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Bricks, trusses and superstructures: Strategies for skeletal reinforcement in batoid fishes (rays and skates)

Crushing and eating hard prey (durophagy) is mechanically demanding. The cartilage jaws of durophagous stingrays are known to be reinforced relative to non-durophagous relatives, with a thickened external cortex of mineralized blocks (tesserae), reinforcing struts inside the jaw (trabeculae), and pa...

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Autores principales: Clark, Brett, Chaumel, Júlia, Johanson, Zerina, Underwood, Charlie, Smith, Moya M., Dean, Mason N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9604235/
https://www.ncbi.nlm.nih.gov/pubmed/36313571
http://dx.doi.org/10.3389/fcell.2022.932341
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author Clark, Brett
Chaumel, Júlia
Johanson, Zerina
Underwood, Charlie
Smith, Moya M.
Dean, Mason N.
author_facet Clark, Brett
Chaumel, Júlia
Johanson, Zerina
Underwood, Charlie
Smith, Moya M.
Dean, Mason N.
author_sort Clark, Brett
collection PubMed
description Crushing and eating hard prey (durophagy) is mechanically demanding. The cartilage jaws of durophagous stingrays are known to be reinforced relative to non-durophagous relatives, with a thickened external cortex of mineralized blocks (tesserae), reinforcing struts inside the jaw (trabeculae), and pavement-like dentition. These strategies for skeletal strengthening against durophagy, however, are largely understood only from myliobatiform stingrays, although a hard prey diet has evolved multiple times in batoid fishes (rays, skates, guitarfishes). We perform a quantitative analysis of micro-CT data, describing jaw strengthening mechanisms in Rhina ancylostoma (Bowmouth Guitarfish) and Rhynchobatus australiae (White-spotted Wedgefish), durophagous members of the Rhinopristiformes, the sister taxon to Myliobatiformes. Both species possess trabeculae, more numerous and densely packed in Rhina, albeit simpler structurally than those in stingrays like Aetobatus and Rhinoptera. Rhina and Rhynchobatus exhibit impressively thickened jaw cortices, often involving >10 tesseral layers, most pronounced in regions where dentition is thickest, particularly in Rhynchobatus. Age series of both species illustrate that tesserae increase in size during growth, with enlarged and irregular tesserae associated with the jaws’ oral surface in larger (older) individuals of both species, perhaps a feature of ageing. Unlike the flattened teeth of durophagous myliobatiform stingrays, both rhinopristiform species have oddly undulating dentitions, comprised of pebble-like teeth interlocked to form compound “meta-teeth” (large spheroidal structures involving multiple teeth). This is particularly striking in Rhina, where the upper/lower occlusal surfaces are mirrored undulations, fitting together like rounded woodworking finger-joints. Trabeculae were previously thought to have arisen twice independently in Batoidea; our results show they are more widespread among batoid groups than previously appreciated, albeit apparently absent in the phylogenetically basal Rajiformes. Comparisons with several other durophagous and non-durophagous species illustrate that batoid skeletal reinforcement architectures are modular: trabeculae can be variously oriented and are dominant in some species (e.g. Rhina, Aetobatus), whereas cortical thickening is more significant in others (e.g. Rhynchobatus), or both reinforcing features can be lacking (e.g. Raja, Urobatis). We discuss interactions and implications of character states, framing a classification scheme for exploring cartilage structure evolution in the cartilaginous fishes.
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spelling pubmed-96042352022-10-27 Bricks, trusses and superstructures: Strategies for skeletal reinforcement in batoid fishes (rays and skates) Clark, Brett Chaumel, Júlia Johanson, Zerina Underwood, Charlie Smith, Moya M. Dean, Mason N. Front Cell Dev Biol Cell and Developmental Biology Crushing and eating hard prey (durophagy) is mechanically demanding. The cartilage jaws of durophagous stingrays are known to be reinforced relative to non-durophagous relatives, with a thickened external cortex of mineralized blocks (tesserae), reinforcing struts inside the jaw (trabeculae), and pavement-like dentition. These strategies for skeletal strengthening against durophagy, however, are largely understood only from myliobatiform stingrays, although a hard prey diet has evolved multiple times in batoid fishes (rays, skates, guitarfishes). We perform a quantitative analysis of micro-CT data, describing jaw strengthening mechanisms in Rhina ancylostoma (Bowmouth Guitarfish) and Rhynchobatus australiae (White-spotted Wedgefish), durophagous members of the Rhinopristiformes, the sister taxon to Myliobatiformes. Both species possess trabeculae, more numerous and densely packed in Rhina, albeit simpler structurally than those in stingrays like Aetobatus and Rhinoptera. Rhina and Rhynchobatus exhibit impressively thickened jaw cortices, often involving >10 tesseral layers, most pronounced in regions where dentition is thickest, particularly in Rhynchobatus. Age series of both species illustrate that tesserae increase in size during growth, with enlarged and irregular tesserae associated with the jaws’ oral surface in larger (older) individuals of both species, perhaps a feature of ageing. Unlike the flattened teeth of durophagous myliobatiform stingrays, both rhinopristiform species have oddly undulating dentitions, comprised of pebble-like teeth interlocked to form compound “meta-teeth” (large spheroidal structures involving multiple teeth). This is particularly striking in Rhina, where the upper/lower occlusal surfaces are mirrored undulations, fitting together like rounded woodworking finger-joints. Trabeculae were previously thought to have arisen twice independently in Batoidea; our results show they are more widespread among batoid groups than previously appreciated, albeit apparently absent in the phylogenetically basal Rajiformes. Comparisons with several other durophagous and non-durophagous species illustrate that batoid skeletal reinforcement architectures are modular: trabeculae can be variously oriented and are dominant in some species (e.g. Rhina, Aetobatus), whereas cortical thickening is more significant in others (e.g. Rhynchobatus), or both reinforcing features can be lacking (e.g. Raja, Urobatis). We discuss interactions and implications of character states, framing a classification scheme for exploring cartilage structure evolution in the cartilaginous fishes. Frontiers Media S.A. 2022-10-12 /pmc/articles/PMC9604235/ /pubmed/36313571 http://dx.doi.org/10.3389/fcell.2022.932341 Text en Copyright © 2022 Clark, Chaumel, Johanson, Underwood, Smith and Dean. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Clark, Brett
Chaumel, Júlia
Johanson, Zerina
Underwood, Charlie
Smith, Moya M.
Dean, Mason N.
Bricks, trusses and superstructures: Strategies for skeletal reinforcement in batoid fishes (rays and skates)
title Bricks, trusses and superstructures: Strategies for skeletal reinforcement in batoid fishes (rays and skates)
title_full Bricks, trusses and superstructures: Strategies for skeletal reinforcement in batoid fishes (rays and skates)
title_fullStr Bricks, trusses and superstructures: Strategies for skeletal reinforcement in batoid fishes (rays and skates)
title_full_unstemmed Bricks, trusses and superstructures: Strategies for skeletal reinforcement in batoid fishes (rays and skates)
title_short Bricks, trusses and superstructures: Strategies for skeletal reinforcement in batoid fishes (rays and skates)
title_sort bricks, trusses and superstructures: strategies for skeletal reinforcement in batoid fishes (rays and skates)
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9604235/
https://www.ncbi.nlm.nih.gov/pubmed/36313571
http://dx.doi.org/10.3389/fcell.2022.932341
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