Sequence of chondrocranial development in the oriental fire bellied toad <scp><i>Bombina orientalis</i></scp>

Lukas, Paul; Olsson, Lennart

doi:10.1002/jmor.21138

Cited by 7 publications

(23 citation statements)

References 55 publications

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“…Additionally, the mediodorsal surfaces of the otic capsules are connected via the mesenchymal Anlage of the synotic tectum, which differentiates into a chondroblast containing Anlage at stage C5. Until Gosner [ 26 ] stage 34 the synotic tectum chondrifies and the basicranial fenestra closes (Fig. 7 ).…”

Section: Resultsmentioning

confidence: 99%

“…The presence of the spicules I-III, a postcondylar process at the posterior margin of the ceratohyal and the presence of transversal tectal taenia were mentioned as defining features of the genus Discoglossus [ 28 , 29 ]. However, these structures are absent in the investigated stages of D. scovazzi (here studied up to Gosner [ 26 ] stage 29 = Go29). If the absence is an apomorphic trait of D. scovazzi or if these structures appear later during development (Haas [ 29 ] studied Go37 and Púgener [ 28 ] Go34 tadpoles) requires further investigation.…”

Section: Discussionmentioning

confidence: 99%

“…They were kept at temperatures between 18 and 25 °C to ensure that every stage of interest can be collected (3–5 tadpoles every 2 h). All specimens (embryos and larvae) were staged according to the simplified staging table for anuran embryos and larvae [ 26 ] and denominated as “Go stages.” A developmental series was established by collecting embryos and larvae from defined stages between Go 20 and Go 34 (n = 156). Anesthesia was performed using 1% tricaine methanesulfonate (MS-222) according to the animal welfare protocols at the Friedrich-Schiller-University Jena.…”

Section: Methodsmentioning

confidence: 99%

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Sequence of chondrocranial development in basal anurans—Let’s make a cranium

Lukas

Ziermann

2022

Front Zool

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Background The craniofacial skeleton is an evolutionary innovation of vertebrates. Due to its complexity and importance to protect the brain and aid in essential functions (e.g., feeding), its development requires a precisely tuned sequence of chondrification and/or ossification events. The comparison of sequential patterns of cartilage formation bears important insights into the evolution of development. Discoglossus scovazzi is a basal anuran species. The comparison of its chondrocranium (cartilaginous neuro- & viscerocranium) development with other basal anurans (Xenopus laevis, Bombina orientalis) will help establishing the ancestral pattern of chondrification sequences in anurans and will serve as basis for further studies to reconstruct ancestral conditions in amphibians, tetrapods, and vertebrates. Furthermore, evolutionary patterns in anurans can be studied in the light of adaptations once the ancestral sequence is established. Results We present a comprehensive overview on the chondrocranium development of D. scovazzi. With clearing and staining, histology and 3D reconstructions we tracked the chondrification of 44 elements from the first mesenchymal Anlagen to the premetamorphic cartilaginous head skeleton and illustrate the sequential changes of the skull. We identified several anuran and discoglossoid traits of cartilage development. In D. scovazzi the mandibular, hyoid, and first branchial arch Anlagen develop first followed by stepwise addition of the branchial arches II, III, and IV. Nonetheless, there is no strict anterior to posterior chondrification pattern within the viscerocranium of D. scovazzi. Single hyoid arch elements chondrify after elements of the branchial arch and mandibular arch elements chondrify after elements of the branchial arch I. Conclusions In Osteichthyes, neurocranial elements develop in anterior to posterior direction. In the anurans investigated so far, as well as in D. scovazzi, the posterior parts of the neurocranium extend anteriorly, while the anterior parts of the neurocranium, extend posteriorly until both parts meet and fuse. Anuran cartilaginous development differs in at least two crucial traits from other gnathostomes which further supports the urgent need for more developmental investigations among this clade to understand the evolution of cartilage development in vertebrates.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Sequence of chondrocranial development in basal anurans—Let’s make a cranium

Lukas

Ziermann

2022

Front Zool

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“…Investigations on the chondrocranial development of larval anurans are scarce, but their number is growing. The developmental sequence of three basal frog species, two discoglossoids ( Bombina orientalis , Discoglossus scovazzi ) and one pipoid ( Xenopus laevis ), was recently described and developmental patterns identified (Lukas & Olsson, 2018, 2020; Lukas & Ziermann, 2022). The development of the viscerocranial elements does not follow the anterior to posterior direction as described in other vertebrate clades.…”

Section: Introductionmentioning

confidence: 99%

Embryonic pattern of cartilaginous head development in the European toad, Bufo bufo

