. Teeth loaded in puncture have localized stress concentrations at the cusp apex that diminish rapidly away from the apex. When loaded in draw and holding, the majority of the teeth show stress concentrations consistent with well designed cantilever beams. Notches result in stress concentration during draw and may serve as a weak point; however they are functionally important for cutting prey during lateral head shaking behavior. As shark teeth are replaced regularly, it is proposed that the frequency of tooth replacement in sharks is driven by tooth wear, not tooth failure. As the tooth tip and cutting edges are worn, the surface areas of these features increase, decreasing the amount of stress produced by the tooth. While this wear will not affect the general structural strength of the tooth, tooth replacement may also serve to keep ahead of damage caused by fatigue that may lead to eventual tooth failure.
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Vertebrate dentitions originated in the posterior pharynx of jawless fishes more than half a billion years ago. As gnathostomes (jawed vertebrates) evolved, teeth developed on oral jaws and helped to establish the dominance of this lineage on land and in the sea. The advent of oral jaws was facilitated, in part, by absence of hox gene expression in the first, most anterior, pharyngeal arch. Much later in evolutionary time, teleost fishes evolved a novel toothed jaw in the pharynx, the location of the first vertebrate teeth. To examine the evolutionary modularity of dentitions, we asked whether oral and pharyngeal teeth develop using common or independent gene regulatory pathways. First, we showed that tooth number is correlated on oral and pharyngeal jaws across species of cichlid fishes from Lake Malawi (East Africa), suggestive of common regulatory mechanisms for tooth initiation. Surprisingly, we found that cichlid pharyngeal dentitions develop in a region of dense hox gene expression. Thus, regulation of tooth number is conserved, despite distinct developmental environments of oral and pharyngeal jaws; pharyngeal jaws occupy hox-positive, endodermal sites, and oral jaws develop in hox-negative regions with ectodermal cell contributions. Next, we studied the expression of a dental gene network for tooth initiation, most genes of which are similarly deployed across the two disparate jaw sites. This collection of genes includes members of the ectodysplasin pathway, eda and edar, expressed identically during the patterning of oral and pharyngeal teeth. Taken together, these data suggest that pharyngeal teeth of jawless vertebrates utilized an ancient gene network before the origin of oral jaws, oral teeth, and ectodermal appendages. The first vertebrate dentition likely appeared in a hox-positive, endodermal environment and expressed a genetic program including ectodysplasin pathway genes. This ancient regulatory circuit was co-opted and modified for teeth in oral jaws of the first jawed vertebrate, and subsequently deployed as jaws enveloped teeth on novel pharyngeal jaws. Our data highlight an amazing modularity of jaws and teeth as they coevolved during the history of vertebrates. We exploit this diversity to infer a core dental gene network, common to the first tooth and all of its descendants.
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Tooth replacement poses many questions about development, pattern formation, tooth attachment mechanisms, functional morphology and the evolution of vertebrate dentitions. Although most vertebrate species have polyphyodont dentitions, detailed knowledge of tooth structure and replacement is poor for most groups, particularly actinopterygians. We examined the oral dentition of the bluefish, Pomatomus saltatrix, a pelagic and coastal marine predator, using a sample of 50 individuals. The oral teeth are located on the dentary and premaxillary bones, and we scored each tooth locus in the dentary and premaxillary bones using a four-part functional classification: absent (A), incoming (I), functional (F=fully ankylosed) or eroding (E). The homodont oral teeth of Pomatomus are sharp, deeply socketed and firmly ankylosed to the bone of attachment. Replacement is intraosseus and occurs in alternate tooth loci with long waves of replacement passing from rear to front. The much higher percentage of functional as opposed to eroding teeth suggests that replacement rates are low but that individual teeth are quickly lost once erosion begins. Tooth number increases ontogenetically, ranging from 15-31 dentary teeth and 15-39 premaxillary teeth in the sample studied. Teeth increase in size with every replacement cycle. Remodeling of the attachment bone occurs continuously to accommodate growth. New tooth germs originate from a discontinuous dental lamina and migrate from the lingual (dentary) or labial (premaxillary) epithelium through pores in the bone of attachment into the resorption spaces beneath the existing teeth. Pomatomus shares unique aspects of tooth replacement with barracudas and other scombroids and this supports the interpretation that Pomatomus is more closely related to scombroids than to carangoids.
