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Frontiers in Zoology Apr 2021Birds exhibit an enormous diversity in adult skull shape (disparity), while their embryonic chondrocrania are considered to be conserved across species. However, there... (Review)
Review
BACKGROUND
Birds exhibit an enormous diversity in adult skull shape (disparity), while their embryonic chondrocrania are considered to be conserved across species. However, there may be chondrocranial features that are diagnostic for bird clades or for Aves as a whole. We synthesized and analyzed information on the sequence of chondrification of 23 elements in ten bird species and five outgroups. Moreover, we critically considered the developmental morphology of the chondrocrania of 21 bird species and examined whether the diversity in adult skull shape is reflected in the development of the embryonic skull, and whether there are group-specific developmental patterns.
RESULTS
We found that chondrocranial morphology is largely uniform in its major features, with some variation in the presence or absence of fenestrae and other parts. In kiwis (Apteryx), the unique morphology of the bony skull in the orbito-nasal region is reflected in its chondrocranial anatomy. Finally, differences in morphology and chondrification sequence may distinguish between different Palaeognathae and Neognathae and between the Galloanserae and Neoaves. The sequence of chondrification is largely conserved in birds, but with some variation in most regions. The peri- and prechordal areas in the base of the chondrocranium are largely conserved. In contrast to the outgroups, chondrification in birds starts in the acrochordal cartilage and the basicranial fenestra is formed secondarily. Further differences concern the orbital region, including early chondrification of the pila antotica and the late formation of the planum supraseptale.
CONCLUSION
Synthesizing information on chondrocranial development confronts terminological issues and a lack of comparable methods used (e.g., different staining; whole-mounts versus histology). These issues were taken into consideration when assessing differences across species. The summary of works on avian chondrocranial development, covered more than a century, and a comparison of the chondrification sequence among birds could be conducted. Future studies could test the hypothesis that chondrocranial disparity in Aves, in terms of the shape and proportion of individual elements, could be as large as adult skull disparity, despite conserved developmental patterns and the richness of forms in other (dermal) portions of the skull.
PubMed: 33926502
DOI: 10.1186/s12983-021-00406-z -
ELife Jun 2022The cranial endo and dermal skeletons, which comprise the vertebrate skull, evolved independently over 470 million years ago and form separately during embryogenesis. In...
The cranial endo and dermal skeletons, which comprise the vertebrate skull, evolved independently over 470 million years ago and form separately during embryogenesis. In mammals, much of the cartilaginous chondrocranium is transient, undergoing endochondral ossification or disappearing, so its role in skull morphogenesis is not well studied and it remains an enigmatic structure. We provide complete 3D reconstructions of the laboratory mouse chondrocranium from embryonic day (E) 13.5 through E17.5 using a novel methodology of uncertainty-guided segmentation of phosphotungstic enhanced 3D micro-computed tomography images with sparse annotation. We evaluate the embryonic mouse chondrocranium and dermatocranium in 3D, and delineate the effects of a variant on embryonic chondrocranial cartilages and on their association with forming dermal bones using the Crouzon syndrome mouse. We show that the dermatocranium develops outside of and in shapes that conform to the chondrocranium. Results reveal direct effects of the variant on embryonic cartilage, on chondrocranium morphology, and on the association between chondrocranium and dermatocranium development. Histologically, we observe a trend of relatively more chondrocytes, larger chondrocytes, and/or more matrix in the embryos at all timepoints before the chondrocranium begins to disintegrate at E16.5. The chondrocrania and forming dermatocrania of embryos are relatively large, but a contrasting trend begins at E16.5 and continues into early postnatal (P0 and P2) timepoints, with the skulls of older mice reduced in most dimensions compared to littermates. Our findings have implications for the study and treatment of human craniofacial disease, for understanding the impact of chondrocranial morphology on skull growth, and potentially on the evolution of skull morphology.
