Microstructural variation in conodont enamel is a functional adaptation

Recognition that conodonts were the earliest vertebrate group to experiment with skeletal biomineralization provides a window in which to study the origin and early evolution of this developmental system. It has been contended that the conodont skeleton comprised a classic suite of vertebrate hard tissues, while others suggest that conodont hard tissues represent divergent specializations within the early diversification of vertebrate hard tissues, supporting a view that the hard tissues of conodonts, particularly enamel, exhibit a range of microstructural variation beyond that seen in vertebrates. New evidence reveals that, although variable, conodont enamel microstructure is consistent between homologous portions of homologous dentitions. Although there is a correlation between morphology and microstructure, this belies a stronger correlation between the commonality of microstructure and dental function. The enamel of conodonts evolved in response to changes in dental function and differentiation of the microstructural layer into a number of enamel types and can be linked to dental occlusion, heterodonty, a permanent dentition, enamel thickness and, probably above all, the small size of the dental elements.     

Testing microstructural adaptation in the earliest dental tools

Conodont elements are the earliest vertebrate dental structures. The dental tools on elements responsible for food fracture—cusps and denticles—are usually composed of lamellar crown tissue (a putative enamel homologue) and the enigmatic tissue known as ‘white matter’. White matter is unique to conodonts and has been hypothesized to be a functional adaptation for the use of elements as teeth. We test this quantitatively using finite-element analysis. Our results indicate that white matter allowed cusps and denticles to withstand greater tensile stresses than do cusps comprised solely of lamellar crown tissue. Microstructural variation is demonstrably associated with dietary and loading differences in teeth, so secondary loss of white matter through conodont phylogeny may reflect changes in diet and element occlusal kinematics. The presence, development and distribution of white matter could thus provide constraints on function in the first vertebrate dental structures.     

Pseudooneotodusi a histological study of an Ordovician to Devonian vertebrate lineage

Detailed histological investigations have shed new light on the nature of Pseudooneotodus Drygant, 1974 (?Arenig/ljanvirn - Emsian). The genus has generally been interpreted as a conodont and is represented by squat phosphatic cones. These conodont dements show a differentiation into a lamellar cap, indistinguishable from vertebrate enamel, which is underlain by a spherulitic basal tissue with several characters indicative of dentine. The presence of these two issues in the elements of a conodont argues persuasively for the. vertebrate classification of the cladc, and illustrates that at least some conodonts have a hard tissue complex which is histologically indistinguishable from those of other primitive vertebrates. These observations have potentially important implications for conodont classification and the stratigraphic first appearances of vertebrate hard tissues.     

Evolution of morphogenesis in 360‐million‐year‐old conodont chordates calibrated in days

SUMMARY Highly rhythmic increments of crown tissue are identifiable in conodont oral apparatus elements from the Late Devonian of the Holy Cross Mountains, Poland; individual laminae being of thickness comparable with daily increments of vertebrate tooth enamel and fish otoliths. Abundant occurrence of such specimens enables bed‐by‐bed (stratophenetic) studies of the process of evolution at the population level and quantitative presentation of the evolution of ontogeny in the sampled geological section covering several million years. The morphologic transformation is expressed as expansion of a juvenile asymmetry to later stages of the ontogeny and in decrease of the mature element width, which was due to a change of the mineral tissue secretion rate. It was not just a simple extension of a juvenile character into the later stage of the ontogeny (heterochrony) but rather a true developmental novelty. The evolution was gradual and very slow. The proposed quantitative approach to growth increments in the mineral skeleton of ancient chordates introduces real‐time units to evolutionary developmental studies connected with direct paleontological evidence on the course of evolution.     

