Observations on tooth development and implantation in the upper pharyngeal jaws in Astatotilapia elegans (Teleostei,Cichlidae)

Prominent stages in the development of teeth, associated with the upper pharyngeal jaws in early postembryonic stages of the mouth brooding cichlid A statotilapia elegans were studied on semithin sections in relation to changes in the underlying endoskeletal parts and to the formation of the dentigerous bone. Because the pattern of tooth implantation on infrapharyngobranchial III-IV is constant, at least in early postembryonic stages, it is possible to trace the life history of a given tooth by tracing its homologue throughout the ontogenetic series. A probable causal relationship exists between tooth development and erosion of the underlying cartilage. Fully developed, though unerupted teeth, differentiate annular bone of attachment, which, depending on its position, is formed either outside the cartilage or within the previously induced erosion cavities. Attachment bone of adjacent teeth fuses to build up the dentigerous bone, which, as a result, may be situated within the area previously occupied by cartilage. As soon as the tooth has built up its bone of attachment, it may erupt. The collagenous matrix between tooth and attachment bone persists and gives rise to the movable connection between both. Differentiation of teeth on infrapharyngobranchial III-IV, together with enlargement of the dentigerous bone, proceeds from the lateral and the rostral border, where new germs constantly form. The appearance of new germs on infrapharyngobranchial II is more unpredictable.     

Ontogeny and phytogeny of the mesopodial skeleton in mosasauroid reptiles

Current phylogenics of mosasauroid reptiles are reviewed and a new phylogeny examining aigialosaur interrelationships presented. Patterns of mesopodial ossification and overall limb morphology are described for adult mosasauroids. Ossification sequences are mapped onto a phylogeny in order to assess the distribution of ontogenetic characters. Consistent and ordered distributions are found. Based on the phylogenetic distribution of ossification patterns, an overall mesopodial ossification sequence for mosasaurs is proposed. Carpal sequence: ulnare—distal carpal four (dc4)—intermedium—dc3—radiale or dc2—de1 or pisiform and dc5. Tarsal sequence: astragalus—distal tarsal four or calcaneum. Skeletal paedomorphosis is recognized as a dominant pattern in the evolution of mosasauroid limbs. Apomorphic characters of skeletal paedomorphosis, apparent in most taxa, reach extremes in tylosaurs. Arguments for the presence of a single proximal cartilage in the tarsus of mosasaurs are made. This cartilage is presumed to include ossification centres from which both the astragalus and calcaneum will ossify.     

Studies on skeleton formation in reptiles: Patterns of ossification in the skeleton of Chelydra serpentina (Reptilia, Testudines)

Patterns and sequence of ossification are described throughout the skeleton of Chelydra serpentina Linnaeus. Evidence is adduced documenting the decoupling of ossification processes from sequence and patterns of chondrification. Convergence of ontogenetic repatterning in the ossification of the axial skeleton in Chelydra and Squamata is discussed, as are problems of adaptive modification of ossification patterns. The development of a carapace may be correlated with changes of ossification patterns in the postcranial axial skeleton of turtles, but the most striking evidence for the adaptive modification of ossification sequence obtains from a comparison of the limb skeleton and its ossification in Chelydra and in sea turtles     

Appendicular skeletal morphology in minute salamanders,genus Thorius (amphibia: Plethodontidae): Growth regulation,adult size determination,and natural variation

