Development and tissue origins of the mammalian cranial base

The vertebrate cranial base is a complex structure composed of bone, cartilage and other connective tissues underlying the brain; it is intimately connected with development of the face and cranial vault. Despite its central importance in craniofacial development, morphogenesis and tissue origins of the cranial base have not been studied in detail in the mouse, an important model organism. We describe here the location and time of appearance of the cartilages of the chondrocranium. We also examine the tissue origins of the mouse cranial base using a neural crest cell lineage cell marker, Wnt1-Cre/R26R, and a mesoderm lineage cell marker, Mesp1-Cre/R26R. The chondrocranium develops between E11 and E16 in the mouse, beginning with development of the caudal (occipital) chondrocranium, followed by chondrogenesis rostrally to form the nasal capsule, and finally fusion of these two parts via the midline central stem and the lateral struts of the vault cartilages. X-Gal staining of transgenic mice from E8.0 to 10 days post-natal showed that neural crest cells contribute to all of the cartilages that form the ethmoid, presphenoid, and basisphenoid bones with the exception of the hypochiasmatic cartilages. The basioccipital bone and non-squamous parts of the temporal bones are mesoderm derived. Therefore the prechordal head is mostly composed of neural crest-derived tissues, as predicted by the New Head Hypothesis. However, the anterior location of the mesoderm-derived hypochiasmatic cartilages, which are closely linked with the extra-ocular muscles, suggests that some tissues associated with the visual apparatus may have evolved independently of the rest of the “New Head”.     

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.     

Development of the cranium and paired fins in Betta splendens (Teleostei: Percomorpha): Intraspecific variation and interspecific comparisons

The development of the chondrocranium and the relative timing of ossification of the osteocranium is described in the teleost fish Betta splendens from a large series of cleared and differentially stained specimens. General trends in ossification patterns are examined from developmental, phylogenetic, and functional contexts. As in many other vertebrates, dermal bones form before cartilage bones. Ossification sequence conforms to functional need in a very general way, but there are many inconsistencies in the details of order. For example, some bones that are directly involved in feeding ossify no earlier than bones more indirectly involved. Comparisons of ossification sequence within specific cranial regions are made among Betta splendens, Oryzias latipes (Atherinomorpha), and Barbus barbus (Ostariophysi) within a phylogenetic framework. Many evolutionary changes in relative sequence of ossification are evident within regions among these taxa, yet many other sequences are conserved. The logistic difficulty of comparing entire cranial ossification sequences (vs. regional sequences) makes evident the need for new methods for identifying and quantifying sequence changes. Intraspecific variation in order of ossification is described for the first time in teleost fishes. To the extent that ossification sequence varies intraspecifically, conclusions drawn from previous interspecific comparisons are compromised. Understanding the importance of changes in ossification order within and among taxa will require experimental, functional, and evolutionary work. © 1996 Wiley-Liss, Inc.     

Patterns of chondrification and ossification in the skull of Graptemys pseudogeographica,the false map turtle (Emydidae)

Patterns of ossification and chondrification are well‐described for several species of turtles, but details of the chondrocranial anatomy are known for only a handful of species. Cleared and double‐stained embryos of Graptemys pseudogeographica were used to examine the fully formed chondrocranium and the formation, chondrification, and ossification of the cranium. The chondrocranium of G. pseudogeographica possesses an unusually large, irregularly shaped foramen epiphaniale that is joined with the fenestra olfactoria. As in other emydids, and many turtles generally, the taenia marginalis is present only as a small projection and the taenia medialis is lacking in mature stages of embryonic development. Ossification data for G. pseudogeographica are consistent with those of other Testudines in that the dentary and maxilla (dermal elements of the upper and lower jaws) ossify early, whereas the articular (an endochondral bone of the lower jaw) ossifies relatively late. Additionally, comparative ossification shows that the vomer is quite variable in its relative timing of ossification across Testudines.     

