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  • 1
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    Trunk neural crest origin of dermal denticles in a cartilaginous fish (2017)
    National Academy of Sciences
    Details
    Publication Date: 2017-11-20
    Description: 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.
    Print ISSN: 0027-8424
    Electronic ISSN: 1091-6490
    Topics: Biology , Medicine , Natural Sciences in General
    Published by National Academy of Sciences
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  • 2
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    Resegmentation is an ancestral feature of the gnathostome vertebral skeleton (2020)
    eLife Sciences Publications
    Details
    Publication Date: 2020-02-24
    Description: 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.
    Electronic ISSN: 2050-084X
    Topics: Biology , Medicine , Natural Sciences in General
    Published by eLife Sciences Publications
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  • 3
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    Extraocular, rod-like photoreceptors in a flatworm express xenopsin photopigment (2019)
    eLife Sciences Publications
    Details
    Publication Date: 2019-10-22
    Description: Animals detect light using opsin photopigments. Xenopsin, a recently classified subtype of opsin, challenges our views on opsin and photoreceptor evolution. Originally thought to belong to the Gαi-coupled ciliary opsins, xenopsins are now understood to have diverged from ciliary opsins in pre-bilaterian times, but little is known about the cells that deploy these proteins, or if they form a photopigment and drive phototransduction. We characterized xenopsin in a flatworm, Maritigrella crozieri, and found it expressed in ciliary cells of eyes in the larva, and in extraocular cells around the brain in the adult. These extraocular cells house hundreds of cilia in an intra-cellular vacuole (phaosome). Functional assays in human cells show Maritigrella xenopsin drives phototransduction primarily by coupling to Gαi. These findings highlight similarities between xenopsin and c-opsin and reveal a novel type of opsin-expressing cell that, like jawed vertebrate rods, encloses the ciliary membrane within their own plasma membrane.
    Electronic ISSN: 2050-084X
    Topics: Biology , Medicine , Natural Sciences in General
    Published by eLife Sciences Publications
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  • 4
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    A symmoriiform chondrichthyan braincase and the origin of chimaeroid fishes (2017)
    Springer Nature
    Details
    Publication Date: 2017-01-01
    Print ISSN: 0028-0836
    Electronic ISSN: 1476-4687
    Topics: Biology , Chemistry and Pharmacology , Medicine , Natural Sciences in General , Physics
    Published by Springer Nature
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  • 5
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    A Dome-Headed Stem Archosaur Exemplifies Convergence among Dinosaurs and Their Distant Relatives (2016)
    Cell Press
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    Publication Date: 2016-10-01
    Print ISSN: 0960-9822
    Electronic ISSN: 1879-0445
    Topics: Biology
    Published by Cell Press
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  • 6
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    Conserved and unique transcriptional features of pharyngeal arches in the skate (Leucoraja erinacea) and evolution of the jaw (2021)
    Oxford University Press
    Details
    Publication Date: 2021-04-27
    Description: The origin of the jaw is a long-standing problem in vertebrate evolutionary biology. Classical hypotheses of serial homology propose that the upper and lower jaw evolved through modifications of dorsal and ventral gill arch skeletal elements, respectively. If the jaw and gill arches are derived members of a primitive branchial series, we predict that they would share common developmental patterning mechanisms. Using candidate and RNAseq/differential gene expression analyses, we find broad conservation of dorsoventral (DV) patterning mechanisms within the developing mandibular, hyoid, and gill arches of a cartilaginous fish, the skate (Leucoraja erinacea). Shared features include expression of genes encoding members of the ventralizing BMP and endothelin signaling pathways and their effectors, the joint markers nkx3.2 and gdf5 and prochondrogenic transcription factor barx1, and the dorsal territory marker pou3f3. Additionally, we find that mesenchymal expression of eya1/six1 is an ancestral feature of the mandibular arch of jawed vertebrates, whereas differences in notch signaling distinguish the mandibular and gill arches in skate. Comparative transcriptomic analyses of mandibular and gill arch tissues reveal additional genes differentially expressed along the DV axis of the pharyngeal arches, including scamp5 as a novel marker of the dorsal mandibular arch, as well as distinct transcriptional features of mandibular and gill arch muscle progenitors and developing gill buds. Taken together, our findings reveal conserved patterning mechanisms in the pharyngeal arches of jawed vertebrates, consistent with serial homology of their skeletal derivatives, as well as unique transcriptional features that may underpin distinct jaw and gill arch morphologies.
    Print ISSN: 0737-4038
    Electronic ISSN: 1537-1719
    Topics: Biology
    Published by Oxford University Press
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  • 7
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    Hox gene expression predicts tetrapod-like axial regionalization in the skate, Leucoraja erinacea (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-27
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Criswell, K. E., Roberts, L. E., Koo, E. T., Head, J. J., & Gillis, J. A. Hox gene expression predicts tetrapod-like axial regionalization in the skate, Leucoraja erinacea. Proceedings of the National Academy of Sciences of the United States of America, 118(51), (2021): e2114563118, https://doi.org/10.1073/pnas.2114563118.
    Description: 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.
    Description: This research was funded by a Natural Environment Research Council Grant (to J.J.H., J.A.G., and K.E.C.: NE/S000739/1) and a Royal Society University Research Fellowship (UF130182 and URF\R\191007), Royal Society Research Grant (RG140377), and University of Cambridge Sir Isaac Newton Trust Grant (14.23z) (to J.A.G.).
    Keywords: Hox genes ; Regionalization ; Chondrichthyan ; Vertebral column
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 8
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    Resegmentation is an ancestral feature of the gnathostome vertebral skeleton (2020)
    eLife Sciences Publications
    Details
    Publication Date: 2022-05-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Criswell, K. E., & Gillis, J. A. Resegmentation is an ancestral feature of the gnathostome vertebral skeleton. Elife, 9, (2020): e51696, doi:10.7554/elife.51696.