Topics: Animals; Cartilage; Craniofacial Dysostosis; Disease Models, Animal; Mammals; Mice; Receptor, Fibroblast Growth Factor, Type 2; Skull; X-Ray Microtomography
PubMed: 35704354
DOI: 10.7554/eLife.76653 -
Seminars in Cell & Developmental Biology Jul 2019The skull is a vertebrate novelty. Morphological adaptations of the skull are associated with major evolutionary transitions, including the shift to a predatory... (Review)
Review
The skull is a vertebrate novelty. Morphological adaptations of the skull are associated with major evolutionary transitions, including the shift to a predatory lifestyle and the ability to masticate while breathing. These adaptations include the chondrocranium, dermatocranium, articulated jaws, primary and secondary palates, internal choanae, the middle ear, and temporomandibular joint. The incredible adaptive diversity of the vertebrate skull indicates an underlying bauplan that promotes evolvability. Comparative studies in craniofacial development suggest that the craniofacial bauplan includes three secondary organizers, two that are bilaterally placed at the Hinge of the developing jaw, and one situated in the midline of the developing face (the FEZ). These organizers regulate tissue interactions between the cranial neural crest, the neuroepithelium, and facial and pharyngeal epithelia that regulate the development and evolvability of the craniofacial skeleton.
Topics: Animals; Biological Evolution; Body Patterning; Facial Bones; Fishes; Gene Expression Regulation, Developmental; Neural Crest; Skull
PubMed: 29248471
DOI: 10.1016/j.semcdb.2017.12.004 -
Zoological Letters 2017An overview of the literature on the chondrocranium of marsupial mammals reveals a relative conservatism in shape and structures. We document the histological cranial... (Review)
Review
An overview of the literature on the chondrocranium of marsupial mammals reveals a relative conservatism in shape and structures. We document the histological cranial anatomy of individuals representing , , sp. and . The marsupial chondrocranium is generally characterized by the great breadth of the lamina basalis, absence of pila metoptica and large otic capsules. Its most anterior portion (cupula nasi anterior) is robust, and anterior to it there are well-developed tactile sensory structures, functionally important in the neonate. Investigations of ossification centers at and around the nasal septum are needed to trace the presence of certain bones (e.g., mesethmoid, parasphenoid) across marsupial taxa. In many adult marsupials, the tympanic floor is formed by at least three bones: alisphenoid (alisphenoid tympanic process), ectotympanic and petrosal (rostral and caudal tympanic processes); the squamosal also contributes in some diprotodontians. The presence of an entotympanic in marsupials has not been convincingly demonstrated. The tubal element surrounding the auditory tube in most marsupials is fibrous connective tissue rather than cartilage; the latter is the case in most placentals recorded to date. However, we detected fibrocartilage in a late juvenile of , and a similar tissue has been reported for . Contradictory reports on the presence of the tegmen tympani can be found in the literature. We describe a small tegmen tympani in . Several heterochronic shifts in the timing of development of the chondocranium and associated structures (e.g., nerves, muscles) and in the ossification sequence have been interpreted as largely being influenced by functional requirements related to the altriciality of the newborn marsupial during early postnatal life. Comparative studies of chondocranial development of mammals can benefit from a solid phylogenetic framework, research on non-classical model organisms, and integration with imaging and sectional data derived from computer-tomography.
PubMed: 28203388
DOI: 10.1186/s40851-017-0062-y -
Zoological Letters 2018The study of chondrocrania has a long tradition with a focus on single specimens and stages. It revealed great interspecific diversity and a notion of intraspecific...
BACKGROUND
The study of chondrocrania has a long tradition with a focus on single specimens and stages. It revealed great interspecific diversity and a notion of intraspecific variation. As an embryonic structure, the chondrocranium is subject to major changes in ontogeny with resorption and ossification of different cartilaginous structures. The cupula nasi anterior is the anteriormost portion of the cartilaginous nasal capsule and is expected to mirror much of the animal's life history and lifestyle. Its diversity in mammals is reflected in the external nasal anatomy of newborns. Marsupials and placentals show marked differences, likely related to breathing and suckling behavior.
