Biting into the Genome to Phenome Map: Developmental Genetic Modularity of Cichlid Fish Dentitions

Within vertebrates, teleost fishes provide a rich evolutionary context for studying the mechanisms of dental divergence because of the numerous axes along which their teeth have diverged phenotypically and presumably developmentally. Using both a review of teleost in situ hybridization and de novo transcriptome sequencing in a cichlid fish, we examined whether 341 gene homologs thought to play a role in developing mice teeth are expressed in the tooth-bearing jaws of teleosts. The similarities and putative differences in gene expression documented between the two most commonly used models, zebrafish and cichlids, highlight what can be learned from using a greater diversity of teleost model systems in studies of tooth development. Both types of gene expression analysis also provide substantial evidence for conservation of tooth gene expression from teleosts to mammals as well as between initial and replacement teeth. Additionally, we found that the cichlid oral and pharyngeal jaws share expression for a large percentage of genes that influence tooth development. Our transcriptome analyses also suggest sub-functionalization between gene paralogs expressed in teeth and paralogs expressed in other structures is likely a common pattern across teleost diversity. Teleost dentitions will continue to provide a potent system in which to examine the importance of both gene duplication as well as the conservation of gene expression for phenotypic diversification

Morphology and distribution of taste papillae and oral denticles in the developing oropharyngeal cavity of the bamboo shark, Chiloscyllium punctatum.

Gustation in sharks is not well understood, especially within species that ingest food items using suction. This study examines the morphological and immunohistochemical characterisation of taste papillae and oral denticles in the oropharynx of the brown-banded bamboo shark Chiloscyllium punctatum and compares their distribution during development. Taste papillae of the brown-banded bamboo shark Chiloscyllium punctatum are located throughout the oropharyngeal region and are most concentrated on the oral valves (2,125-3,483 per cm(2) in embryos; 89-111 per cm(2) in mature adults) close to the tooth territories. Papillae appearance is comparable at all stages of development, with the exception of the embryos (unhatched specimens), where no microvilli are present. Oral valve papillae are comparable in structure to Type I taste buds of teleost fishes, whereas those of the rest of the oropharyngeal region are comparable to Type II. Both types of papillae show immunofluorescence for a number of markers of taste buds, including β-Catenin and Sox2. Taste papillae densities are highest in embryos with 420-941 per cm(2) compared to 8-29 per cm(2) in mature adults. The total number of papillae remains around 1,900 for all stages of development. However, the papillae increase in diameter from 72±1 µm in embryos to 310±7 µm in mature individuals. Microvilli protrude in multiple patches at the apical tip of the papilla covering ∼0.5% of the papillar surface area. We further document the relationship between taste papillae and the closely associated oral denticles within the shark orophayngeal cavity. Oral denticles first break through the epithelium in the antero-central region of the dorsal oral cavity, shortly after the emergence of teeth, around time of hatching. Denticles are located throughout the oropharyngeal epithelium of both immature and mature stages, with the highest concentrations in the antero-dorsal oral cavity and the central regions of the pharynx. These denticle-rich areas of the mouth and pharynx are therefore thought to protect the epithelium, and importantly the taste papillae, from abrasion since they correlate with regions where potential food items are processed or masticated for consumption. Taste papillae and denticles are more dense in anterior oropharyngeal regions in close association with the oral jaws and teeth, and in the juvenile/hatchling shark taste units are functional, and innervated, allowing the shark to seek out food in utero, at birth or on emergence from the egg case

Developing an ancient epithelial appendage: FGF signalling regulates early tail denticle formation in sharks

Background: Vertebrate epithelial appendages constitute a diverse group of organs that includes integumentary structures such as reptilian scales, avian feathers and mammalian hair. Recent studies have provided new evidence for the homology of integumentary organ development throughout amniotes, despite their disparate fnal morphologies. These structures develop from conserved molecular signalling centres, known as epithelial placodes. It is not yet certain whether this homology extends beyond the integumentary organs of amniotes, as there is a lack of knowledge regarding their development in basal vertebrates. As the ancient sister lineage of bony vertebrates, extant chondrichthyans are well suited to testing the phylogenetic depth of this homology. Elasmobranchs (sharks, skates and rays) possess hard, mineralised epithelial appendages called odontodes, which include teeth and dermal denticles (placoid scales). Odontodes constitute some of the oldest known vertebrate integumentary appendages, predating the origin of gnathostomes. Here, we used an emerging model shark (Scyliorhinus canicula) to test the hypothesis that denticles are homologous to other placode-derived amniote integumentary organs. To examine the conservation of putative gene regulatory network (GRN) member function, we undertook small molecule inhibition of fbroblast growth factor (FGF) signalling during caudal denticle formation. Results: We show that during early caudal denticle morphogenesis, the shark expresses homologues of conserved developmental gene families, known to comprise a core GRN for early placode morphogenesis in amniotes. This includes conserved expression of FGFs, sonic hedgehog (shh) and bone morphogenetic protein 4 (bmp4). Additionally, we reveal that denticle placodes possess columnar epithelial cells with a reduced rate of proliferation, a conserved characteristic of amniote skin appendage development. Small molecule inhibition of FGF signalling revealed placode development is FGF dependent, and inhibiting FGF activity resulted in downregulation of shh and bmp4 expression, consistent with the expectation from comparison to the amniote integumentary appendage GRN. Conclusion: Overall, these fndings suggest the core GRN for building vertebrate integumentary epithelial appendages has been highly conserved over 450 million years. This provides evidence for the continuous, historical homology of epithelial appendage placodes throughout jawed vertebrates, from sharks to mammals. Epithelial placodes constitute the shared foundation upon which diverse vertebrate integumentary organs have evolved