Skeletal ontogeny and feeding mechanisms in conodonts

The growth and function of the conodont skeletal apparatus have important implications for early vertebrate relationships and the evolution of vertebrate hard tissues, yet they are poorly understood. Analysis of element length, platform linear dimensions, and platform area in discrete Pa elements of Carboniferous Idiognathodus and Gnathodus bilineatus reveals that the platform increased in size at a rate significantly above that required to maintain geometric similarity. Measurements of P, M and S elements in bedding-plane assemblages of Idiognathodus and G. bilineatus indicate that relative to Pa element length, Pb and S element growth was isometric, whereas M elements grew with negative allometry. There is no evidence to support loss or resorption of S and M elements in later growth stages, or to indicate periodic shedding and replacement of elements. These results are important for understanding apparatus and element Function. The positive allometry of the Pa element platform supports interpretations of a mashing or grinding tooth-like Function for platformed Pa elements. If conodonts were active suspension-feeders, the increasing food requirements of a growing conodont would require the filter array formed by the S and M elements to have grown at a rate significantly above isometry. The lack of positive allometry of S and M elements indicates that conodonts were not suspension-feeders and supports hypotheses that conodonts fed with a raptorial apparatus and teeth. □ Conodonts, vertebrates, skeletal apparatus, ontogeny, allometry, function, suspension-feeding, teeth.     

Conodont affinity of the enigmatic Carboniferous chordate Conopiscius

Conopiscius shares V-shaped myomeres with the co-occurring conodont Clydagnathus but instead of a complex oral apparatus it has only a single pair of conical elements, and structures resembling scales are associated with its myomeres. Moreover, the coarsely crystalline crown tissue typical for conodonts has not been identified in the Conopiscius elements, which show only a finely lamellar skeletal tissue. The gap between conodonts and Conopiscius may be filled by isolated elements of similar morphology and structure occurring in the Late Devonian. They reveal a very thin external layer developed mostly at the tooth tip and resembling conodont crown tissue. The pulp cavity is partially filled with layered or spherulitic phosphatic tissue of the kind known also in conodonts (basal filling tissue) and early vertebrates (lamellin). Conodont elements of similar morphology and representing uni-membrate oral apparatuses have not been previously reported from the Devonian or Carboniferous but occur near the Cambrian–Ordovician transition ( Proconodontus ) and in the Late Permian ( Caenodontus ). It is proposed that Conopiscius represents a mostly cryptic conodont lineage extending from the Early Ordovician to the Permian, instead of being directly related to the agnathans.     

Early evolution of vertebrate skeletal tissues and cellular interactions, and the canalization of skeletal development

The stratigraphically earliest and the most primitive examples of vertebrate skeletal mineralization belong to lineages that are entirely extinct. Therefore, palaeontology offers a singular opportunity to address the patterns and mechanisms of evolution in the vertebrate mineralized skeleton. We test the two leading hypotheses for the emergence of the four skeletal tissue types (bone, dentine, enamel, cartilage) that define the present state of skeletal tissue diversity in vertebrates. Although primitive vertebrate skeletons demonstrate a broad range of tissues that are difficult to classify, the first hypothesis maintains that the four skeletal tissue types emerged early in vertebrate phylogeny and that the full spectrum of vertebrate skeletal tissue diversity is explained by the traditional classification system. The opposing hypothesis suggests that the early evolution of the mineralized vertebrate skeleton was a time of plasticity and that the four tissue types did not emerge until later. On the basis of a considerable, and expanding, palaeontological dataset, we track the stratigraphic and phylogenetic histories of vertebrate skeletal tissues. With a cladistic perspective, we present findings that differ substantially from long-standing models of tissue evolution. Despite a greater diversity of skeletal tissues early in vertebrate phylogeny, our synthesis finds that bone, dentine, enamel and cartilage do appear to account for the full extent of this variation and do appear to be fundamentally distinct from their first inceptions, although why a higher diversity of tissue structural grades exists within these types early in vertebrate phylogeny is a question that remains to be addressed. Citing recent evidence that presents a correlation between duplication events in secretory calcium-binding phosphoproteins (SCPPs) and the structural complexity of mineralized tissues, we suggest that the high diversity of skeletal tissues early in vertebrate phylogeny may result from a low diversity of SCPPs and a corresponding lack of constraints on the mineralization of these tissues.     