RESULTS
We examined histological sections of five marsupial and three placentals species and traced the development of the cupula nasi anterior and the anterior nasal capsule. We found ontogenetic variation for nearly 50% of the 43 characters defined herein. By comparing to the literature and considering ontogenetic variation, we performed an analysis of character evolution in 70 mammalian species and reconstructed the nasal anatomy of the therian ancestor.
CONCLUSIONS
At birth, marsupials have a complete but simple cupula nasi anterior, whereas placentals display a more diverse morphology due to reductions and variations of chondrocranial elements. The more compact nasal capsule in marsupials is related to a long and strong fixation to the mother's teat after birth. Within marsupials and placentals, several derived characters distinguish major taxa, probably related to developmental and functional constraints. The reconstructed ancestral anatomy of the cupula nasi anterior supports the hypothesis that the therian ancestor was placental-like and that the marsupial lifestyle is more derived.
PubMed: 30505462
DOI: 10.1186/s40851-018-0112-0 -
Journal of Developmental Biology Jan 2021The cranial base is a multifunctional bony platform within the core of the cranium, spanning rostral to caudal ends. This structure provides support for the brain and... (Review)
Review
The cranial base is a multifunctional bony platform within the core of the cranium, spanning rostral to caudal ends. This structure provides support for the brain and skull vault above, serves as a link between the head and the vertebral column below, and seamlessly integrates with the facial skeleton at its rostral end. Unique from the majority of the cranial skeleton, the cranial base develops from a cartilage intermediate-the chondrocranium-through the process of endochondral ossification. Owing to the intimate association of the cranial base with nearly all aspects of the head, congenital birth defects impacting these structures often coincide with anomalies of the cranial base. Despite this critical importance, studies investigating the genetic control of cranial base development and associated disorders lags in comparison to other craniofacial structures. Here, we highlight and review developmental and genetic aspects of the cranial base, including its transition from cartilage to bone, dual embryological origins, and vignettes of transcription factors controlling its formation.
PubMed: 33498686
DOI: 10.3390/jdb9010003 -
Vertebrate Zoology Apr 2020In most modern bony vertebrates, a considerable portion of the chondrocranium remains cartilaginous only during a relatively small window of embryonic development,...
In most modern bony vertebrates, a considerable portion of the chondrocranium remains cartilaginous only during a relatively small window of embryonic development, making it difficult to study this complex structure. Yet, the transient nature of some chondrocranial elements is precisely why it is so intriguing. Since the chondrocranium has never been lost in any vertebrate, its function is critical to craniofacial development, disease, and evolution. Experimental evidence for the various roles of the chondrocranium is limited, and though snapshots of chondrocranial development in various species at isolated time points are valuable and informative, these cannot provide the data needed to determine the functions of the chondrocranium, or its relationship to the dermatocranium in evolution, in development, or in disease. Observations of the spatiotemporal associations of chondrocranial cartilage, cartilage bone, and dermal bone over early developmental time are available for many vertebrate species and these observations represent the data from which we can build hypotheses. The testing of those hypotheses requires precise control of specific variables like developmental time and molecular signaling that can only be accomplished in a laboratory setting. Here, we employ recent advances in contrast-enhanced micro computed tomography to provide novel 3D reconstructions of the embryonic chondrocranium in relation to forming dermal and cartilage bones in laboratory mice across three embryonic days (E13.5, E14.5, and E15.5). Our observations provide support for the established hypothesis that the vertebrate dermal (exo-) skeleton and endoskeleton evolved as distinct structures and remain distinct. Additionally, we identify spatiotemporal patterning in the development of the lateral wall, roof, and braincase floor of the chondrocranium and the initial mineralization and growth of the bones associated with these cartilages that provides support for the hypothesis that the chondrocranium serves as a scaffold for developing dermatocranial bones. The experimental protocols described and data presented provide tools for further experimental work on chondrocranial development.
