scholarly journals Embryonic origin of the gnathostome vertebral skeleton

2017 ◽  
Vol 284 (1867) ◽  
pp. 20172121 ◽  
Author(s):  
Katharine E. Criswell ◽  
Michael I. Coates ◽  
J. Andrew Gillis
Keyword(s):  
Vertebral Column ◽  
Bone Matrix ◽  
Cell Lineage ◽  
Body Plan ◽  
Cartilaginous Fish ◽  
Lineage Tracing ◽  
Paraxial Mesoderm ◽  
Teleost Fishes ◽  
Embryonic Origin

The vertebral column is a key component of the jawed vertebrate (gnathostome) body plan, but the primitive embryonic origin of this skeleton remains unclear. In tetrapods, all vertebral components (neural arches, haemal arches and centra) derive from paraxial mesoderm (somites). However, in teleost fishes, vertebrae have a dual embryonic origin, with arches derived from somites, but centra formed, in part, by secretion of bone matrix from the notochord. Here, we test the embryonic origin of the vertebral skeleton in a cartilaginous fish (the skate, Leucoraja erinacea ) which serves as an outgroup to tetrapods and teleosts. We demonstrate, by cell lineage tracing, that both arches and centra are somite-derived. We find no evidence of cellular or matrix contribution from the notochord to the skate vertebral skeleton. These findings indicate that the earliest gnathostome vertebral skeleton was exclusively of somitic origin, with a notochord contribution arising secondarily in teleosts.

scholarly journals Resegmentation is an ancestral feature of the gnathostome vertebral skeleton

2019 ◽  
Author(s):  
Katharine E. Criswell ◽  
J. Andrew Gillis
Keyword(s):  
Cell Lineage ◽  
Body Plan ◽  
Cartilaginous Fish ◽  
Lineage Tracing ◽  
Teleost Fishes ◽  
Body Segment ◽  
The Relationship

AbstractThe vertebral skeleton is a defining feature of vertebrate animals. However, the mode of vertebral segmentation varies considerably between major lineages. In tetrapods, adjacent somite halves recombine to form a single vertebra through the process of “resegmentation”. However, in teleost fishes, there is considerable mixing between cells of the anterior and posterior somite halves, without clear resegmentation. To determine whether resegmentation is a tetrapod novelty, or an ancestral feature of jawed vertebrates, we tested the relationship between somites and vertebrae in a cartilaginous fish, the skate (Leucoraja erinacea). Using cell lineage tracing, we show that skate trunk vertebrae arise through tetrapod-like resegmentation, with anterior and posterior halves of each vertebra deriving from adjacent somites. We further show that tail vertebrae also arise through resegmentation, despite a duplication of the number of vertebrae per body segment. These findings resolve axial resegmentation as an ancestral feature of the jawed vertebrate body plan.

scholarly journals Resegmentation is an ancestral feature of the gnathostome vertebral skeleton

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Katharine E Criswell ◽  
J Andrew Gillis
Keyword(s):  
Cell Lineage ◽  
Body Plan ◽  
Cartilaginous Fish ◽  
Lineage Tracing ◽  
Teleost Fishes ◽  
Body Segment ◽  
The Relationship

The vertebral skeleton is a defining feature of vertebrate animals. However, the mode of vertebral segmentation varies considerably between major lineages. In tetrapods, adjacent somite halves recombine to form a single vertebra through the process of ‘resegmentation’. In teleost fishes, there is considerable mixing between cells of the anterior and posterior somite halves, without clear resegmentation. To determine whether resegmentation is a tetrapod novelty, or an ancestral feature of jawed vertebrates, we tested the relationship between somites and vertebrae in a cartilaginous fish, the skate (Leucoraja erinacea). Using cell lineage tracing, we show that skate trunk vertebrae arise through tetrapod-like resegmentation, with anterior and posterior halves of each vertebra deriving from adjacent somites. We further show that tail vertebrae also arise through resegmentation, though with a duplication of the number of vertebrae per body segment. These findings resolve axial resegmentation as an ancestral feature of the jawed vertebrate body plan.

scholarly journals Embryonic origin and serial homology of gill arches and paired fins in the skate (Leucoraja erinacea)

2020 ◽  
Author(s):  
Victoria A. Sleight ◽  
J. Andrew Gillis
Keyword(s):  
Neural Crest ◽  
Cell Lineage ◽  
Body Plan ◽  
Lineage Tracing ◽  
Germ Layers ◽  
Axial Patterning ◽  
Serial Homology ◽  
Embryonic Origin ◽  
Dual Origin ◽  
Derivatives Of

