On the development of the chondrocranium and the histological anatomy of the head in perinatal stages of marsupial mammals

Abstract

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 Monodelphis domestica, Dromiciops gliroides, Perameles sp. and Macropus eugenii. 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 Dromiciops, and a similar tissue has been reported for Tarsipes. Contradictory reports on the presence of the tegmen tympani can be found in the literature. We describe a small tegmen tympani in Macropus. 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.

Character definition and tempus optimum in comparative chondrocranial research

“…Our own experience shows that haematoxylin and eosin plus Alcian Blue staining might be most useful to differentiate mesenchymal condensations and chondrifications in early development (Yaryhin & Werneburg, ), whereas Azan staining after Haidenhain is particularly useful for late ontogeny, when bones have already started to form (Mulisch & Welsch, ). Another important issue is the diverse terminology of chondrocranial anatomy between major taxonomic groups, which might represent a hindrance to studies of this subject. Examples were highlighted by Sánchez‐Villagra and Forasiepi (). Moreover, for exact character definition, it is extremely important to know more than just bone anatomy.…”

“…(4) Another important issue is the diverse terminology of chondrocranial anatomy between major taxonomic groups, which might represent a hindrance to studies of this subject. Examples were highlighted by Sánchez-Villagra and Forasiepi (2017). Moreover, for exact character definition, it is extremely important to know more than just bone anatomy.…”

“…In free-living larval forms, jaw, neck, and eye musculature attaches to the unossified chondrocranium (Schmidt, Piekarski, & Olsson, 2013) and should have some morphogenetic influence on chondrocranial differentiation. In amniotes, a large part of development occurs in the egg or the maternal uterus and the cartilaginous skull is, in most cases, not under particular pressure (but see Sánchez-Villagra & Forasiepi, 2017). However, already in the embryo and in the foetus uncoordinated muscular activity is present (Cordero, Telemeco, & Gangloff, 2018).…”

Deep time perspective on turtle neck evolution: chasing the Hox code by vertebral morphology

“…Reconstruction of Hox gene expression patterns based on vertebral morphology has become possible only recently 15 , 28 . The correlation between anterior Hox gene expression and the quantifiable shape of the cervical vertebrae of living archosaurs (crocodile, alligator, and chicken) and mammals (mouse) has shown that changes in the expression of the underlying genetic code can be deduced solely from vertebral morphology 15 , 25 . Furthermore, the correlation observed in extant crocodiles and birds permitted the reconstruction of the vertebral Hox code in an extinct relative that lacks preserved DNA and is known only from fossils remains 15 .…”

Didelphis albiventris: an overview of an unprecedented transcriptome sequencing of the white-eared opossum

“…Considering the close phylogenetic relationship to eutherians and the availability of neonates in the pouch (overcoming the difficulties of access when studying in utero development), marsupials can be considered an excellent model to understand the mechanisms that govern cellular differentiation during organogenesis. For instance, different aspects of neocortex development, expansion and evolution have recently been revealed using embryos and neonates of the gray short-tailed opossum (Monodelphis domestica) and of the tammar wallaby (Macropus eugenii) as models [9,10]; while gray short-tailed opossum neonates revealed new insights in the comprehension of bronchioalveolar [11] and chondrocranial development in mammals [12]. The morphological and morphometric study of the skin of marsupial neonates suggested the participation of this organ in gaseous exchange, by the investigation of several species, such as the following: eastern quoll (Dasyurus viverrinus), grey shorttailed opossum (Monodelphis domestica), southern brown bandicoot (Isoodon obesulus), long-nosed bandicoot (Perameles nasuta), brush-tail possum (Trichosurus vulpecula), koala (Phascolarctos cinereus), long-nosed potoroo (Potorous tridactylus), brush-tailed rock wallaby (Petrogale penicillata), red-necked pademelon (Thylogale thetis) and black-striped wallaby (Macropus dorsalis) [13].…”