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. 2020 Oct;17(171):20200474.
doi: 10.1098/rsif.2020.0474. Epub 2020 Oct 14.

Endoskeletal mineralization in chimaera and a comparative guide to tessellated cartilage in chondrichthyan fishes (sharks, rays and chimaera)

Ronald Seidel  1   2 , Michael Blumer  3 , Júlia Chaumel  2 , Shahrouz Amini  2 , Mason N Dean  2
Affiliations

Endoskeletal mineralization in chimaera and a comparative guide to tessellated cartilage in chondrichthyan fishes (sharks, rays and chimaera)

Ronald Seidel et al. J R Soc Interface. 2020 Oct.

Abstract

An accepted uniting character of modern cartilaginous fishes (sharks, rays, chimaera) is the presence of a mineralized, skeletal crust, tiled by numerous minute plates called tesserae. Tesserae have, however, never been demonstrated in modern chimaera and it is debated whether the skeleton mineralizes at all. We show for the first time that tessellated cartilage was not lost in chimaera, as has been previously postulated, and is in many ways similar to that of sharks and rays. Tesserae in Chimaera monstrosa are less regular in shape and size in comparison to the general scheme of polygonal tesserae in sharks and rays, yet share several features with them. For example, Chimaera tesserae, like those of elasmobranchs, possess both intertesseral joints (unmineralized regions, where fibrous tissue links adjacent tesserae) and recurring patterns of local mineral density variation (e.g. Liesegang lines, hypermineralized 'spokes'), reflecting periodic accretion of mineral at tesseral edges as tesserae grow. Chimaera monstrosa's tesserae, however, appear to lack the internal cell networks that characterize tesserae in elasmobranchs, indicating fundamental differences among chondrichthyan groups in how calcification is controlled. By compiling and comparing recent ultrastructure data on tesserae, we also provide a synthesized, up-to-date and comparative glossary on tessellated cartilage, as well as a perspective on the current state of research into the topic, offering benchmark context for future research into modern and extinct vertebrate skeletal tissues.

Keywords: biomineralization; cartilaginous fish; tessellated cartilage; tesserae; vertebrate endoskeleton.

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Conflict of interest statement

We declare we have no competing interests.