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Gnathostome teeth are one of the most promising models for developmental evolutionary studies, they are the most abundant organ in the fossil record and an excellent example of organogenesis. Teeth have a complex morphology and are restricted to the mouth in mammals, whereas actinopterygian teeth have a simple morphology and are found in several locations, notably on pharyngeal bones. Morphological and developmental similarities support the hypothesis that oral and pharyngeal teeth are serially homologous. Gene expression data from the mouse and some teleosts have shown that the gene families involved in pharyngeal odontogenesis are also involved in oral tooth formation, with the notable exception of the evx gene family. Here, we present a complete description of early odontogenesis in the medaka (Oryzias latipes), which has both oral and pharyngeal dentition. We show that oral and pharyngeal teeth share deep developmental similarities. In the medaka, like in the zebrafish, eve1 is the only evx gene expressed during odontogenesis. In each forming tooth, regardless of its location, eve1 transcription is activated in the placode, then becomes restricted to the inner dental epithelium and is activated in the dental mesenchyme during early differentiation, and finally ceases at late differentiation. Thus eve1 expression is not specific to pharyngeal teeth development as was previously suggested. Because it permits direct comparisons between oral and pharyngeal teeth by molecular, development and functional studies, the medaka is an excellent model to develop further insights into the evolution of odontogenesis in gnathostomes.
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Loricariidae or suckermouth armored catfishes are one of several aquatic taxa feeding on epilithic and epiphytic algae. Their upper and lower jaws bear exquisitely curved teeth, which usually are asymmetrically bicuspid. The enlarged lower lip carries papillae with keratinous unicellular epidermal brushes or unculi. Teeth, and probably unculi too, assist in scraping food off substrates. Their morphology, growth, and replacement is examined and compared among several loricariid species, using cleared and stained specimens, serial sections, and SEM. Apart from the general tooth form and crown shape, the anterior layer of soft tissue on the lower shaft region, present in several species, appears to be a specialization for enhancing the mobility of individual teeth when scraping on uneven surfaces. During early ontogeny, a transition from simple conical to mature tooth occurs. The first unculi appear together with the first teeth carrying a bicuspid crown, 2 days after the first exogenous feeding, but synchronous with the complete resorption of the yolk sac.
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Spines are ubiquitous in both plants and animals, and while most spines were likely originally used for defense, over time many have been modified in a variety of ways. Here we take an integrative approach to review the form, function, and evolution of spines as a defensive strategy in order to make new connections between physical mechanisms and functional behavior. While this review focuses on spines in mammals, we reference and draw ideas from the literature on spines in other taxa, including plants. We begin by exploring the biomechanics of defensive spines, their varied functions, and non-defensive modifications. We pay particular attention to the mechanics involved in passive puncture and the ways organisms have overcome limitations associated with the low energy input. We then focus on the ecological, physiological, and behavioral factors that promote the evolution of spiny defenses, including predator- and habitat-mediated hypotheses. While there is considerable evidence to support both, studies have generally found that (1) defensive spines are usually effective against one class of attacker (e.g., larger predators) but ineffective against others or even facilitate predation by others, and (2) species that are more visible or exposed to predators are under much stronger selection to evolve defensive spines or some other robust defense. What type of defensive morphology that evolves, however, is less predictable and probably strongly dependent on both the dominant source of predation and the habitat structure of the organism (e.g., arboreal, terrestrial, fossorial). We then explore traits that are often correlated with defensive spines and armor, potentially forming armor syndromes, suites of traits that evolve together with body armor in a correlated fashion. In mammals, these include aposematic warning coloration, locomotion style, diet, metabolic rate, and relative brain size. Finally, we encourage integration of mechanistic and evolutionary studies of defensive spines and suggest future avenues of research in the biomechanics, evolution, and behavior of spines and spiny organisms.
