Development of the chicken skull: A complement to the external staging table of Hamburger and Hamilton

Embryonic staging tables provide a standard of developmental stages that can be used by individual investigators and provide approximate time points for the study of developmental phenomena. Surprisingly, despite the presence of a plethora of studies on the chicken skull and its role as a model species in developmental research, a staging table of the development of the chicken skull remains lacking. A detailed photographic staging table of the osseous portion of the chicken skull is thus presented here based on cleared and stained HH stages spanning HH 35 (first appearance of skull ossification) to the final stage before hatching (HH 45). This table documents the development of most of the cranial elements in the skull from the start of ossification until the element takes its final shape. The table shows that the elements of the lower jaw and ventral side of the skull begin ossifying before the skull roof and that most elements take roughly 5 days to reach their final shape, whereas others take up to 9 days (e.g., the frontal). The obtained results lead to several hypotheses about chicken skull development and provide a timeframe for future studies on chicken skull development.     

Skull development in the Iberian newt,Pleurodeles waltl (Salamandridae: Caudata: Amphibia): timing,sequence, variations,and thyroid hormone mediation of bone appearance

The cranial ossification sequence in Pleurodeles waltl is widely used in phylogenetic analyses of amphibian origin and evolution. However, the patterns published to date are far from completely resolved and contain certain discrepancies. Based on a large sample of P. waltl specimens ranging from early post-hatching larvae to post-metamorphic newts, we determined the most common cranial ossification sequence and revealed its intraspecific variations. Since thyroid hormones (THs) are involved in the mediation of skull development in salamanders, we studied the role of THs in the cranial development of P. waltl. The normal sequence and timing of bone appearance were compared with those in larvae reared under conditions of high (in 1 and 2 ng mL^-1 triiodothyronine) and low [in 0.02% thiourea (TU), which inhibits thyroid gland activity] TH levels. Metamorphosis was greatly accelerated in the TH-treated larvae and was arrested in the TU-treated larvae, which retained the larval pattern of the palate and rudimentary external gills even after 2 years of the experiment. Early-appearing bones (the coronoid, vomer, palatine, dentary, squamosal, premaxilla, parasphenoid, pterygoid, prearticular, vomer, frontal, parietal, exoccipital, in this order) arise at the same stages and ages, and follow the same ossification sequence under different TH levels. The timing of the appearance of bones normally arising in the late larval and metamorphic periods (the quadratojugal, orbitosphenoid, prootic, maxilla, nasal, os thyroideum, prefrontal, quadrate, in this order) changes depending on the TH level. The maxilla and nasal display the most pronounced reaction to changes in the TH level: they appear precociously in TH-treated animals, while their appearance is postponed and they remain rudimentary in TU-treated animals. Because of different responses to THs, the order in which late-arising bones appear changes depending on the TH level. Although bones appearing early in larval ontogeny (e.g. the premaxilla, vomer, squamosal, palatine) display no TH-induced reaction when they start to develop, their further differentiation shows dependence on THs, and these bones become TH-inducible closer to metamorphosis. These findings indicate that TH involvement in the mediation of cranial development changes from minimal (if at all) in its early stages to maximal during metamorphosis. It is likely that the appearance of bones early in development is mediated by factors other than THs. Their further development is accompanied by changes in the mechanisms mediating their morphological differentiation. That is, likely non-hormonal mediation becomes replaced or/and complemented by hormonal mediation. The constituent parts of the same bone may exhibit differences in their reactions to changes in TH levels. Although in normal development, the overall cranial ossification sequence is constant, there was variation in the order in which late-appearing bones was recorded. These observations suggest that this variation results from individual variability in the internal TH level. Comparison with other salamanders suggests that (a) the pattern of TH mediation described in P. waltl is common for cranial development of metamorphosing urodeles and (b) the same bone may differ in its TH dependence in different salamanders, e.g. there are interspecific variations in the degree of TH dependence of individual cranial bones.     

Limb reduction in squamate reptiles correlates with the reduction of the chondrocranium: A case study on serpentiform anguids

Background

In vertebrates, the skull evolves from a complex network of dermal bones and cartilage—the latter forming the pharyngeal apparatus and the chondrocranium. Squamates are particularly important in this regard as they maintain at least part of the chondrocranium throughout their whole ontogeny until adulthood. Anguid lizards represent a unique group of squamates, which contains limbed and limbless forms and show conspicuous variation of the adult skull.

Results

Based on several emboadryonic stages of the limbless lizards Pseudopus apodus and Anguis fragilis, and by comparing with other squamates, we identified and interpreted major differences in chondrocranial anatomy. Among others, the most important differences are in the orbitotemporal region. P. apodus shows a strikingly similar development of this region to other squamates. Unexpectedly, however, A. fragilis differs considerably in the composition of the orbitotemporal region. In addition, A. fragilis retains a paedomorphic state of the nasal region.

