Sequence and timing of early cranial skeletal development in <i>Xenopus laevis</i>

Lukas, Paul; Olsson, Lennart

doi:10.1002/jmor.20754

Cited by 20 publications

(65 citation statements)

References 45 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…We hypothesize that bapx1 acts as a cartilage preventing gene in unperturbed larval development and ensures that the joint region does not chondrify. Experimental overexpression of bapx1 in amphibians supports this hypothesis (Lukas & Olsson, ). In perturbed larvae, bapx1 expression might be replaced by dorsally expanded barx1 expression as reported in barx1 overexpression experiments (Nichols et al, ).…”

Section: Discussionmentioning

confidence: 67%

Bapx1 is required for jaw joint development in amphibians

Lukas

Olsson

2018

Evolution and Development

Self Cite

View full text Add to dashboard Cite

The acquisition of a movable jaw and a jaw joint are key events in gnathostome evolution. Jaws are derived from the neural crest derived pharyngeal skeleton and the transition from jawless to jawed vertebrates consists of major morphological changes, which must have a genetic foundation. Recent studies on the effects of bapx1 knockdown in fish and chicken indicate that bapx1 has acquired such a role in primary jaw joint development during vertebrate evolution, but evidence from amphibians is missing so far. In the present study, we use Ambystoma mexicanum, Bombina orientalis, and Xenopus laevis to investigate the effects of bapx1 knockdown on the development of these three different amphibians. Using morpholinos we downregulated the expression of bapx1 and obtain morphants with altered mandibular arch morphology. In the absence of bapx1 Meckeĺs cartilage and the palatoquadrate jaw joint initially develop separately but during further development the joint cavity between both fills with chondrocytes. This results in the fusion of both cartilages and the loss of the jaw joint. Despite this the jaw itself remains usable for feeding and breathing. We show that bapx1 plays a role in jaw joint maintenance during development and that the morphants morphology possibly mirrors the morphology of the jawless ancestors of the gnathostomes.

show abstract

Section: Discussionmentioning

confidence: 67%

Bapx1 is required for jaw joint development in amphibians

Lukas

Olsson

2018

Evolution and Development

Self Cite

View full text Add to dashboard Cite

show abstract

“…As described in X. laevis embryos (Lukas & Olsson, 2018a), the external morphology of tadpoles of the same stage sometimes differs greatly in the progress of skeletogenesis. Conclusions about the skeletal state cannot be drawn from the external development and vice versa.…”

Section: Resultsmentioning

confidence: 74%

“…The branchial basket of B. orientalis develops in anterior–posterior direction as described in other anuran larvae (Lukas & Olsson, 2018a; Stöhr, 1882). In X. laevis , the ceratobranchials I‐V develop consecutively and are connected first medially by the hypobranchial plate and later by the simultaneously chondrifying commissurae terminalis I–III.…”

Section: Discussionmentioning

confidence: 73%

“…Investigations on chondrocranial development are available for a growing number of vertebrate species including chondrichthyans (Gillis, Dann, & Shubin, 2009; Gillis, Modrell, & Baker, 2012), sturgeons (Gillis et al, 2012; Warth, Hilton, Naumann, Olsson, & Konstantinidis, 2017), teleosts (Langille & Hall, 1987), coelacanths (Dutel et al, 2019), anurans (Lukas & Olsson, 2018a; Parker, 1876, 1879; Stöhr, 1882), testudines (Kuratani, 1999; Tulenko & Sheil, 2007), and squamates (Hernández‐Jaimes, Jerez, & Ramírez‐Pinilla, 2012; Ollonen, da Silva, Mahlow, & Di‐Poï, 2018). Investigating the sequential development of cartilaginous elements in a variety of vertebrate species is essential for an understanding of evolutionary changes and for the identification of ontogenetic novelties as well as heterochronic events.…”

Section: Introductionmentioning

confidence: 99%

“…The morphology of the chondrocranium of anuran tadpoles has been described in several species (e.g., Candioti, 2007; Candioti, Haas, Altig, & Peixoto, 2017; Haad, Candioti, & Baldo, 2014; Kolenc et al, 2013). Unfortunately, sequential descriptions of cartilage formation from the onset of chondrification until the premetamorphic stage in anurans are scarce (Lukas & Olsson, 2018a; Reiss, 1997) or outdated (Gaupp, 1906; Parker, 1876, 1879; Stephenson, 1951; Stöhr, 1882; van der Westhuizen, 1961). Nevertheless, such investigations are important for questions regarding the origin of tetrapods and the evolution of morphological diversity of anurans.…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