The ontogeny of the chondrocranium in Clarias gariepinus: trends in siluroids

The ontogeny of the chondrocranium of 31 different stages of the African catfish Clarias gariepinus (Siluroidei: Clariidae) was studied, both from cleared and stained, and sectioned material. The fish ranged from 4.1 (1 day post-hatching) to 127.0 mm SL (100 days post-hatching). The chondrocranium of C. gariepinus seemed to correspond to the general adaptive trends in siluroids, especially in relation to the reduction of eye size and the dorso-ventral flattening of the skull. The platybasic neurocranium involved several modifications related to the trabecular bars, the hypophyseal fenestra, the ethmoid region and even the olfactory nerves. Certain reductions were present, which have been observed in all siluroids (e.g. absence of the pila lateralis, the commissura lateralis, the myodomes) or are part of a variable trend within siluroids (e.g. reduction of the taenia marginalis anterior and the tectum synoticum). Compared with some other siluroid species, the neurocranium of C. gariepinus is well developed, for example in the otic region. The same was observed in the splanchnocranium where some general siluroid trends persist (e.g. isolation of palatine from pterygoquadrate, presence of 'hyo-symplectic-pterygoquadrate' plate). Some trends, as observed in other siluroids, were present also (e.g. interhyal continuous with suspensorium and ceratohyal, Meckel's cartilage initially continuous with the suspensorium). The branchial basket is well developed as all expected elements are present (basibranchials I-IV, hypobranchials I-IV, ceratobranchials I-V, epibranchials I-IV). Based on the observed ontogeny of C. gariepinus and data from the literature, a hypothesis was formulated which indicated the presence of a general reductional trend within siluroids. In C. gariepinus , all four (I-IV) infrapharyngobranchials develop, although the anterior two are much reduced and fused with each other.     

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.     

Why is grouper larval rearing difficult?: an approach from the development of the feeding apparatus in early stage larvae of the grouper,Epinephelus coioides

The osteological development of elements forming the oral cavity was examined in early stage larvae of the grouper,Epinephelus coioides, from hatching to 242.5 hours after hatching. By the time of initial mouth opening, at 54 hours after hatching, the fundamental elements, composed of the trabecula, some components of the lower branchial and hyoid arches, the quadrate and symplectic-hyomandibular cartilages, maxilla and Meckel's cartilage, had appeared. No further elements were observed until 165 hours after initial mouth opening, except some components in the lower branchial arch and head region. The appearance of new elements and initial ossification of existing cartilage occurred thereafter, but all elements related to feeding either had not appeared or had not started ossifying until 188.5 hours after initial mouth opening. Based on the morphology and developmental modes of these elements, the feeding mode of grouper larvae was considered to be “sucking/grasping.” However, the appearance and ossification of elements occurred slowly, with no transitional phase from sucking to grasping modes of feeding being observed during the study; such delayed development of the feeding-related bony elements was considered to be a cause of the difficulty in rearing early stage grouper larvae.     

Postembryonic development of the cephalic region in Heterobranchus longifilis

At hatching, Heterobranchus longifilis does not display any primordia of the cephalic skeleton. The latter appears 12 h post–hatching and develops in three stages up to day 16. The first stage (12 h to 2 days) involves almost exclusively the development of the chondrocranium. During the second period (days 3–8), dermal elements of the splanchnocranium appear. The final stage is marked by resorption of the cartilages, progressively replaced by ossifications (days 10–16). At their appearance the elements of the splanchnocranium are fused together, as are the first neurocranial elements. Later, the splanchnocranium splits up. By the time the yolk sac is completely resorbed, the buccal and pharyngeal jaws are present, the suspensoria and hyoid bars are partially developed, and the parasphenoid partially closes the hypophyseal fenestra. These structures delimit a buccal cavity that is probably functional, i.e. capable of participating in the intake of exogenous food. Next to continue its development is principally the splanchnocranium, completing the walls of the buccal cavity. Cartilage resorption parallels the appearance of endochondral ossifications (except for the trabecular bars). Braincase closure begins to accelerate once the buccal system is complete.     

"Keystone" approach for intracranial nasofrontal dermoid sinuses

Nasofrontal dermoid sinus tracts that extend intracranially through the foramen cecum or ethmoid can be difficult to completely resect. Complete extirpation of nasofrontal dermoid sinus cysts is essential for effective treatment of this problem to minimize the chance of recurrence. The authors describe a new technique based on parasagittal osteotomies through the supraorbital bar, or bandeau, that ensures that the resection of the nasofrontal dermoid sinus cysts is complete. This technique also limits the size of the external nasal incision and enhances the surgeon's exposure of the anterior cranial base for resection of intradural extension. This approach also enhances exposure for the direct repair of the dura and the cranial vault.     

Developmental stress and cranial hypostosis by epigenetic trait occurrence and distribution: an exploratory study on the Italian Neandertals

The occurrence and distribution of 35 cranial epigenetic traits in the Italian Neandertals (Saccopastore 1 and 2, Guattari 1) were examined according to morpho-functional cranial regions and with respect to a distinction between hypostosis (i.e., weak osseous development, arrested morphogenesis, retention of infantile features) and hyperostosis (i.e. excess of ossification, not reaching the pathological condition). The results, expressed ashypostotic scores, showed higher levels of hypostosis in these Neandertal specimens than in recent European samples. The highest expressions of hypostotis were observed in those regions of the Neandertal cranium where disequilibrium between skeletal and cerebral growth factors was expected. These results—interpreted as expression of developmental stress—are consistent with a heterochronic interpretation of the development of the Neandertal cranium; namely, a faster ossification of the cranial vault relative to brain growth rates.     