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Most jawed vertebrates (gnathostomes) replace their teeth throughout life (polyphyodonty) and there is currently great interest in its molecular and cellular basis, particularly in fish. While much has still to be elucidated, it appears that whichever tooth replacement mechanism is used, only one tooth replaces one predecessor, at any one time. Here we present fossil crushing dentitions of two extinct pycnodont fishes, Pycnodus zeaformis and Pycnodus maliensis. Their surface features and x‐ray micro‐CT virtual sections show no evidence of one‐for‐one replacement. Instead, individual large teeth were replaced by multiple small teeth, for which, as far as we could ascertain, there is no known mechanism. This occurred where underlying dentigerous bone was damaged. Small teeth also developed where parts of large teeth had broken off, and in gaps between large teeth created by the geometry of their close alignment in rows. We compared the virtual sections to those of functionally analogous crushing dentitions of three modern fishes. Contrasting greatly to the pycnodonts, each showed an orderly, one‐for‐one replacement, typical of osteichthyans. We propose that the pycnodont specimens exhibit a gap‐filling tooth addition hitherto unseen in gnathostomes, and that the oral epithelium retained an initiatory competence throughout life, with a programming of ‘if a gap exists, fill it’. This would also have facilitated the addition of large teeth in rows, in space provided by ontogenetic growth. We hypothesize that gaps were registered as an absence of pressure at the crushing surface, initiating tooth development, as in the modern cichlid Astatoreochromis alluaudi.
Article
Teeth tell the tale of interactions between predator and prey. If a dental battery is made up of teeth that look similar, they are morphologically homodont, but if there is an unspecified amount of regional specialization in size or shape, they are morphologically heterodont. These are vague terms with no useful functional implication because morphological homodonty does not necessarily equal functional homodonty. Teeth that look the same may not function the same. Conical teeth are prevalent in fishes, superficially tasked with the simple job of puncture. There is a great deal of variation in the shape and placement of conical teeth. Anterior teeth may be larger than posterior ones, larger teeth may be surrounded by small ones, and patches of teeth may all have the same size and shape. Such variations suggest that conical dentitions might represent a single morphological solution for different functional problems. We are interested in the concept of homodonty and using the conical tooth as a model to differentiate between tooth shape and performance. We consider the stress that a tooth can exert on prey as stress is what causes damage. To create a statistical measure of functional homodonty, stress was calculated from measurements of surface area, position, and applied force. Functional homodonty is then defined as the degree to which teeth along the jaw all bear/exert similar stresses despite changes in shape. We find that morphologically heterodont teeth are often functionally homodont and that position is a better predictor of performance than shape. Furthermore, the arrangement of teeth affects their function, such that there is a functional advantage to having several smaller teeth surrounding a singular large tooth. We demonstrate that this arrangement of teeth is useful to grab, rather than tear, prey upon puncture, with the smaller teeth dissipating large stress forces around the larger tooth. We show that measurements of how shape affects stress distribution in response to loading give us a clearer picture of the evolution of conically shaped teeth. Teeth tell the tale of interactions between predator and prey. If a dental battery is made up of teeth that look similar, they are morphologically homodont, but if there is an unspecified amount of regional specialization in size or shape, they are morphologically heterodont. Functional homodonty is a statistical metric that lets us explore how different combinations of teeth work together.
Article
Synopsis Teeth lie at the interface between an animal and its environment and, with some exceptions, act as a major component of resource procurement through food acquisition and processing. Therefore, the shape of a tooth is closely tied to the type of food being eaten. This tight relationship is of use to biologists describing the natural history of species and given the high instance of tooth preservation in the fossil record, is especially useful for paleontologists. However, correlating gross tooth morphology to diet is only part of the story, and much more can be learned through the study of dental biomechanics. We can explore the mechanics of how teeth work, how different shapes evolved, and the underlying forces that constrain tooth shape. This review aims to provide an overview of the research on dental biomechanics, in both mammalian and non-mammalian teeth, and to synthesize two main approaches to dental biomechanics to develop an integrative framework for classifying and evaluating dental functional morphology. This framework relates food material properties to the dynamics of food processing, in particular how teeth transfer energy to food items, and how these mechanical considerations may have shaped the evolution of tooth morphology. We also review advances in technology and new techniques that have allowed more in-depth studies of tooth form and function.
