Cranial neural-crest migration and chondrogenic fate in the oriental fire-bellied toadBombina orientalis: Defining the ancestral pattern of head development in anuran amphibians

Olsson, Lennart; Howard, James L.

doi:10.1002/(sici)1097-4687(199607)229:1<105::aid-jmor7>3.0.co;2-2

Cited by 84 publications

(6 citation statements)

References 69 publications

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“…Development of the neural tube and the morphology of the streams of cnc cells are conserved features of frog development and resemble the basic pattern observed in B. variegata (31,35). The cnc cell streams of G. riobambae and of foam-nesting frogs, however, are larger and more clearly defined than in X. laevis, C. machalilla (19,31), and E. tricolor (data not shown).…”

Section: Discussionmentioning

confidence: 81%

A comparative analysis of frog early development

Pino

Venegas-Ferrín

Romero‐Carvajal

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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The current understanding of Xenopus laevis development provides a comparative background for the analysis of frog developmental modes. Our analysis of development in various frogs reveals that the mode of gastrulation is associated with developmental rate and is unrelated to egg size. In the gastrula of the rapidly developing embryos of the foam-nesting frogs Engystomops coloradorum and Engystomops randi, archenteron and notochord elongation overlapped with involution at the blastopore lip, as in X. laevis embryos. In embryos of dendrobatid frogs and in the frog without tadpoles Eleutherodactylus coqui, which develop somewhat more slowly than X. laevis, involution and archenteron elongation concomitantly occurred during gastrulation; whereas elongation of the notochord and, therefore, dorsal convergence and extension, occurred in the postgastrula. In contrast, in the slow developing embryos of the marsupial frog Gastrotheca riobambae, only involution occurred during gastrulation. The processes of archenteron and notochord elongation and convergence and extension were postgastrulation events. We produced an Ab against the homeodomain protein Lim1 from X. laevis as a tool for the comparative analysis of development. By the expression of Lim1, we were able to identify the dorsal side of the G. riobambae early gastrula, which otherwise was difficult to detect. Moreover, the Lim1 expression in the dorsal lip of the blastopore and notochord differed among the studied frogs, indicating variation in the timing of developmental events. The variation encountered gives evidence of the modular character of frog gastrulation.Brachyury ͉ Gastrotheca ͉ Lim1

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Section: Discussionmentioning

confidence: 81%

A comparative analysis of frog early development

Pino

Venegas-Ferrín

Romero‐Carvajal

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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“…The number of elements differs between species and the extent of fusion or ossification later in development is variable. Several elements can be correlated with the pharyngeal arch they derive from (e.g., [ 3 ]). The jaws derive from mesenchyme of the first or mandibular arch, the hyoid elements derive from the 2nd or hyoid arch, and branchial (gill bearing) or posterior pharyngeal elements derive from arches 3 to 6 (in some vertebrates more arches are present) (e.g., [ 4 ]).…”

Section: Introductionmentioning

confidence: 99%

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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“…If the mesoderm/CNC cell boundary established by the stage is persistent through subsequent development, the boundary in the neurocranium should always coincide with the adenohypophysis level. Indeed, the boundary at the cranial base has been reported to coincide with the position of the adenohypophysis in many bony vertebrates, including chickens and mice (Figure 1) (McBratney-Owen et al, 2008;McCarthy et al, 2016;Olsson & Hanken, 1996). However, it remains unclear whether the mesenchymal boundary in the cranial lateral wall should coincide with the position of the adenohypophysis in gnathostomes other than chickens.…”

Section: A Pan-amniote Configuration Of the Mesodermal Primary Crania...mentioning

confidence: 99%

“…Experimental embryology in the 20th century as well as molecular genetic technologies in the 21st century have provided fate mapping data in some animals and revealed that the vertebrate cranium is derived from two types of mesenchymes: a mesodermal mesenchyme and a neural crest mesenchyme (Hörstadius & Sellman, 1946; Jiang et al, 2002; Le Lièvre, 1978; McBratney‐Owen et al, 2008; McCarthy et al, 2016; Olsson & Hanken, 1996; Platt, 1893; Stone, 1926; reviewed by Gross & Hanken, 2008). In the jawed vertebrates, the rostral half of the neurocranium (the part anterior to the notochord; prechordal cranium) is derived from the cranial neural crest (CNC) cells, whereas the posterior half lying alongside the notochord is derived from the mesoderm (chordal cranium) (Figure 1; Couly et al, 1993).…”

Section: Introductionmentioning

confidence: 99%

“…Dorsal views of the chondrocrania are aligned on the position of the adenohypophysis (blue line). The cranium of each animal is colored according to its developmental origins (light blue for the CNC origins; pink for the mesodermal elements) based on Couly et al (1993) (chicken/ Gallus ), McCarthy et al (2016) (zebrafish/ Danio ), Olsson and Hanken (1996) (toad/ Bombia ), with the exception of the mouse chondrocranium, which was redescribed in this study (see also Figure 5 and Supporting Information: Figure ). hf, hypophyseal foramen; nt, notochord; spf, sphenoparietal fenestra; tp, trabecular plate; trb, trabecula.…”

Section: Introductionmentioning

confidence: 99%

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A detailed redescription of the mesoderm/neural crest cell boundary in the murine orbitotemporal region integrates the mammalian cranium into a pan‐amniote cranial configuration

Kuroda

Adachi

Kuratani

2022

Evolution and Development

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The morphology of the mammalian chondrocranium appears to differ significantly from those of other amniotes, since the former possesses uniquely developed brain and cranial sensory organs. In particular, a question has long remained unanswered as to the developmental and evolutionary origins of a cartilaginous nodule called the ala hypochiasmatica. In this study, we investigated the embryonic origin of skeletal elements in the murine orbitotemporal region by combining genetic cell lineage analysis with detailed morphological observation. Our results showed that the mesodermal

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Cranial neural-crest migration and chondrogenic fate in the oriental fire-bellied toadBombina orientalis: Defining the ancestral pattern of head development in anuran amphibians

Cited by 84 publications

References 69 publications

A comparative analysis of frog early development

A comparative analysis of frog early development

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

A detailed redescription of the mesoderm/neural crest cell boundary in the murine orbitotemporal region integrates the mammalian cranium into a pan‐amniote cranial configuration

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