Development of the osteocranium in Corydoras aeneus (Gill, 1858) Callichthyidae,Siluriformes

Development in the osteocranium of Corydoras aeneus was studied based on 48 cleared and stained specimens and 10 series of serial sections. Development overall follows the general trends observed in siluriform development, with ossifications appearing as a response to functional demands. Early development of the skull occurs in two distinct phases. In a first phase, several new bony elements, all of dermal origin and related to feeding, appear shortly after yolk depletion (4.4 mm SL). Between 5 and 8 mm SL, developmental priorities seem to shift to size increase of the cartilaginous skull and no new bony elements appear. Finally, a second phase of osteogenesis occurs from 8 to 18 mm SL, in which all remaining dermal and perichondral bones appear. J. Morphol. 2011. © 2011 Wiley‐Liss, Inc.     

Skeletal development in the Chinese soft‐shelled turtle Pelodiscus sinensis (Testudines: Trionychidae)

We investigated the development of the whole skeleton of the soft‐shelled turtle Pelodiscus sinensis, with particular emphasis on the pattern and sequence of ossification. Ossification starts at late Tokita‐Kuratani stage (TK) 18 with the maxilla, followed by the dentary and prefrontal. The quadrate is the first endoskeletal ossification and appears at TK stage 22. All adult skull elements have started ossification by TK stage 25. Plastral bones are the first postcranial bones to ossify, whereas the nuchal is the first carapacial bone to ossify, appearing as two unstained anlagen. Extensive examination of ossification sequences among autopodial elements reveals much intraspecific variation. Patterns of ossification of cranial dermal elements are more variable than those of endochondral elements, and dermal elements ossify before endochondral ones. Differences in ossification sequences with Apalone spinifera include: in Pelodiscus sinensis the jugal develops relatively early and before the frontal, whereas it appears later in A. spinifera; the frontal appears shortly before the parietal in A. spinifera whereas in P. sinensis the parietal appears several stages before the frontal. Chelydrids exhibit an early development of the postorbital bone and the palatal elements as compared to trionychids. Integration of the onset of ossification data into an analysis of the sequence of skeletal ossification in cryptodirans using the event‐pairing and Parsimov methods reveals heterochronies, some of which reflect the hypothesized phylogeny considered taxa. A functional interpretation of heterochronies is speculative. In the chondrocranium there is no contact between the nasal capsules and planum supraseptale via the sphenethmoid commissurae. The pattern of chondrification of forelimb and hind limb elements is consistent with a primary axis and digital arch. There is no evidence of anterior condensations distal to the radius and tibia. A pattern of quasi‐ simultaneity is seen in the chondrogenesis of the forelimb and the hind limb. J. Morphol. 2009. © 2009 Wiley‐Liss, Inc.     

Osteocranial development in the viviparous surfperch Amphistichus argenteus (pisces: Embiotocidae)

The development of the cranial and branchial skeleton of the surfperch Amphistichus argenteus, a member of the family Embiotocidae, is described, and phylogenetic and functional aspects of the skull development of this species are discussed. The earliest bones to appear are those dermal elements of the branchial skeleton involved with feeding, and the bones, both dermal and endochondral, located in the basicranial region of the neurocranium. These are followed by dermal bones associated with the lateral line system and finally by the remainder of the bones of the branchial skeleton and the cartilaginous bones of the otic capsules. The last bone to develop is the ethmoid.     

The development of the osteocranium of Pleurodeles waltlii Michahelles

Under optimal conditions the development of the osteocranium covers the major part of the larval period and lasts about three and a half months. The earliest ossifications are of dermal origin and concern the tooth-bearing bones. The poorly developed enchondral ossifications found in Urodela, appear at a much later stage, just before metamorphosis.     

Postembryonic ontogeny of the spadefoot toad,Scaphiopus intermontanus (Anura: Pelobatidae): Skeletal morphology

Postembryonic skeletal ontogeny of the pelobatid frog Scaphiopus intermontanus is described based on a developmental series of cleared-and-stained, whole-mount specimens. The focus is on laboratory-reared individuals fed a herbivorous diet as larvae. Although there is variation in the timing of ossification of individual skeletal elements relative to developmental stages based on external morphological criteria, the sequence of skeletal development generally is conservative. Compared with its close relative, S. bombifrons, ossifications that occur during prometamorphosis tend to be slightly delayed in S. intermontanus; however, cranial bones that ossify during late metamorphic climax in S. intermontanus are delayed until postmetamorphosis in S. bombifrons. The differences in timing between the two species are consistent, however, with differences observed between two developmental series of S. intermontanus raised at two different temperatures. Noteworthy features of skeletal development in S. intermontanus include: 1) presence of palatine ossifications that form from independent centers of ossification and soon fuse with the postnarial portion of the vomers to form the compound vomeropalatine bones; 2) compound sphenethmoid that may arise from four or more endochondral centers of ossification and one dorsal, dermal center of ossification; and 3) presence of transverse processes and vestigal prezygapophyses on the first postsacral vertebra. The morphology of the larval orbitohyoideus and interhyoideus muscles is compared. The record of skeletal ontogeny and muscle morphology presented herein for the herbivorous larval morph can serve as a baseline for comparisons with the ontogeny of the carnivorous larval morph of Scaphiopus. J. Morphol. 238:179–244, 1998. © 1998 Wiley-Liss, Inc.     