Article
New World members of the Gobiesocinae (including Acyrtops, Acyrtus, Arcos, Derilissus, Gobiesox, Pherallodiscus, Rimicola, Sicyases, and Tomicodon) exhibit a heterodont oral dentition comprising two, and in some cases three, different types of teeth. The oral jaw teeth of New World gobiesocines are arranged in a series of 2-4 short staggered rows along the anterolateral margin of the premaxilla and dentary, to which new teeth are added posteriorly (rows 1-4) via shallow open crypts located along the labial margin of the jaw bones and medially (row 1 only) via one or two shallow open crypts located adjacent to the jaw symphysis. A putative monophyletic group comprising solely the New World genera of the Gobiesocinae is hypothesized based on characters of tooth arrangement and replacement in the oral jaws. The phylogenetic position of Eckloniaichthys, a homodont and the only Old World member of the Gobiesocinae, is discussed. The mode of tooth attachment in the Gobiesocidae is Type 2 (i.e., ring of collagen between tooth base and bone of attachment), and the mode of tooth replacement in the oral jaws is interpreted as intermediate between intraosseus and extraosseus replacement (sensu Trapani) and to take place in association with an internal cavity along the jaw bones. © 2015 by the American Society of Ichthyologists and Herpetologists.
Article
Adult Atlantic Wolffish, Anarhichas lupus, have a heterodont oral dentition consisting of long caniniform teeth in the symphysial regions of the dentaries and premaxillae and large molariform teeth posteriorly on the dentaries, dermopalatines, and vomer. Teeth are ankylosed to the bone of attachment. Wolffish use the caniniform teeth to capture prey including molluscs, crustaceans, echinoderms, and, less commonly, fishes. Prey are transported posteriorly and crushed between the molariform teeth. The molariform teeth of adults fit closely together despite individually variable shapes and sizes in a space-filling pattern that we term anamestic. Adult wolffish have an unusual tooth replacement pattern in which teeth are lost and subsequently replaced all at once, a pattern called simultaneous replacement. We used dissection, osteology, histology, and micro-computed tomography (CT) to study tooth replacement in a series of Anarhichas lupus from the western North Atlantic. Tooth development is intraosseous, with new tooth germs eroding into a specialized spongy portion of the bone of attachment. Simultaneous replacement involves extensive remodeling of this spongy bone. As planktonic larvae, wolffish have uniformly conical teeth, but relatively soon after settling a heterodont dentition similar to that of adults begins to develop. Juveniles exhibit a striking left-right symmetry of oral teeth and lack the anamestic pattern seen in adults. We compare tooth replacement in Atlantic Wolffish with that of Bluefish, Pomatomus saltatrix, another teleost with intraosseus tooth replacement. Patterns of intraosseous replacement in these taxa represent different evolutionary solutions to different ecological conditions, particularly diets. Not all teleosts with intraosseous tooth development are heterodont, but we predict that teleosts with heterodont dentitions will have intraosseous tooth development because this offers a way to provide attachment for functional teeth while replacement teeth are developing. © 2015 by the American Society of Ichthyologists and Herpetologists.
Article
Fish teeth can play several roles during feeding; capture, retention, and processing. In many fish lineages teeth may be present on non-jaw cranial bones that lack opposing teeth, such as the vomer and palatine. We hypothesized that teeth on different bones have different functions, and that the function of a set of teeth may vary over ontogeny. In this study, puncture, and draw performance of in situ vomerine teeth are compared to premaxillary teeth of the piscivorous lingcod, Ophiodon elongatus. The force required to pierce prey and to draw prey out of the mouth once the teeth were embedded was measured in ten individuals ranging from 205 to 836 mm SL to test for ontogenetic effects. Vomerine teeth in juvenile lingcod required proportionally less force to puncture prey items than adult lingcod, while premaxillary teeth showed the opposite trend. Draw force required to remove prey from the grasp of both toothed bones show the same shift with ontogeny. These results suggest that there is a shift in tooth function from vomerine to premaxillary teeth over ontogeny of lingcods. In juvenile lingcod, vomerine teeth function more effectively during initial puncture. In contrast, the premaxillary teeth pierce more effectively in adults. Juvenile lingcod are expected to use the premaxillary teeth while adult lingcod are expected to use the vomerine teeth to retain prey due to the larger force required for the prey to escape. The curvature of vomerine teeth increases over ontogeny suggesting increasing functional performance in retaining prey. J. Exp. Zool. 9999A:1–7, 2015. © 2015 Wiley Periodicals, Inc.