Patterns of growth and variation of the appendicular skeleton were examined in Thorius, a speciose genus of minute terrestrial plethodontid salamanders from southern Mexico. Observations were based primarily on ontogenetic series of each of five species that collectively span the range of adult body size in the genus; samples of adults of each of seven additional species provided supplemental estimates of the full range of variation of limb skeletal morphology. Limbs are generally reduced, i.e., pedomorphic, in both overall size and development, and they are characterized by a pattern of extreme variation in the composition of the limb skeleton, especially mesopodial elements, both within and between species. Fifteen different combinations of fused carpal or tarsal elements are variably present in the genus, producing at least 18 different overall carpal or tarsal arrangements, many of which occur in no other plethodontid genus. As many as four carpal or tarsal arrangements were observed in single population samples of each of several; five tarsal arrangements were observed in one population of T. minutissimus. Left-right asymmetry of mesopodial arrangement in a given specimen is also common. In contrast, several unique, nonpedomorphic features of the limb skeleton, including ossification of the typically cartilaginous adult mesopodial elements and ontogenetic increase in the degree of ossification of long bones, are characteristic of all species and distinguish Thorius from most related genera. They form part of a mechanism of determinate skeletal growth that restricts skeletal growth after sexual maturity. Interspecific differences in the timing of the processes of appendicular skeletal maturation relative to body size are well correlated with interspecific differences in mean adult size and size at sexual maturity, suggesting that shifts in the timing of skeletal maturation provide a mechanism of achieving adult size differentiation among species. Processes of skeletal maturation that confer determinate skeletal growth in Thorius are analogous to those typical of most amniotes – both groups exhibit ontogenetic reduction and eventual disappearance of the complex of stratified layers of proliferating and maturing cartilage in long bone epiphyses – but, unlike most amniotes, Thorius lacks secondary ossification centers. Thus, the presence of secondary ossification centers cannot be used as a criterion for establishing determinate skeletal growth in all vertebrates.     

Phylogeny and biogeography of a large radiation of Andean lizards (Iguania, Stenocercus)

With 61 species occurring mostly in the Andes and adjacent lowland areas, Stenocercus lizards represent one of the most widespread and well-represented Andean vertebrate groups. Phylogenetic relationships among species of Stenocercus are inferred using different datasets based on mitochondrial DNA sequence data of 35 species and morphological data of 59 species. Among morphological data, polymorphic and meristic/morphometric characters are coded under the frequency parsimony and gap-weighting methods, respectively, and the accuracy of these methods is tested. When both types of characters are included, the resulting tree topology is more similar to the topologies obtained from analyses of DNA sequence data than those topologies obtained after exclusion of one or both types of characters. The phylogenetic hypotheses inferred including 59 species of Stenocercus (dataset 1) and excluding those species for which DNA data were not available (dataset 2) are generally congruent with each other, as well as with previously published hypotheses. The most parsimonious tree obtained from analysis of dataset 2 is used in a dispersal-vicariance analysis to infer ancestral areas and major biogeographical events. Species of Stenocercus are divided into two major clades. Clade A has diversified mostly in the central Andes, with a few species in the northern Andes and one species in the southern Andes. Clade B is more widespread, with species in the northern, central, and southern Andes, as well as in the Atlantic lowlands and Amazon basin. The most recent common ancestor of Stenocercus is inferred to have occurred in the eastern cordillera of the central Andes. Given morphological similarity and altitudinal distribution of some species nested in a northern-Andes clade, as well as the relatively recent uplift of this Andean region, it is possible that species in this clade have diverged as recently as the mid-Pliocene.     

Studies on skeleton formation in reptiles. I. The postembryonic development of the skeleton in Cyrtodactylus pubisulcus (Reptilia: Gekkonidae)

The study of ossification during postembryonic development of the lizard Cyrtodactylus pubisulcus reveals consistent patterns in the skeleton of the body axis and of the limbs. The vertebral column shows a distinct antero-posterior gradient in ossification; the serial homology of sacral ribs and caudal transverse processes with dorsal ribs requires further scrutiny. The sequence of ossification of carpal and tarsal elements is constant, yet different from the pattern of chondrification as described in the literature. The homology of a separate 'intermedium' in the ossified lizard carpus requires further discussion. The development of the lizard astragalus is discussed in detail, as is the ossification of epiphyses in the limbs.     

Chondrocranium and skeletal development of Phrynops hilarii (Pleurodira: Chelidae)

The present study represents the first comprehensive contribution to the knowledge of the skeletal development of a pleurodiran turtle, Phrynops hilarii (Pleurodira, Chelidae). The most remarkable features found are: (1) absence of ascending process on pterygoquadrate cartilage; (2) presence of ossification centres for the epiotics; (3) as in other pleurodirans, dorsal ribs IX and X are ‘sacralized’; (4) contact between ilium and carapace occurs later in ontogenetic development; (5) suture between ischia, pubes and plastron occurs in posthatching specimens; (6) contrary to previous interpretations, the phalangeal formula of the pes of P. hilarii is 2 : 3 : 3 : 3 : 5; (7) the hooked bone represents the fifth metatarsal.     

