The presence of an embryonic opercular flap in amniotes

Richardson, Jo; Shono, Toshiyuki; Okabe, Masataka; Graham, Anthony

doi:10.1098/rspb.2011.0740

Cited by 22 publications

(37 citation statements)

References 19 publications

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“…Expression analysis on paraffin sections reveals that Shh transcripts localise to the posterior pharyngeal arch epithelium (Fig. 2C,D), consistent with previous reports of Shh expression in the posterior hyoid arches of chick (Wall and Hogan, 1995) and zebrafish (Richardson et al, 2012) embryos. Analysis of Ptc2 expression at stage 22 indicates that the pharyngeal arch Shh signal is transduced posteriorly within the developing gill arches, in pharyngeal arch epithelium, mesenchyme and in the mesodermally derived core (Fig.…”

Section: Results and Discussion Shh Signalling In Skate Gill Arch Devsupporting

confidence: 76%

A shared role for sonic hedgehog signalling in patterning chondrichthyan gill arch appendages and tetrapod limbs

Gillis

Hall

2016

Development

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Chondrichthyans (sharks, skates, rays and holocephalans) possess paired appendages that project laterally from their gill arches, known as branchial rays. This led Carl Gegenbaur to propose that paired fins (and hence tetrapod limbs) originally evolved via transformation of gill arches. Tetrapod limbs are patterned by a sonic hedgehog (Shh)-expressing signalling centre known as the zone of polarising activity, which establishes the anteroposterior axis of the limb bud and maintains proliferative expansion of limb endoskeletal progenitors. Here, we use loss-of-function, label-retention and fate-mapping approaches in the little skate to demonstrate that Shh secretion from a signalling centre in the developing gill arches establishes gill arch anteroposterior polarity and maintains the proliferative expansion of branchial ray endoskeletal progenitor cells. These findings highlight striking parallels in the axial patterning mechanisms employed by chondrichthyan branchial rays and paired fins/limbs, and provide mechanistic insight into the anatomical foundation of Gegenbaur's gill arch hypothesis.

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Section: Results and Discussion Shh Signalling In Skate Gill Arch Devsupporting

confidence: 76%

A shared role for sonic hedgehog signalling in patterning chondrichthyan gill arch appendages and tetrapod limbs

Gillis

Hall

2016

Development

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“…In fish, this transcription factor is expressed in the pharyngeal pouches and their derivatives, the gill buds, and is required for their development. In chicks, gcm2 is also expressed in the pharyngeal pouches, which subsequently give rise to the parathyroids (modified from [3]). ( B ) Schematic of a transverse section through a human embryo, showing the second arch growing caudally over the posterior pouches (arrows).…”

Section: Reviewmentioning

confidence: 99%

“…Although, dermal ossifications - such as the opercle, found in actinopterygians, do not form in the second arch in amniotes, in both groups the development of the second arch is characterized by its disproportionate posterior expansion, whereby it comes to overlie the posterior arches, which form internal gills in fish or the parathyroids in amniotes (Figure 2) [3]. Furthermore, the second arches of both chick and zebrafish embryos express the same set of genes [3]. In particular, the caudal edge expresses Shh , which is a proliferative driver in many epithelia, and Shh signalling is required for posterior expansion of the second arch in both species [3].…”

Section: Reviewmentioning

confidence: 99%

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Developmental and evolutionary origins of the pharyngeal apparatus