Formation of dermal skeletal and dental tissues in fish: a comparative and evolutionary approach

Osteichthyan and chondrichthyan fish present an astonishing diversity of skeletal and dental tissues that are often difficult to classify into the standard textbook categories of bone, cartilage, dentine and enamel. To address the question of how the tissues of the dermal skeleton evolved from the ancestral situation and gave rise to the diversity actually encountered, we review previous data on the development of a number of dermal skeletal elements (odontodes, teeth and dermal denticles, cranial dermal bones, postcranial dermal plates and scutes, elasmoid and ganoid scales, and fin rays). A comparison of developmental stages at the tissue level usually allows us to identify skeletogenic cell populations as either odontogenic or osteogenic on the basis of the place of formation of their dermal papillae and of the way of deposition of their tissues. Our studies support the evolutionary affinities (1) between odontodes, teeth and denticles, (2) between the ganoid scales of polypterids and the elasmoid scales of teleosts, and (3) to a lesser degree between the different bony elements. There is now ample evidence to ascertain that the tissues of the elasmoid scale are derived from dental and not from bony tissues. This review demonstrates the advantage that can be taken from developmental studies, at the tissue level, to infer evolutionary relationships within the dermal skeleton in chondrichthyans and osteichthyans.     

New insights into the ultrastructure, permeability, and integrity of conodont apatite determined by transmission electron microscopy

New crystalline structures have been observed in argon ion‐milled conodont elements from a diverse suite of Ordovician taxa (‘Cordylodus robustus’, Drepanoistodus suberectus, Panderodus gracilis, Plectodina? sp., Aphelognathus sp., Periodon aculeatus), using transmission electron microscopy (TEM). Electron diffraction patterns of albid tissue reveal that the component crystals are extraordinarily large, in the order of hundred(s) of microns. These large albid crystals show typical cancellate porosity, although a distinctly lamellar structure has also been observed within a large albid crystal positioned between hyaline lamellar and cancellate albid tissues. There is a distinct absence of ‘interlamellar space’ within all hyaline tissues examined, which are characterized by a polycrystalline matrix of micron‐scale elongate crystals that are both strongly aligned and tightly bound within a broader lamellar structure. Optical opacity, caused by light scattering within large (≥ 0.5 µm) pores, is also a feature of both albid and polycrystalline lamellar crown tissues. Accordingly, conodont hard tissues are differentiated by crystal size and shape, as well as inter‐ and intracrystalline porosity. These new observations highlight the structural complexities of conodont histologies and the need for more comprehensive investigations particularly of transitional crown tissues, which are not well defined by terms typically used in the literature. Their histological structures are interpreted to be a product of in vivo crystallization and thus provide new insights into the relative porosity, permeability, and inherent integrity of the tissues as well as their growth relationships. Accordingly, these data not only have implications for earlier histological and palaeobiological interpretations of conodont hard tissues but are also fundamental in determining their chemical integrity, which is crucial for characterizing palaeoseawater composition and palaeoenvironmental change. The potential for conodont apatite to retain primary chemical information depends on crystal size and permeability, so the large albid crystal domains are consistent with parallel geochemical studies that suggest that cancellate albid crown is more resistant to diagenetic modification.     