The evolution of development: two portraits of skull ossification in pipoid frogs

Abstract.— Development creates morphology, and the study of developmental processes has repeatedly shed light on patterns of morphological evolution. However, development itself evolves as well, often concomitantly with changes in life history or in morphology. In this paper, two approaches are used to examine the evolution of skull development in pipoid frogs. Pipoids have highly unusual morphologies and life histories compared to other frogs, and their development also proves to be remarkable. First, a phylogenetic examination of skull bone ossification sequences reveals that jaw ossification occurs significantly earlier in pipoids than in other frogs; this represents a reversal to the primitive vertebrate condition. Early jaw ossification in pipoids is hypothesized to result from the absence of certain larval specializations possessed by other frogs, combined with unusual larval feeding behaviors. Second, thin-plate spline morphometric studies of ontogenetic shape change reveal important differences between pipoid skull development and that of other frogs. In the course of frog evolution, there has been a shift away from salamander-like patterns of ontogenetic shape change. The pipoids represent the culmination of this trend, and their morphologies are highly derived in numerous respects. This study represents the first detailed examination of the evolution of skull development in a diverse vertebrate clade within a phylogenetic framework. It is also the first study to examine ossification sequences across vertebrates, and the first to use thin-plate spline morphometrics to quantitatively describe ontogenetic trajectories.     

Description of the adult skeleton and developmental osteology of the hyperossified horned frog,Ceratophrys cornuta (Anura: Leptodactylidae)

The adult skeleton and tadpole chondrocranium of the leptodcatylid frog, Ceratophrys cornuta (Ceratophryinae), are described in detail, including the ontogenetic development of the chondrocanium and the ossification sequence of the skeleton. The chondrocranium of the carnivorous larvae is unique in lacking a frontoparietal fontanelle and possessing a complete dorsal roof of cartilage. Furthermore, the chondrocranium is extremely robust, particularly those elements involved in the feeding mechanism; these include large palatoquadrate cartilages, stout Meckel's, supra- and infrarostral cartilages, and short, wide, cornua trabeculae. The chondrocranium of C. cornuta resembles that described for Ceratophrys cranwelli, but differs from the chondrocrania reported for the species of Lepidobatrachus. The large adult skull is hyperossified; most elements are fused into a single unit, and nearly all dermal elements are ornamented, casqued, and co-ossified. Calcification is present in nearly every cartilaginous element of the skeleton in larger (older) adults. Several osteological characters previously used in ceratophryine systematics, such as the otic ramus of the squamosal and the columella, are reassessed. Contrary to previous reports, the ossified, dorsal dermal shield above the vertebral column in many ceratophryine anurans is absent in C. cornuta. With few exceptions, the ossification sequence relative to metamorphosis is consistent with those that are known for other anurans. The squamosal arises from three distinct centers of ossification, including an otic element. The frontoparietal arises from two centers of ossification that fuse early in development. A robust postorbital arch is formed primarily by the otic flange of the frontoparietal, which articulates laterally with the medial border of the otic ramus of the squamosal. Changes in the timing of development, or heterochrony, are involved with the evolution of the unusual skull and skeleton of ceratophryine frogs. J Morphol 232:169–206, 1997. © 1997 Wiley-Liss, Inc.     

Ossification and midline shape changes of the human fetal cranial base

An appreciation of ontogenetic changes to the cranial base is important for understanding the evolution of modern human skull form. Using geometric morphometric techniques, this study explores midline shape variations of the basicranium and midface during human prenatal ontogeny. In particular, the analysis sets out to explore shape variations associated with endochondral ossification and to reassess shape variations previously observed on the basis of angular measures.Fifty-four formalin-preserved human fetuses were imaged using high-resolution MRI. Coordinates for 10 landmarks defining the midline basicranium and midface were acquired and areas of ossification in the midline basioccipital, basisphenoid, and presphenoid cartilages were measured as percentages of overall cranial base area. The results show shape variations with increasing fetal size that are consistent with cranial base retroflexion, anterior facial projection and dorsal facial rotation. These growth variations are centered on the midsphenoid area and are associated with disproportionate variations of sphenoid height and length. Small but significant correlations were observed between ossification of the presphenoid cartilage and components of shape that described, among other variations, sphenoid shortening. While ossification cannot be directly linked with the shape variations observed, it seems likely that bone formation plays a role in modulating the influence of other factors on the fetal cranial base.     