    Description: 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.
    Description: Royal Society (NF160762) Katharine E Criswell Royal Society (UF130182) J. Andrew Gillis Marine Biological Laboratory Katharine E. Criswell
    Repository Name: Woods Hole Open Access Server
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  • 9
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    Conserved and unique transcriptional features of pharyngeal arches in the skate (Leucoraja erinacea) and evolution of the jaw (2021)
    Oxford University Press
    Details
    Publication Date: 2022-05-27
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Hirschberger, C., Sleight, V. A., Criswell, K. E., Clark, S. J., & Gillis, J. A. Conserved and unique transcriptional features of pharyngeal arches in the skate (Leucoraja erinacea) and evolution of the jaw. Molecular Biology and Evolution, (2021): msab123, https://doi.org/10.1093/molbev/msab123
    Description: The origin of the jaw is a long-standing problem in vertebrate evolutionary biology. Classical hypotheses of serial homology propose that the upper and lower jaw evolved through modifications of dorsal and ventral gill arch skeletal elements, respectively. If the jaw and gill arches are derived members of a primitive branchial series, we predict that they would share common developmental patterning mechanisms. Using candidate and RNAseq/differential gene expression analyses, we find broad conservation of dorsoventral patterning mechanisms within the developing mandibular, hyoid and gill arches of a cartilaginous fish, the skate (Leucoraja erinacea). Shared features include expression of genes encoding members of the ventralising BMP and endothelin signalling pathways and their effectors, the joint markers nkx3.2 and gdf5 and pro-chondrogenic transcription factor barx1, and the dorsal territory marker pou3f3. Additionally, we find that mesenchymal expression of eya1/six1 is an ancestral feature of the mandibular arch of jawed vertebrates, while differences in notch signalling distinguish the mandibular and gill arches in skate. Comparative transcriptomic analyses of mandibular and gill arch tissues reveal additional genes differentially expressed along the dorsoventral axis of the pharyngeal arches, including scamp5 as a novel marker of the dorsal mandibular arch, as well as distinct transcriptional features of mandibular and gill arch muscle progenitors and developing gill buds. Taken together, our findings reveal conserved patterning mechanisms in the pharyngeal arches of jawed vertebrates, consistent with serial homology of their skeletal derivatives, as well as unique transcriptional features that may underpin distinct jaw and gill arch morphologies.
    Description: This work was supported by a Biotechnology and Biological Sciences Research Council Doctoral Training Partnership studentship to CH, by a Wolfson College Junior Research Fellowship and MBL Whitman Early Career Fellowship to VAS, and by a Royal Society University Research Fellowship (UF130182 and URF\R\191007), Royal Society Research Grant (RG140377) and University of Cambridge Sir Isaac Newton Trust Grant (14.23z) to JAG.
    Repository Name: Woods Hole Open Access Server
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  • 10
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    Extraocular, rod-like photoreceptors in a flatworm express xenopsin photopigment (2020)
    eLife Sciences Publications
    Details
    Publication Date: 2022-05-26
    Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Rawlinson, K. A., Lapraz, F., Ballister, E. R., Terasaki, M., Rodgers, J., McDowell, R. J., Girstmair, J., Criswell, K. E., Boldogkoi, M., Simpson, F., Goulding, D., Cormie, C., Hall, B., Lucas, R. J., & Telford, M. J. Extraocular, rod-like photoreceptors in a flatworm express xenopsin photopigment. Elife, 8, (2019): e45465, doi: 10.7554/eLife.45465.
    Description: Animals detect light using opsin photopigments. Xenopsin, a recently classified subtype of opsin, challenges our views on opsin and photoreceptor evolution. Originally thought to belong to the Gαi-coupled ciliary opsins, xenopsins are now understood to have diverged from ciliary opsins in pre-bilaterian times, but little is known about the cells that deploy these proteins, or if they form a photopigment and drive phototransduction. We characterized xenopsin in a flatworm, Maritigrella crozieri, and found it expressed in ciliary cells of eyes in the larva, and in extraocular cells around the brain in the adult. These extraocular cells house hundreds of cilia in an intra-cellular vacuole (phaosome). Functional assays in human cells show Maritigrella xenopsin drives phototransduction primarily by coupling to Gαi. These findings highlight similarities between xenopsin and c-opsin and reveal a novel type of opsin-expressing cell that, like jawed vertebrate rods, encloses the ciliary membrane within their own plasma membrane.
    Description: We thank Andrew Gillis and Ariane Dimitris for help in the field, Kasia Hammar, Paul Linser, Anne Zakrzewski and Sidney Tamm for support in electron microscopy fixation, analysis and interpretation, Elaine Seaver and Danielle de Jong for helping to establish an in situ hybridization protocol for the Maritigrella crozieri larval stage, and Matthew Berriman and Michael Akam (Isaac Newton Trust grant (15.4(n)) for support in securing funding to complete this work. We thank the two reviewers whose comments and suggestions helped improve and clarify this manuscript. The research was supported by a a Wellcome Trust Janet Thornton Fellowship (WT206194) to KR, a research exchange award to KR through the EDEN NSF Network (National Foundation Grant Number IOS-0955517 to Cassandra G Extavour), a Natural Sciences and Engineering Research grant (A5056) to BKH and by a Biotechnology and Biological Sciences Research Council grant (BB/H006966/1) (FL) and a Leverhulme Trust grant (F/07 134/DA) to MT. MT is supported by European Research Council (ERC-2012-AdG 322790).
    Repository Name: Woods Hole Open Access Server
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