Observations on the skulls of sturgeons (Acipenseridae): shared similarities of <Emphasis Type="Italic">Pseudoscaphirhynchus kaufmanni</Emphasis> and juvenile specimens of <Emphasis Type="Italic">Acipenser stellatus</Emphasis>

A novel hypothesis uniting Acipenser stellatus and Pseudoscaphirhynchus as sister groups has recently been proposed based on analysis of DNA sequences. In this paper I compare specimens of A. stellatus and P. kaufmanni, and show that they share several putatively derived similarities in the structure of their skulls, including: the presence of large spines on the dermal bones of skull; lateral extrascapular bones that enclose the confluence of the posttemporal, supratemporal, and otic sensory canals; elongate dorsal rostral bones; border rostral bones distinct in shape from dorsal rostral bones; greatly enlarged jugal that lacks a median flange; rostral canal bones that loop posteriorly at the anterior commissure of the rostral sensory canals; and the presence of an elongate, flat, and broad posterior ventral rostral bone. These similarities support a close relationship between A. stellatus and Pseudoscaphirhynchus, but still remain to be critically tested.     

Ontogeny of the osteocranium in the African catfish,Clarias gariepinus Burchell (1822) (Siluriformes: Clariidae): Ossification sequence as a response to functional demands

The ontogeny of the bony skull of the African catfish, Clarias gariepinus, is studied from initial ossification until a complete skull is formed. The ossification sequence in C. gariepinus seems to be related to the functional demands that arise in a developing larva. Early ossification of the opercular bone coincides with the initiation of opercular skin movements. Early ossifications involve several dentulous bones, formed shortly before the transition phase from endogenous to exogenous feeding. The enlarging branchiostegal membrane becomes supported by the gradual adding of branchiostegal rays. Parasphenoid ossification may be related to protection of the brain during prey transport, whereas the several hyoid bones, including the parurohyal, are formed in relation to the increasing loads exerted onto the tendons of the sternohyoideus and consequently onto the hyoid bar. Overall skull reinforcement occurs almost simultaneously, with a whole set of perichondral bones arising especially at places of high mechanical load. The suspensorium becomes protected against dislocation in an anteroposterior direction through a ligamentous connection, which even becomes partially ossified, forming the sesamoid entopterygoid. Later, the cranial lateral-line system becomes enclosed by a set of gutters, which close, frequently becoming plate-like later in ontogeny. The brain also becomes covered dorsally. Additional dentition (prevomeral tooth plates) formation seems to coincide with formation of the opercular four-bar system, as well as with the time the digestive system becomes completely functional. Eventually, unossified regions between the bones become closed off, fortifying and completely covering the skull. J. Morphol. 235:183–237, 1998. © 1998 Wiley-Liss, Inc.     

Variation and timing of the cranial ossification sequence of the oriental fire-bellied toad,Bombina orientalis (Amphibia,Discoglossidae)

The sequence of appearance of the 17 different skull bones in the oriental fire-bellied toad, Bombina orientalis, is described. Data are based primarily on samples of ten or 11 laboratory-reared specimens of each of 11 Gosner developmental stages (36–46) representing middle through late metamorphosis. Ossification commences as early as stage 37 (hind limb with all five toes distinct), but the full complement of adult bones is not attained until stage 46 (metamorphosis complete). Number of bones present at intermediate stages is poorly correlated with external morphology. As many as four Gosner developmental stages elapse before a given bone is present in all specimens following the stage at which it may first appear. The modal ossification sequence is frontoparietal, exoccipital, parasphenoid, septomaxilla, premaxilla, vomer, nasal, maxilla, angulosplenial, dentary, squamosal, quadratojugal, pterygoid, prootic, interfrontal, sphenethmoid, and mentomeckelian. Most specimens are consistent with this sequence, despite the poor correlation between cranial ossification and external development as assayed by Gosner stage. The timing of cranial ossification in Bombina orientalis differs in many respects from that described for two other, distantly related anurans, the leopard frog (Rana pipiens) and the western toad (Bufo boreas). These include the total number and sequence of appearance of bones, and the timing of ossification relative to the development of external morphology. Interspecific variation may reflect differences in the timing of the tissue interactions known to underlie skeletal differentiation and evolution.     