Early development of the cephalic skeleton in the turbot

At hatching Scophthalmus maximus shows no cartilaginous and no bony structure. Mecke?s cartilages appear when the fry are 1 day old, followed on day 2, by formation of the trabecular bars, fused at the outset to form a trabecula communis. Concurrently, the palatoquadrates complete the mandibular arch, and the first two pairs of ceratobranchials, associated with a pair of hyoid bars, form the beginnings of the hyobranchial system. By day 3, the parachordals have fused with the trabecular bars, the hyosymplectics have linked to the hyoid bars by interhyals, and the first four pairs of ceratobranchials have appeared. The first bony structures appear: the preoperculars. On day 8, the frontals develop above the orbits and the maxillaries and dentaries appear. On day 10, the primordia of the taeniae marginales appear, the palatoquadrates bear a pterygoid process, and to the branchial basket have been added the fifth pair of ceratobranchials and the four pairs of epibranchials. On day 12, both pairs of posterior pharyngobranchials are present. The premaxillaries develop in front of the maxillaires, and retroarticulars and the angulars complete the lower jaws. On day 13, a thin parasphenoid contributes to the floor of the neurocranium, and ectopterygoids and entopterygoids to the splanchnocranium. The set of opercular bones is complete. On day 15, the tectum synoticum closes the braincase posteriorly. The splanchnocranium possesses a basihyal and the pharyngobranchials of the first epibranchials. On day 18, the tectum posterius completes the dome of the braincase. The rear end and lateral walls of the skull are formed by the basioccipital, the exoccipitals, the pterotics, and the parietals. The suspensorium is nearly complete. From day 10, the first resorptions begin in parallel with the construction of the chondrocranium. Mecke?s cartilages each split in two, then the posterior part of the trabecular bars disappears. On day 23, the right taenia marginalis separates from the lamina orbitonasalis and curves towards the centre. Simultaneously, the right eye begins its migration to the left. This is the only metamorphosis-linked asymmetry to appear during the development of the chondrocranium. On day 25, many more bony structures appear, a characteristic of this stage: the nasals, lateral ethmoids, mesethmoid, sphenotics, prootics, pleurosphenoids, epiotics, and supraoccipital. From this stage on, the bony structures continue to develop, while the front of the neurocranium and the jaws undergo a deep remodelling due to metamorphosis. The left taenia marginalis does not appear reduced until day 29. By day 45, there remain only a few small elements of the cartilaginous skull.     

Cranial capacity/cranial base relationships and prediction of vault form: A canonical correlation analysis

Canonical correlation analysis was used to test an hypothesized morphological relationship between vault form and cranial capacity relative to length of the chondrocranium. Ninety-five adult male Czech skulls were measured for vault form expressed as length, width and height of the brain case; the chondrocranium was represented by nasion-basion and basion-opisthion lengths. In terms of explained variation, the first and most important dimension of covariation between vault and chondrocranial variables was size. The second most significant dimension of covariation expressed the hypothesized shape relationships—i.e., overall size being equal, the shorter the chondrocranial base relative to cranial capacity, the shorter and wider the vault. Furthermore, the competing hypothesis that vault form is determined by facial length proved untenable since facial length was predictive of vault shape only when measured as prosthion-basion, a measure that incorporates basal length. When corrected for basal length, facial length is unrelated to vault form. The results are consistent with the assumption that phylogenetic and microevolutionary trends toward brachycephaly in man stem from changes in the relationship between two components of skull growth, the chondrocranial base and the brain.     

Early ontogeny of aquarium-raised Moenkhausia sanctaefilomenae (Characiformes: Characidae)

The ontogeny of the characiform fish Moenkhausia sanctaefilomenae, from early embryogenesis through the early larval period, is presented. Fertilized eggs were slightly elliptical, measured 0.6 mm in diameter, and were surrounded by a fertilization envelope 0.8 mm in diameter. Much of the early embryogenesis is complete after 12 h, with cleavages complete after 2.5 h and gastrulation complete after 3 additional hours. The initial formation of organs needed for predatory behaviors occurs within 72 h. Growth of the cranial elements is quite dramatic and allows for the capture of relatively large prey at the onset of exogenous feeding. Elaboration of these elements continues into the early larval period.