Evolutionary genetics of vertebrate tissue mineralization: the origin and evolution of the secretory calcium-binding phosphoprotein family

Three principal mineralized tissues are present in teeth; a highly mineralized surface layer (enamel or enameloid), body dentin, and basal bone. Similar tissues have been identified in the dermal skeleton of Paleozoic jawless vertebrates, suggesting their ancient origin. These dental tissues form on protein matrix and their mineralization is controlled by distinctive proteins. We have shown that many secretory calcium-binding phosphoproteins (SCPPs) are involved in tetrapod tissue mineralization. These SCPPs all originated from the common ancestral gene SPARCL1 (secreted protein, acidic, cysteine-rich like 1) that initially arose from SPARC. The SCPP family also includes a bird eggshell matrix protein, mammalian milk casein, and salivary proteins. The eggshell SCPP plays crucial roles in rigid eggshell production, milk SCPPs in efficient lactation and in the evolution of complex dentition, and salivary SCPPs in maintaining tooth integrity. A comparative analysis of the mammalian, avian, and amphibian genomes revealed a tandem duplication history of the SCPP genes in tetrapods. Although these tetrapod SCPP genes are fewer in teleost genomes, independent parallel duplication has created distinct SCPP genes in this lineage. These teleost SCPPs are also used for enameloid and dentin mineralization, implying essential roles of SCPPs for dental tissue mineralization in osteichthyans. However, the SCPPs used for tetrapod enamel and teleost enameloid, as well as tetrapod dentin and teleost dentin, are all different. Thus, the evolution of vertebrate mineralized tissues seems to be explained by phenogenetic drift: while mineralized tissues are retained during vertebrate evolution, the underlying genetic basis has extensively drifted.     

Growth and patterning in the conodont skeleton

Recent advances in our understanding of conodont palaeobiology and functional morphology have rendered established hypotheses of element growth untenable. In order to address this problem, hard tissue histology is reviewed paying particular attention to the relationships during growth of the component hard tissues comprising conodont elements, and ignoring a priori assumptions of the homologies of these tissues. Conodont element growth is considered further in terms of the pattern of formation, of which four distinct types are described, all possibly derived from a primitive condition after heterochronic changes in the timing of various developmental stages. It is hoped that this may provide further means of unravelling conodont phylogeny. The manner in which the tissues grew is considered homologous with other vertebrate hard tissues, and the elements appear to have grown in a way similar to the growing scales and growing dentition of other vertebrates.     

The SCPP gene repertoire in bony vertebrates and graded differences in mineralized tissues

The vertebrate tooth is covered with enamel in most sarcopterygians or enameloid in chondrichthyans and actinopterygians. The evolutionary relationship among these two tissues, the hardest tissue in the body, and other mineralized tissues has long been controversial. We have recently reported that specific combinations of secretory calcium-binding phosphoprotein (SCPP) genes are involved in the mineralization of bone, dentin, enameloid, and enamel. Thus, the early repertoire of SCPP genes would elucidate the evolutionary relationship across these tissues. However, the diversity of SCPP genes in teleosts and tetrapods and the roles of these genes in distinct tissues have remained unclear, mainly because many SCPP genes are lineage-specific. In this study, I show that the repertoire of SCPP genes in the zebrafish, frog, and humans includes many lineage-specific genes and some widely conserved genes that originated in stem osteichthyans or earlier. Expression analysis demonstrates that some frog and zebrafish SCPP genes are used primarily in bone, but also in dentin, while the reverse is true of other genes, similar to some mammalian SCPP genes. Dentin and enameloid initially use shared genes in the matrix, but enameloid is subsequently hypermineralized. Notably, enameloid and enamel use an orthologous SCPP gene in the hypermineralization process. Thus, the hypermineralization machinery ancestral to both enameloid and enamel arose before the actinopterygian–sarcopterygian divergence. However, enamel employs specialized SCPPs as structuring proteins, not used in enameloid, reflecting the divergence of enamel from enameloid. These results show graded differences in mineralized dental tissues and reinforce the hypothesis that bone–dentin–enameloid–enamel constitutes an evolutionary continuum. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Brief communication: Contributions of enamel‐dentine junction shape and enamel deposition to primate molar crown complexity