Shark tooth regeneration reveals common stem cell characters in both human rested lamina and ameloblastoma

The human dentition is a typical diphyodont mammalian system with tooth replacement of most positions. However, after dental replacement and sequential molar development, the dental lamina undergoes apoptosis and fragments, leaving scattered epithelial units (dental lamina rests; DLRs). DLRs in adult humans are considered inactive epithelia, thought to possess limited capacity for further regeneration. However, we show that these tissues contain a small proportion of proliferating cells (assessed by both Ki67 and PCNA) but also express a number of common dental stem cell markers (Sox2, Bmi1, β-catenin and PH3) similar to that observed in many vertebrates that actively, and continuously regenerate their dentition. We compared these human tissues with the dental lamina of sharks that regenerate their dentition throughout life, providing evidence that human tissues have the capacity for further and undocumented regeneration. We also assessed cases of human ameloblastoma to characterise further the proliferative signature of dental lamina rests. Ameloblastomas are assumed to derive from aberrant lamina rests that undergo changes, which are not well understood, to form a benign tumour. We suggest that dental lamina rests can offer a potential source of important dental stem cells for future dental regenerative therapy. The combined developmental genetic data from the shark dental lamina and ameloblastoma may lead to the development of novel methods to utilise these rested populations of adult lamina stem cells for controlled tooth replacement in humans

The dental lamina: an essential structure for perpetual tooth regeneration in sharks

In recent years non-classical models have emerged as mainstays for studies of evolutionary, developmental and regenerative biology. Genomic advances have promoted the use of alternative taxa for the study of developmental biology, and the shark is one such emerging model vertebrate. Our research utilizes the embryonic shark (Scyliorhinus canicula) to characterize key developmental and regenerative processes that have been overlooked or not possible to study with more classic developmental models. Tooth development is a major event in the construction of the vertebrate body plan, linked in part with the emergence of jaws. Early development of the teeth and morphogenesis is well known from the murine model, but the process of tooth redevelopment and regeneration is less well known. Here we explore the role of the dental lamina in the development of a highly regenerative dentition in sharks. The shark represents a polyphyodont vertebrate with continuously repeated whole tooth regeneration. This is presented as a major developmental shift from the more derived renewal process that the murine model offers, where incisors exhibit continuous renewal and growth of the same tooth. Not only does the shark offer a study system for whole unit dental regeneration, it also represents an important model for understanding the evolutionary context of vertebrate tooth regeneration

Effects of herbivory, nutrients, and reef protection on algal proliferation and coral growth on a tropical reef

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

Discriminating dynamical from additive noise in the Van der Pol oscillator

We address the distinction between dynamical and additive noise in time series analysis by making a joint evaluation of both the statistical continuity of the series and the statistical differentiability of the reconstructed measure. Low levels of the latter and high levels of the former indicate the presence of dynamical noise only, while low values of the two are observed as soon as additive noise contaminates the signal. The method is presented through the example of the Van der Pol oscillator, but is expected to be of general validity for continuous-time systems.Comment: 12 pages (Elsevier LaTeX class), 4 EPS figures, submitted to Physica D (4 july 2001

Modelling hand gestures to test leap motion controlled applications

Programs that use a Natural User Interface (NUI) are not controlled with a mouse and keyboard, but through input devices that monitor the user’s body movements. Manually testing applications through such interfaces is time-consuming. Generating realistic test data automatically is also challenging, because the input is a complex data structure that represents real body structures and movements. Previously, it has been shown that models learned from user interactions can be used to generate tests for NUI applications controlled by the Microsoft Kinect. In this paper, we study the case of the Leap Motion input device, which allows applications to be controlled with hand movements and finger positions, resulting in substantially more complex input data structures. We present a framework to model human hand data interacting with applications, and generate test data automatically from these models. We also evaluate the influence of the training data, as well as the influence of using a single model of the complete user data vs. multiple models for the different aspects of hand movement (e.g., finger positions, hand positions, hand rotations). Experiments on five applications controlled by the Leap Motion demonstrate that our approach generates effective test data. The quality and quantity of the training data used to derive the models is the main factor that determines their effectiveness. On the other hand, the effects of using multiple (as opposed to single) models are minor and application specific

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

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

Adsorption of CO in amorphous water-ice surfaces

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