Lukas

2023

J Exp Zool Pt B

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The craniofacial skeleton of vertebrates is a major innovation of the whole clade. Its development and composition requires a precisely orchestrated sequence of chondrification events which lead to a fully functional skeleton. Sequential information on the precise timing and sequence of embryonic cartilaginous head development are available for a growing number of vertebrates. This enables a more and more comprehensive comparison of the evolutionary trends within and among different vertebrate clades. This comparison of sequential patterns of cartilage formation enables insights into the evolution of development of the cartilaginous head skeleton. The cartilaginous sequence of head formation of three basal anurans (Xenopus laevis, Bombina orientalis, Discoglossus scovazzi) was investigated so far. This study investigates the sequence and timing of larval cartilaginous development of the head skeleton from the appearance of mesenchymal Anlagen until the premetamorphic larvae in the neobatrachian species Bufo bufo. Clearing and staining, histology, and 3D reconstruction enabled the tracking of 75 cartilaginous structures and the illustration of the sequential changes of the skull as well as the identification of evolutionary trends of sequential cartilage formation in the anuran head. The anuran viscerocranium does not chondrify in the ancestral anterior to posterior direction and the neurocranial elements do not chondrify in posterior to anterior direction. Instead, the viscerocranial and neurocranial development is mosaic‐like and differs greatly from the gnathostome sequence. Strict ancestral anterior to posterior developmental sequences can be observed within the branchial basket. Thus, this data is the basis for further comparative developmental studies of anuran skeletal development.

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“…The reason we chose this toad to study is that (i) the morphology and skeletal development of Bombina were previously described in detail (e.g., Maglia and Púgener, 1998;Lukas and Olsson, 2020;Roček et al, 2021), (ii) B. orientalis was used in pioneering experimental studies on the TH-mediation of cranial development in anurans (Hanken and Hall, 1988b;Hanken and Summers, 1988), and (iii) B. variegata belongs to the basal anuran family.…”

Section: Introductionmentioning

confidence: 99%

Increasing Hormonal Control of Skeletal Development: An Evolutionary Trend in Amphibians

Vassilieva

Смирнов

2021

Front. Ecol. Evol.

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The biphasic life history of amphibians includes metamorphosis, a complex developmental event that involves drastic changes in the morphology, physiology and biochemistry accompanying the transition from the larval to adult stage of development. Thyroid hormones (THs) are widely known to orchestrate this remodeling and, in particular, to mediate the development of the bony skeleton, which is a model system in evolutionary morphological studies of amphibians. Detailed experimental studies of the role of THs in the craniogenesis of diverse urodelan amphibians revealed that (i) these hormones affect both the timing and sequence of bone formation, (ii) TH involvement increases in parallel with the increase in divergence between larval and adult skull morphology, and (iii) among urodelans, TH-involvement in skull development changes from a minimum in basal salamanders (Hynobiidae) to the most pronounced in derived ones (Salamandridae and Plethodontidae). Given the increasing regulatory function of THs in urodelan evolution, we hypothesized a stronger involvement of THs in the control of skeletogenesis in anurans with their most complex and dramatic metamorphosis among all amphibians. Our experimental study of skeletal development in the hypo- and hyperthyroid yellow-bellied toad (Bombina variegata: Bombinatoridae) supports the greater involvement of THs in the mediation of all stages of anuran cranial and postcranial bones formation. Similar to urodelans, B. variegata displays enhancing TH involvement in the development of cranial bones that arise during larval ontogeny: while the hormonal impact on early larval ossifications is minimal, the skull bones forming during metamorphosis are strictly TH-inducible. However, in contrast to urodelans, all cranial bones, including the earliest to form, are TH-dependent in B. variegata; moreover, the development of all elements of the axial and limb skeleton is affected by THs. The more accentuated hormonal control of skeletogenesis in B. variegata demonstrates the advanced regulatory and inductive function of THs in the orchestration of anuran metamorphosis. Based on these findings, we discuss (i) changes in THs function in amphibian evolution and (ii) the role of THs in the evolution of life histories in amphibians.

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Sequence of chondrocranial development in the oriental fire bellied toad Bombina orientalis

Cited by 7 publications

References 55 publications

Sequence of chondrocranial development in basal anurans—Let’s make a cranium

Sequence of chondrocranial development in basal anurans—Let’s make a cranium

Embryonic pattern of cartilaginous head development in the European toad, Bufo bufo

Increasing Hormonal Control of Skeletal Development: An Evolutionary Trend in Amphibians

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