Article
Teeth are found in almost all vertebrates, and they therefore provide a general paradigm for the study of epithelial organ development and evolution. Here, we review the developmental mechanisms underlying changes in tooth complexity and tooth renewal during evolution, focusing on recent studies of fish, reptiles and mammals. Mammals differ from other living vertebrates in that they have the most complex teeth with restricted capacity for tooth renewal. As we discuss, however, limited tooth replacement in mammals has been compensated for in some taxa by the evolution of continuously growing teeth, the development of which appears to reuse the regulatory pathways of tooth replacement.
Article
Teleost fishes display a remarkable diversity of adult dentitions; this diversity is all the more remarkable in light of the uniformity of first-generation dentitions. Few studies have quantitatively documented the transition between generalized first-generation dentitions and specialized adult dentitions in teleosts. We investigated this transition in the Mexican tetra, Astyanax mexicanus (Characidae), by measuring aspects of the dentition in an ontogenetic series of individuals from embryos to 160 days old, in addition to adults of unknown age. The first-generation dentition and its immediate successors consist of small, unicuspid teeth that develop extraosseously. Multicuspid teeth first appear during the second tooth replacement event, and are derived from single tooth germs, rather than from the fusion of multiple conical tooth germs. We document that the transition from unicuspid to multicuspid teeth corresponds to a change in the location of developing tooth germs (from extraosseous to intraosseous) and in patterns of tooth replacement (from haphazard to simultaneous within a jaw quadrant). In addition, while the size of the largest teeth scales with positive allometry to fish size, the transition to multicuspid teeth is accompanied by an exceptionally large increase in tooth size. © 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 145, 523–538.
Article
The potentially molluscivorous East-African cichlid Astatoreochromis alluaudi is known to exhibit phenotypic plasticity in its pharyngeal jaw apparatus. We examined wild-caught (snail-eating) fish and specimens experimentally reared on soft food for differences in bone structure in their lower pharyngeal jaw (LPJ). The LPJ is built up of two halves, each of which consists of four structural units: a bony dentigerous, sutural and cortical plate, surrounding a medullary cavity containing sparse bone. Histomorphometric data and associated statistical analysis on serial microradiographs through the posterior third region of the LPJ, where crushing forces are assumed to be the highest, reveal differing growth trajectories: (1) compensating for fish size (standard length) the LPJ grows to a significantly larger size and volume in snail-eating specimens, (2) all structural units distinguished contribute to the volume increase of the LPJ in the hard versus the soft phenotype, and (3) the bone volume fraction in each of the units keeps pace with the growth of the unit proper, indicating that porosity does not change on one growth trajectory or from one phenotype to another. In addition, morphological observations show in hard food specimens: (1) the development of a structurally different bony layer along the inner side of the cortical plate, and (2) a reinforcement of the medullary cavity in the form of oriented trabeculae. Both are interpreted as a consolidation of the medullary cavity to resist the compressive forces exerted when hard food particles (mollusc shells) are crushed. © 1994 Wiley-Liss, Inc.
Article
Organogenesis depends upon a well-ordered series of inductive events involving coordination of molecular pathways that regulate the generation and patterning of specific cell types. Key questions in organogenesis involve the identification of the molecular mechanisms by which proteins interact to organize distinct pattern formation and cell fate determination. Tooth development is an excellent context for investigating this complex problem because of the wealth of information emerging from studies of model organisms and human mutations. Since there are no obvious sources of stem cells in adult human teeth, any attempt to create teeth de novo will probably require the reprogramming of other cell types. Thus, the fundamental understanding of the control mechanisms responsible for normal tooth patterning in the embryo will help us understand cell fate specificity and may provide valuable information towards tooth organ regeneration.
Article
Previous studies on tooth replacement in lower vertebrates have been plagued by a lack of common integrative approaches and methods making it impossible to furnish a phylogenetic synthesis. This study is based on serial sections of the jaw of Prionurus microlepidotus. Each Toothgerm was characterized by its developmental stage and its position in the jaw. The relationship between the developmental stage of toothgerm and position in the jaw has been studied and expressed in several graphical illustrations. The following conclusions have been made: (1) The initiation of toothgerms in P. microlepidotus is governed by two Zahnreihen, which respectively initiate toothgerms on the lingual and labial side of the functioning teeth in an alternating pattern. (2) Therefore, functioning teeth in one locus are supplied by the alternate eruption of lingual and lubial toothgerms. (3) Advancing of tooth replacement in each locus is independent of functioning teeth and their successors in adjacent loci. (4) The disorders of replacement patterns are caused by an alternated rate of eruption of successive toothgerms as a response to unusual shedding of the functioning teeth.