Development of the skull and pectoral girdle in Siberian sturgeon,Acipenser baerii,and Russian sturgeon,Acipenser gueldenstaedtii (Acipenseriformes: Acipenseridae)

The head is considered the major novelty of the vertebrates and directly linked to their evolutionary success. Its form and development as well as its function, for example in feeding, is of major interest for evolutionary biologists. In this study, we describe the skeletal development of the cranium and pectoral girdle in Siberian (Acipenser baerii ) and Russian sturgeon (A. gueldenstaedtii ), two species that are commonly farmed in aquaculture and increasingly important in developmental studies. This study comprises the development of the neuro‐, viscero‐ and dermatocranium and the dermal and chondral components of the pectoral girdle, from first condensation of chondrocytes in prehatchlings to the early juvenile stage and reveals a clear pattern in formation. The otic capsules, the parachordal cartilages, and the trabeculae cranii are the first centers of chondrification, at 8.4mm TL. These are followed by the mandibular, then the hyoid, and later the branchial arches. Teeth form early on the dentary, dermopalatine, and palatopterygoid, and then appear later in the buccal cavity as dorsal and ventral toothplates. With ongoing chondrification in the neurocranium a capsule around the brain and a strong rostrum are formed. Dermal ossifications start to form before closure of the dorsal neurocranial fenestrae. Perichondral ossification of cartilage bones occurs much later in ontogeny. Our results contribute data bearing on the homology of elements such as the lateral rostral canal bone that we regard homologous to the antorbital of other actinopterygians based on its sequence of formation, position and form. We further raise doubts on the homology of the posterior ceratobranchial among Actinopteri based on the formation of the hyoid arch elements. We also investigate the basibranchials and the closely associated unidentified gill‐arch elements and show that they are not homologous. J. Morphol. 278:418–442, 2017. © 2017 Wiley Periodicals, Inc.     

Comparative ossification and development of the skull in palaeognathous birds (Aves: Palaeognathae)

Ratites and tinamous are a morphologically diverse group of flightless and weakly flighted birds. As one of the most basal clades of extant birds, they are frequently used as an outgroup for studies discussing character evolution within other avian orders. Their skeletal development is not well known in spite of their important phylogenetic position, and studies have historically been plagued with small sample sizes and limited anatomical and temporal scope. Here, I describe the ossification of the skull in the emu (Dromaius novaehollandiae), ostrich (Struthio camelus), greater rhea (Rhea americana), and elegant crested‐tinamou (Eudromia elegans). Skeletal development is remarkably consistent within palaeognaths, in spite of large differences in absolute size and incubation period. Adult morphology appears to play a role in interordinal differences in the sequence and timing of ossification of certain bones. Neither the timing of cranial ossification events relative to stage nor the sequence of ossification events provides any evidence in support of a paedomorphic origin of the palaeognathous palate. This study provides an important first look at the timing and sequence of skull development in palaeognathous birds, providing data that can be compared to better‐studied avian systems in order to polarize ontogenetic characters. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 156 , 184–200.     

Inter‐ and intraspecific variation in the surface pattern of the dermal bones of two sturgeon species

Archaeological bone remains of sturgeon (Acipenser sturio/Acipenser oxyrinchus) from northwestern Europe are often identified to species on the basis of their surface morphology and then used to reconstruct the spatial distribution of the two species through time. The dermal bones of A. sturio are said to have an exterior surface pattern consisting of tubercles, while those of A. oxyrinchus are said to display alveoli. In the present paper, the validity of the surface pattern as a species‐specific characteristic is critically assessed. To this purpose, dermal plates from modern, genetically identified museum specimens were studied and the surface morphology observed in a series of archaeological remains was compared with the genetic identifications obtained on these same remains. The analyses show that the surface pattern of dermal bones is related to the size of the individual, with the pattern of small A. oxyrinchus being similar to that of A. sturio. In addition, variations in the surface pattern among the bones of a single individual and within the same bone have been observed. These findings explain previous conflicting results between morphological and genetic identifications and allow the formulation of some recommendations for more accurate morphological identification of isolated archaeological sturgeon dermal bones.     

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.     