AbstractPaired fins are a defining feature of the jawed vertebrate body plan, but their evolutionary origin remains unresolved. Gegenbaur proposed that paired fins evolved as gill arch serial homologues, but this hypothesis is now widely discounted, owing largely to the presumed distinct embryonic origins of these structures from mesoderm and neural crest, respectively. Here, we use cell lineage tracing to test the embryonic origin of the pharyngeal and paired fin skeleton in the skate (Leucoraja erinacea). We find that while the jaw and hyoid arch skeleton derive from neural crest, and the pectoral fin skeleton from mesoderm, the gill arches are of dual origin, receiving contributions from both germ layers. We propose that gill arches and paired fins are serially homologous as derivatives of a continuous, dual-origin mesenchyme with common skeletogenic competence, and that this serial homology accounts for their parallel anatomical organization and shared responses to axial patterning signals.

scholarly journals hox gene expression predicts tetrapod-like axial regionalization in the skate, Leucoraja erinacea

2021 ◽  
Vol 118 (51) ◽  
pp. e2114563118
Author(s):  
Katharine E. Criswell ◽  
Lucy E. Roberts ◽  
Eve T. Koo ◽  
Jason J. Head ◽  
J. Andrew Gillis
Keyword(s):  
Gene Expression ◽  
Vertebral Column ◽  
Evolutionary History ◽  
Cell Lineage ◽  
Axial Skeleton ◽  
Lineage Tracing ◽  
Paraxial Mesoderm ◽  
Evolutionary Transition ◽  
Geometric Morphometric ◽  
Geometric Morphometric Analysis

The axial skeleton of tetrapods is organized into distinct anteroposterior regions of the vertebral column (cervical, trunk, sacral, and caudal), and transitions between these regions are determined by colinear anterior expression boundaries of Hox5/6, -9, -10, and -11 paralogy group genes within embryonic paraxial mesoderm. Fishes, conversely, exhibit little in the way of discrete axial regionalization, and this has led to scenarios of an origin of Hox-mediated axial skeletal complexity with the evolutionary transition to land in tetrapods. Here, combining geometric morphometric analysis of vertebral column morphology with cell lineage tracing of hox gene expression boundaries in developing embryos, we recover evidence of at least five distinct regions in the vertebral skeleton of a cartilaginous fish, the little skate (Leucoraja erinacea). We find that skate embryos exhibit tetrapod-like anteroposterior nesting of hox gene expression in their paraxial mesoderm, and we show that anterior expression boundaries of hox5/6, hox9, hox10, and hox11 paralogy group genes predict regional transitions in the differentiated skate axial skeleton. Our findings suggest that hox-based axial skeletal regionalization did not originate with tetrapods but rather has a much deeper evolutionary history than was previously appreciated.

scholarly journals Embryonic origin and serial homology of gill arches and paired fins in the skate, Leucoraja erinacea

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Victoria A Sleight ◽  
J Andrew Gillis
Keyword(s):  
Neural Crest ◽  
Cell Lineage ◽  
Body Plan ◽  
Lineage Tracing ◽  
Germ Layers ◽  
Axial Patterning ◽  
Serial Homology ◽  
Embryonic Origin ◽  
Dual Origin ◽  
Derivatives Of

Paired fins are a defining feature of the jawed vertebrate body plan, but their evolutionary origin remains unresolved. Gegenbaur proposed that paired fins evolved as gill arch serial homologues, but this hypothesis is now widely discounted, owing largely to the presumed distinct embryonic origins of these structures from mesoderm and neural crest, respectively. Here, we use cell lineage tracing to test the embryonic origin of the pharyngeal and paired fin skeleton in the skate (Leucoraja erinacea). We find that while the jaw and hyoid arch skeleton derive from neural crest, and the pectoral fin skeleton from mesoderm, the gill arches are of dual origin, receiving contributions from both germ layers. We propose that gill arches and paired fins are serially homologous as derivatives of a continuous, dual-origin mesenchyme with common skeletogenic competence, and that this serial homology accounts for their parallel anatomical organization and shared responses to axial patterning signals.

scholarly journals Trunk neural crest origin of dermal denticles in a cartilaginous fish

2017 ◽  
Vol 114 (50) ◽  
pp. 13200-13205 ◽  
Author(s):  
J. Andrew Gillis ◽  
Els C. Alsema ◽  
Katharine E. Criswell
Keyword(s):  
Neural Crest ◽  
Cell Lineage ◽  
Neural Crest Cell ◽  
Neural Crest Cells ◽  
Cartilaginous Fish ◽  
Lineage Tracing ◽  
Skeletal Tissue ◽  
Trunk Neural Crest ◽  
Neural Crest Origin ◽  
Cranial Neural Crest Cells