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

Lukas

Olsson

2020

Journal of Morphology

Self Cite

View full text Add to dashboard Cite

The vertebrate head as a major novelty is directly linked to the evolutionary success of the vertebrates. Sequential information on the embryonic pattern of cartilaginous head development are scarce, but important for the understanding of its evolution. In this study, we use the oriental fire bellied toad, Bombina orientalis, a basal anuran to investigate the sequence and timing of larval cartilaginous development of the head skeleton from the appearance of mesenchymal Anlagen in post-neurulation stages until the premetamorphic larvae. We use different methodological approaches like classic histology, clearing and staining, and antibody staining to examine the larval skeletal morphology. Our results show that in contrast to other vertebrates, the ceratohyals are the first centers of chondrification. They are followed by the palatoquadrate and the basihyal. The latter later fuses to the ceratohyal and the branchial basket. Anterior elements like Meckel's cartilage and the rostralia are delayed in development and alter the ancestral anterior posterior pattern observed in other vertebrates. The ceratobranchials I-IV, components of the branchial basket, follow this strict anterior-posterior pattern of chondrification as reported in other amphibians.Chondrification of different skeletal elements follows a distinct pattern and the larval skeleton is nearly fully developed at Gosner Stage 28. We provide baseline data on the pattern and timing of early cartilage development in a basal anuran species, which may serve as guidance for further experimental studies in this species as well as an important basis for the understanding of the evolutionary changes in head development among amphibians and vertebrates.

show abstract

Developmental sequence of the chondrocranium in the obligate carnivorous larvae of Lepidobatrachus laevis (Amphibia: Ceratophryidae)

Hernández‐Nieto,

Ziermann‐Canabarro,

Lukas

2024

The Anatomical Record

View full text Add to dashboard Cite

The vertebrate head and its skull represent a significant innovation that has played a key role in the evolutionary and ecological success of vertebrates. For a global and integral understanding of the evolution of the head skeleton, it is essential to have reliable information on the development of chondrocranium in a wide range of vertebrate species. Therefore, we studied the cranial chondrogenesis of the larva of the Budgett frog, Lepidobatrachus laevis (Ceratophryidae, Neobatrachia). We studied the development using several methods, including histological preparation of transverse sections of the chondrocranium, morphological analysis of three different states of development (mesenchymal aggregation, differentiation, and chondrification), and three‐dimensional digital reconstructions. As a result, we observed that the Anlage of the chondrocranium at Gosner stage 19 is laterally compressed, that is, it is initially higher than wide. It gradually flattens, enlarges, and differentiates until reaching a very wide and flat shape at Gosner stage 26. Furthermore, we show that the chondrocranial development of L. laevis takes place in a mosaic pattern, which differs to nontetrapod vertebrates in which an anterior to posterior gradient of chondrification is observed. We identified 19 developmental stages in L. laevis according to the chondrification state of its cranial structures. The first element reaching the differentiation‐into‐chondroblast stage is the hypobranchial plate of the branchial basket, and chondrification, that is, final differentiation, occurs simultaneously in several structures of the neurocranium and viscerocranium. We hypothesize that the rapid chondrification of L. laevis' chondrocranium is an adaptation to the semi‐arid climate conditions from its type locality, El Gran Chaco in South America. Due to the only temporary availability of suitable water accumulations this apparent accelerated development would make sense to ensure the tadpoles are froglets by the time the water body disappears. Here, we provide novel information on chondrocranial development in L. laevis. We compare our results to the developmental sequences, previously known from other vertebrate taxa, particularly within the amphibian phylogeny, in an attempt to understand developmental variability and the evolutionary history of the vertebrate head skeleton.

show abstract

Sequence and timing of early cranial skeletal development in Xenopus laevis

Cited by 20 publications

References 45 publications

Bapx1 is required for jaw joint development in amphibians

Bapx1 is required for jaw joint development in amphibians

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

Developmental sequence of the chondrocranium in the obligate carnivorous larvae of Lepidobatrachus laevis (Amphibia: Ceratophryidae)

Contact Info

Product

Resources

About