The origin and early development of the clavicle in the quail (Coturnix c. japonica)

Development of the clavicle in the Japanese quail is described in detail and evidence presented for its development in cartilage. Chondroblast cells and the chondroitin sulphate of the cartilage matrix are identified using a toluidine blue-silver impregnation technique. It was found that the cartilage phase is transitory and is rapidly obliterated by the ossification stage. An initial invasion of the cartilage by osteoblasts is followed by deposition of granules of calcified material scattered randomly in the cartilage in the region of the ramus. In the hypocleideum, however, the calcification is initially perichondral, as seen in the initial ossification of the coracoid, but later resembles that of the clavicular ramus, in being random. The pattern of chondrogenesis and'osteogenesis seen in the clavicle suggests an acceleration of the normal process of endochondral ossification with an abbreviation of the cartilage phase. This study reveals that the development of the clavicle in this bird is not dissimilar (as is generally accepted) to that of other skeletal elements of the primary pectoral girdle.     

The angular process of Monodelphis domestica (Didelphidae, Marsupialia) and its relation to the middle ear: an ontogenetic and evolutionary morphologic study

In most marsupials, the angular process is inflected medially. By using an ontogenetic series of Monodelphis domestica, the development of this characteristic structure has been described. In contrast with the eutherian mammals, in marsupials there is retained a close connection between the dentale and the tympanicum and goniale; it is well known that these 2 elements of the middle ear are derived from the angulare and prearticulare of the reptilian lower jaw. At the neonatal stage, the dentale and tympanicum are both relatively vertically orientated; during the following 2 weeks, they take an increasingly oblique position, which is primarily caused by the rapid growth of the braincase. Only after the eruption of the first teeth, the ascending ramus of the dentale takes a more and more vertical position, whereas the angular process remains with its tip near the medioventral floor of the tympanic bulla. The bulla shows at this place a rectangular fenestra which is covered by a membrane of loose connective tissue; the tip of the angular process, which is always free of muscular insertions, maintains contacts with this fenestra throughout life. During juvenile and adult life stages, the process becomes somewhat removed from the fenestra for obvious reasons, but at a gape of about 40 to 50 degrees it inevitably must touch the "inferior tympanic membrane" and possibly also the tympanic ring. It is speculated that the relationship between the angular process and the tympanic bulla represents a specific form-function complex for sound transmission, which may be a modified retention from archaic mammalian conditions. Further details of the ontogenetic development of the tympanic region have been described which may be of some relevance for the evolutionary morphology of mammals: The tympanic process of the petrosal, which fixes the posterior end of the tympanic ring, is formed by 'Zuwachsknochen' (additional bone) but not by cartilage. The styloid process remains cartilaginous throughout life: its free tip ends in the lateral wall of the tympanic cavity and it is closely connected with the collum mallei and the posterior end of the tympanicum; it guides the chorda tympani and may therefore be homologous with the cartilage of Spence. The cartilage of Paauw is interpreted in terms of functional morphology. A model of evolutionary transformation of the dentale-tympanicum complex in mesozoic mammals in outlined on the basis of the ontogenetic findings in Monodelphis and other didelphid and dasyurid marsupials.     