Molar crown morphology varies among primates from relatively simple in some taxa to more complex in others, with such variability having both functional and taxonomic significance. In addition to the primary cusps, crown surface complexity derives from the presence of crests, cuspules, and crenulations. Developmentally, this complexity results from the deposition of an enamel cap over a basement membrane (the morphology of which is preserved as the enamel‐dentine junction, or EDJ, in fully formed teeth). However, the relative contribution of the enamel cap and the EDJ to molar crown complexity is poorly characterized. In this study we examine the complexity of the EDJ and enamel surface of a broad sample of primate (including fossil hominin) lower molars through the application of micro‐computed tomography and dental topographic analysis. Surface complexity of the EDJ and outer enamel surface (OES) is quantified by first mapping, and then summing, the total number of discrete surface orientation patches. We investigate the relative contribution of the EDJ and enamel cap to crown complexity by assessing the correlation in patch counts between the EDJ and OES within taxa and within individual teeth. We identify three patterns of EDJ/OES complexity which demonstrate that both crown patterning early in development and the subsequent deposition of the enamel cap contribute to overall crown complexity in primates. Am J Phys Anthropol, 2010. © 2010 Wiley‐Liss, Inc.     

The Adaptive Significance of Enamel Loss in the Mandibular Incisors of Cercopithecine Primates (Mammalia: Cercopithecidae): A Finite Element Modelling Study

In several primate groups enamel is reduced or absent from the lingual (tongue) side of the mandibular incisor crowns akin to other placental and marsupial mammalian groups such as rodents, lagomorphs and wombats. Here we investigate the presumed adaptation of crowns with unilateral enamel to the incision of tough foods in cercopithecines, an Old World monkey subfamily, using a simulation approach. We developed and validated a finite element model of the lower central incisor of the rhesus macaque (Macaca mulatta) with labial enamel only to compute three-dimensional displacements and maximum principal stresses on the crown subjected to compressive loads varying in orientation. Moreover, we developed a model of a macaque incisor with enamel present on both labial and lingual aspects, thus resembling the ancestral condition found in the sister taxon, the leaf-eating colobines. The results showed that, concomitant with experimental results, the cercopithecine crown with unilateral enamel bends predominantly towards the inside of the mouth, while displacements decreased when both labial and lingual enamel are present. Importantly, the cercopithecine incisor crown experienced lower maximum principal stress on the lingual side compared to the incisor with enamel on the lingual and labial aspects under non-axial loads directed either towards the inside or outside of the mouth. These findings suggest that cercopithecine mandibular incisors are adapted to a wide range of ingestive behaviours compared to colobines. We conclude that the evolutionary loss of lingual enamel in cercopithecines has conferred a safeguard against crown failure under a loading regime assumed for the ingestion (peeling, scraping) of tough-skinned fruits.     

Enamel hypoplasia in the deciduous teeth of great apes: variation in prevalence and timing of defects

The prevalence of enamel hypoplasia in the deciduous teeth of great apes has the potential to reveal episodes of physiological stress in early stages of ontogenetic development. However, little is known about enamel defects of deciduous teeth in great apes. Unresolved questions addressed in this study are: Do hypoplastic enamel defects occur with equal frequency in different groups of great apes? Are enamel hypoplasias more prevalent in the deciduous teeth of male or female apes? During what phase of dental development do enamel defects tend to form? And, what part of the dental crown is most commonly affected? To answer these questions, infant and juvenile skulls of two sympatric genera of great apes (Gorilla and Pan) were examined for dental enamel hypoplasias. Specimens from the Powell‐Cotton Museum (Quex Park, UK; n = 107) are reported here, and compared with prior findings based on my examination of juvenile apes at the Cleveland Museum of Natural History (Hamman‐Todd Collection; n = 100) and Smithsonian Institution (National Museum of Natural History; n = 36). All deciduous teeth were examined by the author with a ×10 hand lens, in oblique incandescent light. Defects were classified using Fédération Dentaire International (FDI)/Defects of Dental Enamel (DDE) standards; defect size and location on the tooth crown were measured and marked on dental outline charts. Enamel defects of ape deciduous teeth are most common on the labial surface of canine teeth. While deciduous incisor and molar teeth consistently exhibit similar defects with prevalences of ～10%, canines average between 70–75%. Position of enamel defects on the canine crown was analyzed by dividing it into three zones (apical, middle, and cervical) and calculating defect prevalence by zone. Among gorillas, enamel hypoplasia prevalence increases progressively from the apical zone (low) to the middle zone to the cervical zone (highest), in both maxillary and mandibular canine teeth. Results from all three study collections reveal that among the great apes, gorillas (87–92%) and orangutans (91%) have a significantly higher prevalence of canine enamel defects than chimpanzees (22–48%). Sex differences in canine enamel hypoplasia are small and not statistically significant in any great ape. Factors influencing intergroup variation in prevalence of enamel defects and their distribution on the canine crown, including physiological stress and interspecific dento‐gnathic morphological variation, are evaluated. Am J Phys Anthropol 116:199–208, 2001. © 2001 Wiley‐Liss, Inc.     