Conclusions

Taxonomic comparisons indicate that even closely related species with reduced limbs show significant differences in chondrocranial anatomy. The Pearson correlation coefficient suggests strong correlation between chondrocranial reduction and limb reduction. We pose the hypothesis that limb reduction could be associated with the reduction in chondrocrania by means of genetic mechanisms.

     

Delayed membranous ossification of the cranium associated with familial translocation (2;3)(p15;q12)

The relationship of delayed membranous cranial ossification to cranium bifidum and parietal foramina syndromes is unclear. We report on a family with delayed cranial membranous ossification (OMIM 155980) that segregates with an apparently balanced reciprocal translocation between chromosomes 2 and 3. The propositus had apparently low-set ears, proptosis, and a soft skull at birth. A radiographic survey of the skeleton showed markedly decreased ossification of the cranial bones and no other skeletal abnormalities. The mother and maternal grandmother of the propositus have brachycephaly, hypertelorism, and a history of a soft skull at birth. Chromosome analysis of peripheral blood from the propositus showed 46,XY,t(2;3)(p15;q12). The propositus, mother, and grandmother carry the same reciprocal translocation, whereas the mother's two phenotypically normal sibs have a normal karyotype. We used an STS-linked BAC resource to define the translocation breakpoint by identifying flanking BAC clones from both chromosomes 2, 1006D24 (D2S2279) and 1060A5 (D2S2231), and chromosome 3, 3D17 (WI8558) and 3D18 [CITB Human BAC Library, J.R.K.]. This represents the second report of a family with delayed membranous ossification of the cranium and the first report of the phenotype segregating with a chromosome rearrangement.     

Ontogeny of the Early Triassic Cynodont Thrinaxodon liorhinus (Therapsida): Cranial Morphology

The cranial morphology of 68 Thrinaxodon liorhinus specimens, ranging in size from 30 to 96 mm in basal skull length, is investigated using both qualitative and quantitative analyses. From this comprehensive survey, we determined that nine cranial features, including five in the temporal region, separated the sample into four ontogenetic stages. A bivariate analysis of 60 specimens indicated that the skull generally increased in size isometrically, with the exception of four regions. The orbit had negative allometry, a result consistent with other ontogenetic studies of tetrapods, whereas the length of the snout, palate, and temporal region showed positive allometry. The last trend had strong positive allometry indicating that during ontogeny the length of the sagittal crest increased at a much faster rate than the rest of the skull. The large number of changes in the temporal region of the skull of Thrinaxodon may indicate a greater development of the posterior fibres of the temporalis musculature from an early ontogenetic stage. For example, the posterior sagittal crest developed much earlier in ontogeny than the anterior crest that formed in adults, and bone was deposited dorsally creating a unified posterior sagittal crest rather than having a suture that spanned the entire depth of the skull roof. In combination with the isometric height of the zygomatic arch and the almost complete absence of the zygomatic arch angulation, these ontogenetic changes suggest that there was greater development of the temporalis relative to the masseter muscles, indicating a strong posterodorsal movement of the mandible in Thrinaxodon. Anat Rec, 298:1440–1464, 2015. © 2015 Wiley Periodicals, Inc.     

Assessing age-related ossification of the petro-occipital fissure: laying the foundation for understanding the clinicopathologies of the cranial base

The petro-occipital fissure (POF) lies within a critical interface of cranial growth and development in the posterior cranial fossa. The relationships between skeletal and soft tissues make this region especially important for examining biomechanical and basic biologic forces that may mold the cranial base and contribute to significant clinicopathologies associated with the structures located near the POF. Therefore, this study investigates the POF in adults in both preserved human cadavers and dried crania in order to determine if developmental changes can be observed and, if so, their value in age assessment as a model system for describing normal morphogenesis of the POF. This study demonstrates that tissue within the POF undergoes characteristic changes in ossification with age, the onset of which is considerably later than that of other synchondroses of the cranial base. Statistically, there is a moderate to strong correlation between age and stage of ossification within the POF. Further, male crania were observed to reach greater degrees of ossification at a younger age than female crania and that individual asymmetry in ossification of the tissue within the POF was not uncommon. An understanding of the basic temporal biological processes of the POF may yield insight into the development of clinicopathologies in this region of the cranial base.     