Cartilaginous fishes (e.g., sharks and skates) possess a postcranial dermal skeleton consisting of tooth-like “denticles” embedded within their skin. As with teeth, the principal skeletal tissue of dermal denticles is dentine. In the head, cranial neural crest cells give rise to the dentine-producing cells (odontoblasts) of teeth. However, trunk neural crest cells are generally regarded as nonskeletogenic, and so the embryonic origin of trunk denticle odontoblasts remains unresolved. Here, we use expression of FoxD3 to pinpoint the specification and emigration of trunk neural crest cells in embryos of a cartilaginous fish, the little skate (Leucoraja erinacea). Using cell lineage tracing, we further demonstrate that trunk neural crest cells do, in fact, give rise to odontoblasts of trunk dermal denticles. These findings expand the repertoire of vertebrate trunk neural crest cell fates during normal development, highlight the likely primitive skeletogenic potential of this cell population, and point to a neural crest origin of dentine throughout the ancestral vertebrate dermal skeleton.

scholarly journals The pseudobranch of jawed vertebrates is a mandibular arch-derived gill

2021 ◽  
Author(s):  
Christine Hirschberger ◽  
J. Andrew Gillis
Keyword(s):  
Gene Expression ◽  
Cell Lineage ◽  
Cell Types ◽  
Cartilaginous Fish ◽  
Lineage Tracing ◽  
Gill Arch ◽  
Pharyngeal Arch ◽  
Anatomical Features ◽  
Mandibular Arch ◽  
Ancestral Origin

AbstractThe pseudobranch is a gill-like epithelial elaboration that sits behind the jaw of most fishes. This structure was classically regarded as a vestige of the ancestral gill-arch like condition of the gnathostome jaw. However, more recently, hypotheses of jaw evolution by transformation of a gill arch have been challenged, and the pseudobranch has alternatively been considered a specialised derivative of the second (hyoid) pharyngeal arch. Here, we demonstrate by cell lineage tracing in a cartilaginous fish, the skate (Leucoraja erinacea), that the pseudobranch does, in fact, derive from the mandibular arch, and that it shares gene expression features and cell types with gills. We also show that the mandibular arch pseudobranch is supported by a spiracular cartilage that is patterned by a shh-expressing epithelial signalling centre. This closely parallels the condition seen in the gill arches, where cartilaginous appendages called branchial rays supporting the respiratory lamellae of the gills are patterned by a shh-expressing gill arch epithelial ridge (GAER). Taken together, these findings support serial homology of the pseudobranch and gills, and an ancestral origin of gill arch-like anatomical features from the gnathostome mandibular arch.

scholarly journals Nerve-associated Schwann cell precursors contribute extracutaneous melanocytes to the heart, inner ear, supraorbital locations and brain meninges

2021 ◽  
Author(s):  
Marketa Kaucka ◽  
Bara Szarowska ◽  
Michaela Kavkova ◽  
Maria Eleni Kastriti ◽  
Polina Kameneva ◽  
...  
Keyword(s):  
Schwann Cell ◽  
Inner Ear ◽  
Gene Knockout ◽  
Hair Follicles ◽  
Lineage Tracing ◽  
Pigment Cells ◽  
Hearing Function ◽  
Embryonic Origin ◽  
Schwann Cell Precursors ◽  
Evolutionary Aspects

AbstractMelanocytes are pigmented cells residing mostly in the skin and hair follicles of vertebrates, where they contribute to colouration and protection against UV-B radiation. However, the spectrum of their functions reaches far beyond that. For instance, these pigment-producing cells are found inside the inner ear, where they contribute to the hearing function, and in the heart, where they are involved in the electrical conductivity and support the stiffness of cardiac valves. The embryonic origin of such extracutaneous melanocytes is not clear. We took advantage of lineage-tracing experiments combined with 3D visualizations and gene knockout strategies to address this long-standing question. We revealed that Schwann cell precursors are recruited from the local innervation during embryonic development and give rise to extracutaneous melanocytes in the heart, brain meninges, inner ear, and other locations. In embryos with a knockout of the EdnrB receptor, a condition imitating Waardenburg syndrome, we observed only nerve-associated melanoblasts, which failed to detach from the nerves and to enter the inner ear. Finally, we looked into the evolutionary aspects of extracutaneous melanocytes and found that pigment cells are associated mainly with nerves and blood vessels in amphibians and fish. This new knowledge of the nerve-dependent origin of extracutaneous pigment cells might be directly relevant to the formation of extracutaneous melanoma in humans.

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