Morphological novelty and modest developmental truncation in Barboides,Africa's smallest vertebrates (Teleostei: Cyprinidae)

Miniaturization, the evolution of extremely small adult body size, is widespread amongst animals and commonly associated with novel ecological, physiological, and morphological attributes. The phenotypes of miniaturized taxa are noteworthy because they combine reductions and structural simplifications with novel traits not developed in their larger relatives. Previous research on miniature cyprinid fishes (focused predominantly on South and South East Asian taxa of a single subfamily) has identified two distinct classes of miniature taxa: proportioned dwarves and developmentally truncated miniatures. Miniaturization has also occurred independently in the subfamily Cyprininae, particularly in African lineages. We investigate the skeletal anatomy of Barboides , a genus of miniature African cyprinids that includes Africa's smallest known species of vertebrates, to assess whether miniaturization has resulted in similar organismal outcomes in different lineages of the Cyprinidae. The skeleton of Barboides is characterized by the complete absence of a number of dermal and endochondral ossifications, and marked reduction in size and/or complexity of other skeletal elements, particularly those of the dermatocranium. Absent skeletal elements in Barboides include those which develop relatively late in the ossification sequence of the non‐miniature African relative ‘Barbus ’ holotaenia suggesting that their absence in Barboides can be explained by a simple scenario of developmental truncation. In contrast to this theme of loss and reduction, the os suspensorium of Barboides is enlarged and the outer arm distally trifid and associated with a novel bulbous muscle in males. An evaluation of the skeleton of Barboides provides further evidence for a link between developmental truncation and evolutionary morphological novelty in Cyprinidae. In the spectrum of miniature cyprinids ranging from proportioned dwarves with few bones missing to highly progenetic taxa with dozens of missing bones, the two species of Barboides range roughly in the middle showing that the extremes are connected by intermediate levels of truncatedness.     

A partial skeleton of <Emphasis Type="Italic">Cetorhinus parvus</Emphasis> Leriche, 1910 (Chondrichthyes,Cetorhinidae) from the Oligocene of Germany

A partial skeleton of a shark was found in the Frauenweiler clay pit near Rauenberg (Oligocene, Rupelian; Baden-Württemberg, S. Germany). The shark is identified as Cetorhinus parvus Leriche 1910. One tooth, vertebrae, dermal denticles and most of the filter apparatus of the juvenile specimen are described and illustrated. A terminology is introduced for the gill raker elements of the genus Cetorhinus to compare C. parvus and C. maximus.     

The development of cephalic armor in the tokay gecko (Squamata: Gekkonidae: Gekko gecko)

Armored skin resulting from the presence of bony dermal structures, osteoderms, is an exceptional phenotype in gekkotans (geckos and flap-footed lizards) only known to occur in three genera: Geckolepis, Gekko, and Tarentola. The Tokay gecko (Gekko gecko LINNAEUS 1758) is among the best-studied geckos due to its large size and wide range of occurrence, and although cranial dermal bone development has previously been investigated, details of osteoderm development along a size gradient remain less well-known. Likewise, a comparative survey of additional species within the broader Gekko clade to determine the uniqueness of this trait has not yet been completed. Here, we studied a large sample of gekkotans (38 spp.), including 18 specimens of G. gecko, using X-rays and high-resolution computed tomography for visualizing and quantifying the dermal armor in situ. Results from this survey confirm the presence of osteoderms in a second species within this genus, Gekko reevesii GRAY 1831, which exhibits discordance in timing and pattern of osteoderm development when compared with its sister taxon, G. gecko. We discuss the developmental sequence of osteoderms in these two species and explore in detail the formation and functionality of these enigmatic dermal ossifications. Finally, we conducted a comparative analysis of endolymphatic sacs in a wide array of gekkotans to explore previous ideas regarding the role of osteoderms as calcium reservoirs. We found that G. gecko and other gecko species with osteoderms have highly enlarged endolymphatic sacs relative to their body size, when compared to species without osteoderms, which implies that these membranous structures might fulfill a major role of calcium storage even in species with osteoderms.     

The pigs and “Old World peccaries” (Suidae and Palaeochoeridae,Suoidea, Artiodactyla) from the Miocene of Sandelzhausen (southern Germany): phylogeny and an updated classification of the Hyotheriinae and Palaeochoeridae