Potential For Intracranial Movements in Pterosaurs

Based on comparative anatomical, morphological, and phylogenetic considerations the potential of pterosaurs for cranial kinesis is assessed. Our investigation shows that whereas skeletally mature derived pterodactyloids have completely fused, rigid and doubtlessly akinetic skulls, skeletally immature derived pterodactyloids and more basal pterosaurs possess key features in the morphology of their otic and basal joints that are suggestive of cranial kinesis, namely streptostyly. In addition, pterosaurs exhibit an evolutionarily informative trend in the degree of cranial ossification, where it is low in most nonpterodactyloids (here named bifenestratans), intermediate in Rhamphorhynchus and Archaeopterodactyloidea, and high in derived pterodactyloids. Incomplete fusion could also indicate loose connections between skull elements. However, another crucial anatomical requirement of a kinetic skull, the permissive kinematic linkage is absent in all pterosaurian taxa. The fact, that the presence of permissive kinematic linkages in the skull is also a prerequisite of all types of cranial kinesis, provides hard evidence that all members of Pterosauria had akinetic skulls. Thus, the presence of the morphological attributes indicative of intracranial movements in some pterosaurs must be explained on grounds other than real potential for cranial kinesis. It could either be of mechanical or ontogenetic importance, or both. Alternatively, it might be considered as the morphological remnant of a real, kinetic skull possessed by the diapsid ancestors of pterosaurs. Anat Rec, , 2011. © 2011 Wiley‐Liss, Inc.     

Craniofacial growth in fetal Tarsius bancanus: brains, eyes and nasal septa

The tarsier skull has been of particular interest in studies of primate taxonomy and functional morphology for several decades. Despite this, there remains no comprehensive data on how the tarsier skull develops, especially in relation to the soft-tissues of the head. Here we have documented for the first time fetal development of the skull and brain as well as the nasal septum and eyes in T. bancanus. We have also tested for the possible influence of these tissues in shaping skull architecture. Nineteen post-mortem specimens were imaged using high-resolution magnetic resonance imaging and magnetic resonance microscopy. Landmarks and volume data were collected and analysed. Findings demonstrated massive increases of brain size and eye size as well as flattening of the midline cranial base, facial projection and orbital margin frontation. Little evidence was found to support the notion that growth of the brain or nasal septum physically drives the observed changes of the skull. However, increases in the size of the eyes relative to skull size were associated with orbital margin frontation. With the possible exception of the results for eye size, the findings indicate that rather than forcing change the soft-tissues form a framework that physically constrains the morphogenetic template of the skeletal elements. This suggests, for example, that the degree of cranial base angulation seen in adulthood is not directly determined by brain expansion bending the basicranium, but by brain enlargement limiting the extent of cranial base flattening (retroflexion) in the fetus.     

Occipital Ossification of Balaenopteroid Mysticetes

The bones of the posterior portion of the mammalian skull often exhibit incomplete ossification of the joints between the bones at the time of birth, with complete ossification at some point after birth. The sequence of ossification of these joints in mysticetes can be used to characterize the relative age in the calf and early juvenile ontogenetic stages. This study examined occipital joints ossification of 38 dry prepared neonate specimens in four mysticete species from two families (Eschrichtiidae: Eschrichtius robustus; Balaenopteridae: Balaenoptera acutorostrata, Balaenoptera physalus, and Megaptera novaeangliae). Each of the joints responsible for the fusion of the occiput were examined and rated for degree of ossification. The cranial ossification analysis indicates that E. robustus calves have open occipital joints until ～6 months of age and are born at a less mature stage than closely related balaenopterids. All of the species followed the same sequence of ossification: basioccipital/exoccipital joint, followed by the basioccipital/basisphenoid joint, and completed by the supraoccipital/exoccipital joint. Anat Rec, 2011. © 2011 Wiley‐Liss, Inc.     

The Muenke syndrome mutation (FgfR3P244R) causes cranial base shortening associated with growth plate dysfunction and premature perichondrial ossification in murine basicranial synchondroses

Muenke syndrome caused by the FGFR3(P250R) mutation is an autosomal dominant disorder mostly identified with coronal suture synostosis, but it also presents with other craniofacial phenotypes that include mild to moderate midface hypoplasia. The Muenke syndrome mutation is thought to dysregulate intramembranous ossification at the cranial suture without disturbing endochondral bone formation in the skull. We show in this study that knock-in mice harboring the mutation responsible for the Muenke syndrome (FgfR3(P244R)) display postnatal shortening of the cranial base along with synchondrosis growth plate dysfunction characterized by loss of resting, proliferating and hypertrophic chondrocyte zones and decreased Ihh expression. Furthermore, premature conversion of resting chondrocytes along the perichondrium into prehypertrophic chondrocytes leads to perichondrial bony bridge formation, effectively terminating the postnatal growth of the cranial base. Thus, we conclude that the Muenke syndrome mutation disturbs endochondral and perichondrial ossification in the cranial base, explaining the midface hypoplasia in patients.