Anatomical diversification of a skeletal novelty in bat feet

Neomorphic, membrane‐associated skeletal rods are found in disparate vertebrate lineages, but their evolution is poorly understood. Here we show that one of these elements—the calcar of bats (Chiroptera)—is a skeletal novelty that has anatomically diversified. Comparisons of evolutionary models of calcar length and corresponding disparity‐through‐time analyses indicate that the calcar diversified early in the evolutionary history of Chiroptera, as bats phylogenetically diversified after evolving the capacity for flight. This interspecific variation in calcar length and its relative proportion to tibia and forearm length is of functional relevance to flight‐related behaviors. We also find that the calcar varies in its tissue composition among bats, which might affect its response to mechanical loading. We confirm the presence of a synovial joint at the articulation between the calcar and the calcaneus in some species, which suggests the calcar has a kinematic functional role. Collectively, this functionally relevant variation suggests that adaptive advantages provided by the calcar led to its anatomical diversification. Our results demonstrate that novel skeletal additions can become integrated into vertebrate body plans and subsequently evolve into a variety of forms, potentially impacting clade diversification by expanding the available morphological space into which organisms can evolve.     

晚三叠世台形牙形刺分子的演化

晚三叠世台形牙形刺分子属有Ｐａｒａｇｏｎｄｏｌｅｌｌａ,Ｍｅｔａｐｏｌｙｇｎａｔｈｕｓ,Ａｎｃｙｒｏｇｏｎｄｏｌｅｌｌａ和Ｅｐｉｇｏｎｄｏｌｅｌｌａ。这些属都源于中三叠世,可能来自同一根源──Ｎｅｏｇｏｎｄｏｌｅｌｌａ,但有两个不同的演化趋向。本文认为这些台形分子分类演化上最重要的形态特征仅是一些微小的变化,如齿台下方后龙脊─基部附着面,基穴和环台面的细部变化。对Ｍｅｔａｐｏｌｙｇｎａｔｈｕｓ属台形分子的发展演化作了专门讨论,指出了晚三叠世台形牙形刺分子的演化系统。     

«Relative growth» from the dentino-enamel junction in primate maxillary molars

The dentino-enamel junction is critical throughout growth to mature crown configurations, being the interface between the papilla and the dental cap. Enamel deposition occurs relatively late and often causes changes from the pattern residing in the dentino-enamel junction. Primate teeth (mostly M¹) have been stripped of enamel after measurement and mapping of the original crown. Relative growth, a variant of static adult (allomorphic) allometries, is assessed by displacement of enamel basal crown component landmarks from dentine homologues relative to tooth size. The hypothesis that differential enamel growth reflects evolutionary history is supported by the positive allometry and shape differences in enamel versus dentine landmarks among phyletically enlarged and dentally-reduced primates.