PubMed: 33163116
DOI: No ID Found -
Seminars in Cell & Developmental Biology Jul 2019Chrondrocranium, the cartilaginous skull, is one of the major innovations that underlie evolution of the vertebrate head. Control of the induction and shaping of the... (Review)
Review
Chrondrocranium, the cartilaginous skull, is one of the major innovations that underlie evolution of the vertebrate head. Control of the induction and shaping of the cartilage is a key for the formation of the facial bones and largely defines facial shape. The appearance of cartilage in the head enabled many new functions such as protection of central nervous system and sensory structures, support of the feeding apparatus and formation of muscle attachment points ensuring faster and coordinated jaw movements. Here we review the evolution of cartilage in the cranial region and discuss shaping of the chondrocranium in different groups of vertebrates.
Topics: Animals; Biological Evolution; Cartilage; Facial Bones; Humans; Lancelets; Models, Biological; Skull; Vertebrates
PubMed: 29248472
DOI: 10.1016/j.semcdb.2017.12.007 -
Journal of Anatomy Jun 2019Little is known about the embryonic development and variation of the chondrocranium in Crocodylia and there are no works on any Caiman species. Due to the importance of...
Little is known about the embryonic development and variation of the chondrocranium in Crocodylia and there are no works on any Caiman species. Due to the importance of cranial features in the systematics of this clade, investigating the development of the skull in embryonic stages is essential. In this study, we present for the first time the development of the cartilaginous skull of two extant Caiman species. Anatomical descriptions of the embryonic chondrocranium of Caiman latirostris and Caiman yacare were made, paying special attention to their inter- and intraspecific variation. For this purpose, pre-hatching ontogenetic cranial series of these two caiman species were prepared with a double staining and diaphanization technique. The main differences with other crocodylian species were observed in the palatoquadrate, and interspecific variation within the genus was recorded in the hyobranchial apparatus and larynx. Some characters may be distinctive of Caiman (posterior and ventral surface of the otic process of the palatoquadrate articulated with the dorsal process of the columella auris, and otic process articulated with the lateral wall of the auditory capsule), Alligatoridae (presence of an epiphanial foramen) or C. latirostris and C. yacare (Corpus hyoidei with different number and position of foramina and different shapes of its anterior contour and anterior and posterior notch, different degrees of broadening of the distal end of the Cornu branchiale I, and presence/absence of a notch in the posteroventral surface of the cricoid). Homologies of the elements belonging to the hyobranchial apparatus could not be confirmed. As in other tetrapods the trachea consists of incomplete cartilaginous rings. Morphological changes and dissimilarities found in this study are useful as a context to start studying phylogenetic constraints. Moreover, in a heterochronic context, variations may be involved.
Topics: Alligators and Crocodiles; Animals; Osteogenesis; Skull
PubMed: 30861120
DOI: 10.1111/joa.12968 -
Frontiers in Cell and Developmental... 2020The head represents the most complex part of the body and a distinctive feature of the vertebrate body plan. This intricate structure is assembled during embryonic... (Review)
Review
The head represents the most complex part of the body and a distinctive feature of the vertebrate body plan. This intricate structure is assembled during embryonic development in the four-dimensional process of morphogenesis. The head integrates components of the central and peripheral nervous system, sensory organs, muscles, joints, glands, and other specialized tissues in the framework of a complexly shaped skull. The anterior part of the head is referred to as the face, and a broad spectrum of facial shapes across vertebrate species enables different feeding strategies, communication styles, and diverse specialized functions. The face formation starts early during embryonic development and is an enormously complex, multi-step process regulated on a genomic, molecular, and cellular level. In this review, we will discuss recent discoveries that revealed new aspects of facial morphogenesis from the time of the neural crest cell emergence till the formation of the chondrocranium, the primary design of the individual facial shape. We will focus on molecular mechanisms of cell fate specification, the role of individual and collective cell migration, the importance of dynamic and continuous cellular interactions, responses of cells and tissues to generated physical forces, and their morphogenetic outcomes. In the end, we will examine the spatiotemporal activity of signaling centers tightly regulating the release of signals inducing the formation of craniofacial skeletal elements. The existence of these centers and their regulation by enhancers represent one of the core morphogenetic mechanisms and might lay the foundations for intra- and inter-species facial variability.
PubMed: 33392208
DOI: 10.3389/fcell.2020.620735