The fossil remains of two species of Suoidea (Artiodactyla, Mammalia) from the Early/Middle Miocene locality of Sandelzhausen (MN5; Bavaria, Germany) are described. A skull and some isolated teeth and bones reveal hitherto unknown features of Schizoporcus muenzenbergensis, Schizoporcini, Taucanaminae, Palaeochoeridae (Old World peccaries), Suoidea. The phylogeny of the Taucanaminae is discussed and an updated classification of the Palaeochoeridae is presented. The new names Schizoporcus and Schizoporcini replace the junior homonyms Schizochoerus Crusafont and Lavocat (1954) and Schizochoerini Golpe-Posse (1974). Remains of several skulls and mandibles, over 50 associated tooth rows, over 300 isolated teeth, and over 200 bones, constitute one of the largest collections of a Miocene suid known, and are assigned to Hyotherium soemmeringi wylensis, Hyotheriini, Hyotheriinae, Suidae (pigs), Suoidea. Hyotherium is the oldest certain suid genus known and many assumed it to be one of the most primitive. While the postcranial bones of the Suidae and Palaeochoeridae differ in many ways, the bones of Hyotherium are already very similar in morphology to those of living pigs, although they are much more slender, suggesting that the genus was more fleet-footed. Features related to rooting behaviour indicate that Hyotherium was a more efficient rooter than Palaeochoeridae and living Dicotylidae, but not as efficient as living suids. The phylogeny of the Hyotheriinae is discussed. The subfamily is divided into Hyotheriini and Aureliachoerini, new tribe, and an updated classification is presented.     

Pecularities of bony skeleton development in Asian clawed salamanders (Onychodactylus, Hynobiidae) related to embryonization

We studied skull, vertebral column, and limb skeleton development in Japanese clawed salamander Onychodactylus japonicus (Hynobiidae). The study is based on the ontogenetic series of embryos and larvae obtained from wild-captured adults by artificial induction of breeding using hormonal stimulation. The first stages of the skeleton formation in O. japonicus are shifted to the late embryonic period and hatching larvae already possess a well-ossified vertebral column, large number of skull ossifications and show signs of ossification in the forelimb skeleton. Compared to the primitive pattern of the skeleton development typical for other hynobiid salamanders, O. japonicus shows a number of heterochronies related to embryonization. In particular, this species is characterized by an earlier ossification of the vertebral column compared to that of the skull and by the delayed development and early reduction of the coronoid. Our results, along with the previously reported data on the skeleton development in the Fischer’s clawed salamander O. fischeri (Smirnov and Vassilieva, 2002), indicate that the genus Onychodactylus is characterized by the loss or reduction of several skeletal features typically found at early larval stages in other Hynobiidae species. In particular, provisional bones (especially the coronoid) and their dentition are underdeveloped. In addition, it is corroborated that the first tooth generation is absent in Onychodactylus, whereas such monocuspid nonpedicellate tooth generation normally develops at the early larval stages of other caudate amphibians. Since similar patterns of skeleton ontogeny are observed in other caudate groups with different extent of embryonization, it is proposed that, in different lineages of Urodela, the evolution of ontogeny followed similar pathways and was accompanied by the same changes in skeletogenesis.     

A heterochronic interpretation of the origin of digging adaptations in the northern water vole, Arvicola terrestris (Rodentia: Arvicolidae)

The Palaearctic genus Arvicola includes two species: the south‐western water vole A. sapidus, and the northern water vole A. terrestris. The latter has semiaquatic and/or subterranean populations, while populations of A. sapidus are always semiaquatic. According to the current phylogenetic and palaeontological data, adaptation to semiaquatic life is plesiomorphic for the genus Arvicola. We studied the ontogenetic allometry of skull and long bones of the semiaquatic A. sapidus, a semiaquatic population of A. terrestris (A. t. italicus), and two fossorial populations of A. terrestris (A. t. scherman and A. t. monticola). Animals from fossorial populations were smaller than were those from semiaquatic populations. We found that most of the ontogenetic allometric exponents of characters linked to digging in the skull and in the long bones were significantly higher in A. t. monticola, a fossorial clade, than they were in the semiaquatic populations. On the other hand, there may have been an evolutionary lag between invasion of the hypogeic habitat and the acquisition of fossorial adaptations in A. t. scherman. We showed statistically that the morphological differences linked to the invasion of a hypogeic habitat are already present in juvenile animals and, according to these results, suggest that these morphological differences are the direct expression of genetic changes rather than the outcome of epigenetic factors of mechanical origin. Moreover, we tried to ascertain whether the apomorphic shape of the skull and long bones in the fossorial populations of A. terrestris (compared with the primitive condition that would have been retained by the semiaquatic A. sapidus) are the outcome of a heterochronic process. Optimization by squared change parsimony supported the hypothesis of an apomorphic reduction of body size linked to the invasion of the subterranean habitat. The comparison of the ontogenetic trajectories of both skull shape and long bone shape suggested that a heterochronic process was involved in this morphological transformation. By using the ‘clock model’ method, this mechanism was identified as ‘accelerated dwarfism’ affecting both the skull and long bones. © 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 87 , 381–391.