Article
The potentially molluscivorous cichlid fish Astatoreochromis alluaudi is known to exhibit a pronounced phenotypic plasticity in its pharyngeal jaw apparatus. Two phenotypes (wild-caught snail-eating specimens and specimens raised on soft food) were examined for differences in the number, size, shape, spacing and wear of functional teeth on the lower pharyngeal jaw. During growth, snail-eating specimens maintain tooth numbers but invest in teeth of a larger size (width and depth). In contrast, specimens fed a soft diet invest in more teeth, their size remaining unchanged except for the central, most posterior teeth. All changes in the dentition must be achieved through successive tooth generations. Serial microradiographs in the caudal area of the lower pharyngeal jaw, a region that is most significant in food processing, indicated that functional teeth in hard-food specimens more often show a successor below. This may be due to more time needed for larger replacement teeth to form and possibly to a shorter replacement cycle linked to the greater wear of the functional teeth. It is hypothesized that maintenance of tooth numbers and increase of tooth size in hard-food specimens is achieved by a one-for-one replacement and expansion of the tooth-bearing region and possibly by closer spacing of the teeth. Increase of tooth numbers in the soft-food specimens is probably achieved through the establishment of new tooth loci at the margins of the dentigerous area in addition to a one-for-one replacement.
Article
The diversity of tooth location in teleost fishes provides an excellent system for comparing genetic divergence between teeth in different species (phylogenetic homologs) with divergence between teeth within one species (iterative homologs). We have chosen to examine the expression of three members of the bone morphogenetic protein (Bmp) family because they are known to play multiple roles in tooth development and evolution in tetrapod vertebrates. We characterized expression of Bmp2a, Bmp2b, and Bmp4 during the development of oral and pharyngeal dentitions in three species of teleost fishes, the zebrafish (Danio rerio), Mexican tetra (Astyanax mexicanus), and Japanese medaka (Oryzias latipes). We found that expression in teleosts is generally highly conserved, with minor differences found among both iteratively homologous and phylogenetically homologous teeth. Expression of orthologous genes differs in several ways between the teeth of teleost fishes and those of the mouse, but between these vertebrate groups the summed expression pattern of Bmp genes is highly conserved. Significantly, the toothless oral region of the zebrafish lacks Bmp expression domains found in teleosts with oral teeth, implicating these genes in evolutionary tooth loss. We conclude that Bmp expression has been largely conserved in vertebrate tooth development over evolutionary time, and that loss of Bmp expression is correlated with region-specific loss of the dentition in a major group of fishes.
Article
Tooth shape is a hallmark of repeated evolutionary radiations among cichlid fishes from East Africa. Cusp shape and number vary both within populations and among closely related species with different feeding behaviors and ecologies. Here, we use histology and scanning electron microscopy to chart the developmental trajectory of tooth shape differences in fishes from Lake Malawi. We demonstrate that species with bi- or tricuspid adult (replacement) teeth initially possess a first-generation unicuspid dentition. Notably, the timing of turnover from first-generation to replacement teeth differs among species and is correlated with feeding ecology. Next, we use field data for cichlid species with adult unicuspid, bicuspid, and tricuspid teeth to demonstrate a strong and positive relationship between the number of teeth in a row and tooth shape. We discuss cichlid tooth ontogeny in the context of morphogenetic models designed to explain the developmental basis of tooth shape variation in mammals. We suggest that the dramatic differences in cichlid dentitions can be explained by variation in the expression of common activators and inhibitors acting at multiple stages of odontogenesis.
2021 Data from: The moment of tooth: rate, fate and pattern of Pacific lingcod dentition revealed by pulse-chase
  • E M Carr
  • A P Summers
  • K E Cohen
Carr EM, Summers AP, Cohen KE. 2021 Data from: The moment of tooth: rate, fate and pattern of Pacific lingcod dentition revealed by pulse-chase. Dryad Digital Repository. (doi:10.5061/dryad.fj6q573vt)