The morphology and post-hatching development of the skull of Bolitoglossa nicefori (Caudata: Plethodontidae): developmental implications of recapitulation and repatterning

The cranial morphology of the direct-developing salamander Bolitoglossa nicefori and its post-hatching development are described and compared with that of other urodeles. Four stages of cranial development are defined on the basis of conspicuous events that occur during post-hatching ontogeny. The adult skull morphology of B. nicefori is similar to that of other plethodontids; however, some regions show interspecific variation. The post-hatching ontogeny of the skull and the stage of ossification observed in the hatchlings of B. nicefori show two important ontogenetic features: (1) a mosaic of early larval, metamorphic and post-metamorphic skull features in hatchlings, and (2) absence of characteristic larval elements in skull and hyoid apparatus. The distinctive stage of ossification in the hatchlings of B. nicefori could be caused by heterochronic changes in the ossification sequence, compared to the ontogeny of metamorphic salamanders. The possible heterochronic changes and the absence of larval traits are perhaps due to ontogenetic repatterning, yet without an obvious impact on the adult skull morphology (absence of morphological novelties). This might indicate a compartmentalized development. Further studies should be performed in order to establish the possible occurrence of recapitulatory patterns or ontogenetic repatterning in the skull morphogenesis of B. nicefori during its embryonic development.     

Senile features in the skeleton of an aged Japanese monkey

The senile features in the skeleton of a male Japanese monkey, who is presumed to be about 40 years old, were examined in comparison with younger individuals. As for the skull, every part is constructed solidly, and the sutures around the temporal and parietal bones are for the most part closed. In the dentition many of the front teeth are destroyed or lost, and the cheek teeth are severely worn. In the vertebrae, the annular epiphyseal discs unite completely with the body at its anterior and posterior surfaces, and the porosity and deformation of the bodies are remarkable. The hip bones, in the pelvis, unite with each other by solid ossification of the pubic symphysis. The long bones of the anterior and posterior limbs are marked by their general thickness, the rugged increase of bone around the joints, especially in the arms, and the complete union of each epiphysis with the shaft through the ossification of the epiphyseal cartilage. These senile features furnish a clue as to the establishment of a criterion for age estimation in Japanese monkeys.This observation was briefly reported inMonkey Vol. 13, No. 1, 1969, and Fig. 9 was used there.     

Phylogenetic relationships of South American lizards of the genus Stenocercus (Squamata: Iguania): A new approach using a general mixture model for gene sequence data

The South American iguanian lizard genus Stenocercus includes 54 species occurring mostly in the Andes and adjacent lowland areas from northern Venezuela and Colombia to central Argentina at elevations of 0-4000m. Small taxon or character sampling has characterized all phylogenetic analyses of Stenocercus, which has long been recognized as sister taxon to the Tropidurus Group. In this study, we use mtDNA sequence data to perform phylogenetic analyses that include 32 species of Stenocercus and 12 outgroup taxa. Monophyly of this genus is strongly supported by maximum parsimony and Bayesian analyses. Evolutionary relationships within Stenocercus are further analyzed with a Bayesian implementation of a general mixture model, which accommodates variability in the pattern of evolution across sites. These analyses indicate a basal split of Stenocercus into two clades, one of which receives very strong statistical support. In addition, we test previous hypotheses using non-parametric and parametric statistical methods, and provide a phylogenetic classification for Stenocercus.     

Development of the cranium and paired fins in the zebrafish Danio rerio (Ostariophysi,Cyprinidae)

Because of the genetic and developmental information available, Danio rerio stands out as a vertebrate model system in which significant progress in the areas of development and evolution can be made. Despite its increasing popularity, little research has been done on skeletal development. In this report, we provide developmental information on the structure and composition of the zebrafish skull, pectoral, and pelvic girdle. We describe the sequence of ossification of the skull and paired fins from a large series of cleared and Alizarin red-stained specimens at larval and adult stages. The most commonly followed developmental sequence in Danio rerio is described. Chondrocranial development is noted from Alcian blue-stained specimens. General trends in ossification patterns are examined from developmental, phylogenetic, and functional contexts. No clear pattern in ossification order of dermal versus cartilage bones is evident. Ossification sequence conforms to functional need in a general way, but there are inconsistencies in the details of order. Selected phylogenetic comparisons of ossification sequence within cranial regions are made among Danio rerio, Betta splendens, Oryzias latipes, and Barbus barbus. Greater sequence conservation is apparent between D. rerio and Barbus barbus, the ostariophysans, than among other taxon pairs. Intraspecific variation in ossification order is apparent, most of which involves small adjustments in timing. © 1996 Wiley-Liss, Inc.     