Graham

Richardson

2012

EvoDevo

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The vertebrate pharyngeal apparatus, serving the dual functions of feeding and respiration, has its embryonic origin in a series of bulges found on the lateral surface of the head, the pharyngeal arches. Developmental studies have been able to discern how these structures are constructed and this has opened the way for an analysis of how the pharyngeal apparatus was assembled and modified during evolution. For many years, the role of the neural crest in organizing pharyngeal development was emphasized and, as this was believed to be a uniquely vertebrate cell type, it was suggested that the development of the pharyngeal apparatus of vertebrates was distinct from that of other chordates. However, it has now been established that a key event in vertebrate pharyngeal development is the outpocketing of the endoderm to form the pharyngeal pouches. Significantly, outpocketing of the pharyngeal endoderm is a basal deuterostome character and the regulatory network that mediates this process is conserved. Thus, the framework around which the vertebrate pharyngeal apparatus is built is ancient. The pharyngeal arches of vertebrates are, however, more complex and this can be ascribed to these structures being populated by neural crest cells, which form the skeletal support of the pharynx, and mesoderm, which will give rise to the musculature and the arch arteries. Within the vertebrates, as development progresses beyond the phylotypic stage, the pharyngeal apparatus has also been extensively remodelled and this has seemingly involved radical alterations to the developmental programme. Recent studies, however, have shown that these alterations were not as dramatic as previously believed. Thus, while the evolution of amniotes was believed to have involved the loss of gills and their covering, the operculum, it is now apparent that neither of these structures was completely lost. Rather, the gills were transformed into the parathyroid glands and the operculum still exists as an embryonic entity and is still required for the internalization of the posterior pharyngeal arches. Thus, the key steps in our phylogenetic history are laid out during the development of our pharyngeal apparatus.

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“…The NC origin of the opercular series, as conclusively shown using our long-term labeling approach, was previously assumed on the basis of its dermal bone composition and the expression of specific transgenes (Kimmel et al, 2010). Recent findings demonstrating the presence of an embryonic operculum in amniotes have rekindled interest in this 923 RESEARCH ARTICLE NC origin of gill pillar cells structure, which was presumed to have been lost completely with the evolution of tetrapods and the emergence of a terrestrial lifestyle (Richardson et al, 2012).…”

Section: Nc Contribution To Cranial Skeletal Elements and Barbels In mentioning

confidence: 99%

Genetic lineage labeling in zebrafish uncovers novel neural crest contributions to the head, including gill pillar cells

et al. 2013

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SUMMARYAt the protochordate-vertebrate transition, a new predatory lifestyle and increased body size coincided with the appearance of a true head. Characteristic innovations of this head are a skull protecting and accommodating a centralized nervous system, a jaw for prey capture and gills as respiratory organs. The neural crest (NC) is a major ontogenetic source for the 'new head' of vertebrates and its contribution to the cranial skeleton has been intensively studied in different model organisms. However, the role of NC in the expansion of the respiratory surface of the gills has been neglected. Here, we use genetic lineage labeling to address the contribution of NC to specific head structures, in particular to the gills of adult zebrafish. We generated a sox10:ER T2 -Cre line and labeled NC cells by inducing Cre/loxP recombination with tamoxifen at embryonic stages. In juvenile and adult fish, we identified numerous established NC derivatives and, in the cranium, we precisely defined the crest/mesoderm interface of the skull roof. We show the NC origin of the opercular bones and of multiple cell types contributing to the barbels, chemosensory organs located in the mouth region. In the gills, we observed labeled primary and secondary lamellae. Clonal analysis reveals that pillar cells, a craniate innovation that mechanically supports the filaments and forms gill-specific capillaries, have a NC origin. Our data point to a crucial role for the NC in enabling more efficient gas exchange, thus uncovering a novel, direct involvement of this embryonic tissue in the evolution of respiratory systems at the protochordate-vertebrate transition.

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The presence of an embryonic opercular flap in amniotes

Cited by 22 publications

References 19 publications

A shared role for sonic hedgehog signalling in patterning chondrichthyan gill arch appendages and tetrapod limbs

A shared role for sonic hedgehog signalling in patterning chondrichthyan gill arch appendages and tetrapod limbs

Developmental and evolutionary origins of the pharyngeal apparatus

Genetic lineage labeling in zebrafish uncovers novel neural crest contributions to the head, including gill pillar cells

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