Figures

Figure 1.
Figure 1.
Mineralized skeletal tissue in sharks and rays (Elasmobranchii) and the evolution of tessellated cartilage in cartilaginous fishes. (a) Sharks' and rays’ cartilaginous skeletons show two primary mineralized tissues, tessellated and areolar cartilage. Tessellated cartilage: comprises most of the endoskeleton, where the unmineralized skeletal core is sheathed in a mineralized and tessellated layer, shown here in the round stingray U. halleri and (i) its hyomandibula, a skeletal element connecting the jaws and cranium. (ii) Cross-sections of elasmobranch skeletal elements show the outer tessellated layer (t) is quite thin, with the bulk of the skeletal cross-section being unmineralized, hyaline-like cartilage (uc). (iii) In modern sharks and rays, the individual tesserae are typically small (less than or equal to 500 µm across), polygonal and numerous—for example, this hyomandibula is covered by thousands of tesserae. Areolar cartilage: a less studied and less broadly distributed tissue, found exclusively in the spool-shaped centra of (i) the vertebral column. (ii) A cross-section of a vertebra, showing a tessellated neural arch topping the (iii) centrum, with mineralized tissue concentric around the centrum's core (notochordal remnant). (b) A schematic cross-section of tessellated cartilage showing tesserae are closely associated with various types of connective tissue, sandwiched between a fibrous perichondrium and the cartilaginous skeletal core. (c) Condensed chondrichthyan phylogeny, including stem and crown groups and reflecting the current state of knowledge of the evolution of specific structural features of tessellated cartilage. The more elaborate ‘modern’ tesserae (see (b)) described in crown chondrichthyans appear to have been derived from simpler mineralized tiles in stem chondrichthyans. The difficulty determining phylogenetic affinities for extinct taxa (particularly stem chondrichthyans), the patchy phylogenetic record of tesserae from fossil species and the lack of broad comparative data for modern species currently limit our understanding of the precise occurrence of ‘modern’ tesserae and their ecological significance in chondrichthyans. Modern species data derived from the current work and studies cited in the text; fossil data and phylogeny synthesized from [2]. All images in (a) from Urobatis, except areolar cartilage, (i), from a tiger shark. All images from μCT scan data, except areolar cartilage, (ii and iii) from confocal fluorescence microscopy. See text for explanation of features; ch, chondrocytes; icz, intertesseral contact zone; ifz, intertesseral fibre zone with aligned fibre bundles linking tesserae; itj, intertesseral joint = icz + ifz; la, cell lacunae; lil, Liesegang lines; sh, Sharpey's fibres; sp, spokes. (Image (b) adapted from [3] with permission from Elsevier.)
Figure 2.
Figure 2.
Variation in tessellation patterns in elasmobranchs and holocephalans. Computed tomography virtual sections of tesserae (T; with individual tesserae coloured yellow) from four different elasmobranch species: (a,e) a skate, Raja stellulata; (b,f) a stingray, Pteroplatytrygon violacea and two sharks (c,g) Heterodontus francisci; (d,h) Notorynchus cepedianus; and a holocephalan species (i–k) C. monstrosa. Images a–d and i,j show virtual planar sections, e–h,k are virtual vertical sections of tesserae. (i) The tiling pattern of skeletal mineralization in the chondrocranium of C. monstrosa appears most similar to that of the broadnose sevengill shark Notorynchus cepedianus (d,h), with tesserae exhibiting irregular geometric shapes and almost no cellular lacunae (visible as black dots in most of the elasmobranch tesserae). The presence of cell lacunae is considered the standard condition for (a–h) elasmobranch tesserae. (j) Averaged planar section created from six consecutive sections, revealing tesserae borders (intertesseral joints), which were not clearly visible in (i) a single section plane. (k) In vertical sections, some adjacent tesserae in C. monstrosa overlap (red tesserae, marked with arrowheads), whereas others are in contact at their lateral edges (intertesseral joints, marked with arrows). (Images a–h adapted from [23] with permission from Wiley.)
Figure 3.
Figure 3.
Patterns of mineral density variation in tesserae. BSE allows visualization of differences in either tissue elemental density (e.g. mineral density) or elemental composition as variation in greyscale values (low and high concentrations shown as dark and bright grey values, respectively). Although tesserae from (a,b) chain catshark Scyliorhinus retifer, (c–f) U. halleri and (g–j) C. monstrosa differ in their morphology and tiling pattern, they show similar intratesseral features of varying mineral density. All three species exhibit acellular spokes (sp), high mineral density features in regions where adjacent tesserae abut one another (intertesseral contact zones, icz). Unlike in the elasmobranch tesserae, in some regions, in Chimaera (g), adjacent tesserae appear fused (stars). Liesegang lines (lil), successive growth lines reflecting accretional growth in elasmobranchs; (e) Liesegang lines (lil) in tesserae from U. halleri, are also visible in (h) tesserae from C. monstrosa. (g–i) Unlike the majority of elasmobranch tesserae, tesserae in C. monstrosa lack cell lacunae (la). Dark, ovoid regions, however, suggest the presence of mineralized cells (mc) or in-filled cell lacunae. (j) Mineralized globules associated with tesseral borders (arrowheads) suggest similar mechanisms of accretional growth between elasmobranch and chimaera tesserae [23].
Figure 4.
Figure 4.
Intertesseral joints and spokes. LM and TEM of adjacent tesserae from an elasmobranch and chimaera. (a,b,e–f) In demineralized tesserae from both elasmobranch (U. halleri) and chimaera (C. monstrosa), spokes (Sp) are visible as laminated structures, their laminae parallel to the lateral edge of the tesserae where they abut one another. (c,d,g,h) Intertesseral fibrous zones (IFZ), gaps between tesserae filled with densely aligned fibre bundles linking adjacent tesserae. (d) Between the fibre bundles, cells are aligned in strings in elasmobranchs, whereas (h) in chimaera, very few cells were visible in the IFZ. Images: (a, c and e) LM images of toluidine blue and (g) H&E stained sections; (d,h) polarized LM images of (c,g), respectively; (b,f) TEM images.
Figure 5.
Figure 5.
Chemical and mechanical similarity of elasmobranch and holocephalan tesserae. (a) Area normalized spectral graphs (EDX) of tesserae from C. monstrosa and round stingray U. halleri, and elemental maps from chimaera tesserae showing no regional variation in elemental composition. Relatively high phosphate concentrations result in low Ca/P ratios in both elasmobranch and chimaera tesserae (atomic percent: approx. 1.25 at% and approx. 1.35 at%, respectively) in comparison to bone (approx. 1.59 at%) [101]. (b) Raman spectra of tesserae from U. halleri and C. monstrosa, identifying the mineral in both as carbonated apatite. Raman peaks indicating vibrational bands of the phosphate group in the apatite. (c) Nanoindentation of C. monstrosa tesserae (planar section, figure 3g), illustrating a positive correlation of mineral density (grey value from the BSE image) and mechanical properties (indentation modulus and hardness), similar to that seen in elasmobranch tesserae [13]. (d) Range (coloured bars), mean (black line) and standard deviation (dashed line) of indentation modulus, stiffness (E) and hardness (H) values from non-spoke and spoke regions in planar sections of tesserae from C. monstrosa and U. halleri [13].
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References

    1. Hall BK. 2005. Bones and cartilage: developmental skeletal biology. London, UK: Academic Press.
    1. Maisey John G, Denon John SS, Carole B, Alan P. 2020. Architectural and ultrastructural features of tessellated calcified cartilage in modern and extinct chondrichthyan fishes. J. Fish Biol. 1–23. (10.1111/jfb.14376) - DOI - PubMed
    1. Seidel R, Blumer M, Pechriggl EJ, Lyons K, Hall BK, Fratzl P, Weaver JC, Dean MN. 2017. Calcified cartilage or bone? Collagens in the tessellated endoskeletons of cartilaginous fish (sharks and rays). J. Struct. Biol. 200, 54–71. (10.1016/j.jsb.2017.09.005) - DOI - PubMed
    1. Applegate SP. 1967. A survey of shark hard parts, pp. 37–66. Baltimore, MD: Johns Hopkins University Press.
    1. Dean MN, Summers AP. 2006. Mineralized cartilage in the skeleton of chondrichthyan fishes. Zoology 109, 164–168. (10.1016/j.zool.2006.03.002) - DOI - PubMed

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