Ontogenetic Sequence Analysis: using parsimony to characterize developmental sequences and sequence polymorphism

Ontogenetic sequences are a pervasive aspect of development and are used extensively by biologists for intra- and interspecific comparisons. A tacit assumption behind most such analyses is that sequence is largely invariant within a species. However, recent embryological and experimental work emphasizes that ontogenetic sequences can be variable and that sequence polymorphism may be far more prevalent than is generally realized. We present a method that uses parsimony algorithms to map hierarchic developmental patterns that capture variability within a sample. This technique for discovering and formalizing sequences is called the "Ontogenetic Sequence Analysis" (OSA). Results of OSA include formalized diagrams of reticulating networks, describe all most parsimonious sequences, and can be used to develop statistics and metrics for comparison of both intraspecific and interspecific sequence variation. The method is tested with examples of human postnatal skeletal ossification, comprising a time-calibrated data set of human hand and wrist epiphyseal unions, and a longitudinal data set of human wrist ossification. Results illustrate the validity of the method for discovering sequence patterns and for predicting morphologies not represented in analytic samples. OSA demonstrates the potential and challenges of incorporating ontogenetic sequences of morphological information into evolutionary analyses.     

Fetal growth and development of the coypu (Myocastor coypus): Prenatal growth,tooth eruption,and cranial ossification

We examined the fetal growth and development of the coypu (Myocastor coypus), a member of the Caviomorpha that produces extremely precocial young. Analyses of 69 fetuses derived from the latter half of the prenatal period (60–125 days of gestation) focused on external feature growth and development, tooth eruption, and cranial ossification. There were four developmental stages based on morphological characteristics; major external changes predominated over somatic growth in the early stages by 100–105 days of gestation, whereas the last stage was a time of rapid somatic growth. Growth rate was greater in hind foot length (4.3) than in fore foot length (3.4). Soft X-ray photos from 120 to 125 days of gestation show that the incisors, premolars, and first molars were completely calcified, and the second molars were present in the alveolus but not completely calcified. The occlusal surfaces of these teeth were subjected to wear. We analyzed the bone and cartilage of the coypu fetal cranium using a double-staining method. Early ossification of the jugular processes of the occipital bone was a prominent feature of coypu development. The digastric muscle originates on the jugular process, and early ossification should be linked to an adaptation to the herbivorous habit of weaned young coypu. Additionally, the sizes and closure times of six fontanelles are correlated with gestational age and are suggested as a comparative parameter for fetal maturity within and between mammalian species.     

Dynamic 3D culture: Models of chondrogenesis and endochondral ossification

The formation of cartilage from stem cells during development is a complex process which is regulated by both local growth factors and biomechanical cues, and results in the differentiation of chondrocytes into a range of subtypes in specific regions of the tissue. In fetal development cartilage also acts as a precursor scaffold for many bones, and mineralization of this cartilaginous bone precursor occurs through the process of endochondral ossification. In the endochondral formation of bones during fetal development the interplay between cell signalling, growth factors, and biomechanics regulates the formation of load bearing bone, in addition to the joint capsule containing articular cartilage and synovium, generating complex, functional joints from a single precursor anlagen. These joint tissues are subsequently prone to degeneration in adult life and have poor regenerative capabilities, and so understanding how they are created during development may provide useful insights into therapies for diseases, such as osteoarthritis, and restoring bone and cartilage lost in adulthood. Of particular interest is how these tissues regenerate in the mechanically dynamic environment of a living joint, and so experiments performed using 3D models of cartilage development and endochondral ossification are proving insightful. In this review, we discuss some of the interesting models of cartilage development, such as the chick femur which can be observed in ovo, or isolated at a specific developmental stage and cultured organotypically in vitro. Biomaterial and hydrogel‐based strategies which have emerged from regenerative medicine are also covered, allowing researchers to make informed choices on the characteristics of the materials used for both original research and clinical translation. In all of these models, we illustrate the essential importance of mechanical forces and mechanotransduction as a regulator of cell behavior and ultimate structural function in cartilage. Birth Defects Research (Part C) 105:19–33, 2015. © 2015 Wiley Periodicals, Inc.