Architectural and ultrastructural features of tessellated calcified cartilage in modern and extinct chondrichthyan fishes.

Tessellated calcified cartilage (TCC) is a distinctive kind of biomineralized perichondral tissue found in many modern and extinct chondrichthyans (sharks, rays, chimaeroids and their extinct allies). Customarily, this feature has been treated somewhat superficially in phylogenetic analyses, often as a single "defining" character of a chondrichthyan clade. TCC is actually a complex hard tissue with numerous distinctive attributes, but its use as a character complex for phylogenetic analysis has not yet been optimized. This study attempts to improve this situation by presenting new terminology for certain aspects of tesseral architecture, including single-monolayered, multiple-monolayered, polylayered and voussoir tesserae; new histological data, including thin sections of TCC in several Palaeozoic taxa, and new proposals for ways in which various characters and states (many of which are defined here for the first time) could be applied in future phylogenetic analyses of chondrichthyan fishes. It can be concluded that many, but not all, of the unique attributes of modern TCC evolved by the Early Devonian (ca. 400 before present (bp)). The globular calcified cartilage reported in Silurian sinacanthids and the so-called subtessellated perichondral biomineralization (with irregular and ill-defined geometries of a layer or layers of calcified cartilage blocks) of certain extinct "acanthodians" (e.g., Climatius, Ischnacanthus, Cheiracanthus) could represent evolutionary precursors of TCC, which seems to characterize only part of the chondrichthyan total group. It is hypothesized that heavily biomineralized "layer-cake" TCC in certain Palaeozoic chondrichthyans perhaps served a dual physiological role, as a phosphate sink and in providing increased skeletal density in very large (>7 m) Devonian-Permian marine sharks such as ctenacanths and as an adaptation to calcium-deficient environments among Permo-Carboniferous non-marine sharks such as xenacanths. By contrast, the equivalent tissue in modern elasmobranchs probably serves only to reinforce regions of cartilage (mostly in the jaws) subjected to high loading. It is also noted that much of the variation observed in tesseral architecture (including localized remodelling), ultrastructure and histology in modern and extinct chondrichthyans is confined to the perichondrally facing cap zone (where Type-1 collagen matrix predominates in modern TCC), whereas the main body of the tessera (where Type-2 collagen matrix predominates) exhibits comparatively little evidence of remodelling and histological or structural variation.

First evidence of a functional spiracle in stem chondrichthyan acanthodians, with the oldest known elastic cartilage.

Spiracles are a general character of gnathostomes (jawed fishes), being present in antiarch placoderms, commonly regarded as the most basal gnathostome group. The presence of spiracular tubes in acanthodians has been deduced from grooves on the neurocranium of the derived acanthodiform Acanthodes bronni from the Permian of Germany, but until now these tubes were presumed to lack an external opening, rendering them non-functional. Here we describe the external spiracular elements in specimens of the Middle Devonian acanthodiforms Cheiracanthus murchisoni, Cheiracanthus latus and Mesacanthus pusillus from northern Scotland, and the internal structure of these elements in C. murchisoni, demonstrating that the spiracle in acanthodiforms differed from all known extant and extinct fishes in having paired cartilage-pseudobranch structures. This arrangement represents a transitional state between the presumed basal gnathostome condition with an unconstricted first gill slit (as yet not identified in any fossil) and the derived condition with a spiracle and a single pseudobranch derived from the posterior hemibranch of the mandibular arch. We identify the main tissue forming the pseudobranch as elastic cartilage, a tissue previously unrecorded in fossils.

First shark from the Late Devonian (Frasnian) Gogo Formation, Western Australia sheds new light on the development of tessellated calcified cartilage.

BACKGROUND: Living gnathostomes (jawed vertebrates) comprise two divisions, Chondrichthyes (cartilaginous fishes, including euchondrichthyans with prismatic calcified cartilage, and extinct stem chondrichthyans) and Osteichthyes (bony fishes including tetrapods). Most of the early chondrichthyan ('shark') record is based upon isolated teeth, spines, and scales, with the oldest articulated sharks that exhibit major diagnostic characters of the group--prismatic calcified cartilage and pelvic claspers in males--being from the latest Devonian, c. 360 Mya. This paucity of information about early chondrichthyan anatomy is mainly due to their lack of endoskeletal bone and consequent low preservation potential. METHODOLOGY/PRINCIPAL FINDINGS: Here we present new data from the first well-preserved chondrichthyan fossil from the early Late Devonian (ca. 380-384 Mya) Gogo Formation Lägerstatte of Western Australia. The specimen is the first Devonian shark body fossil to be acid-prepared, revealing the endoskeletal elements as three-dimensional undistorted units: Meckel's cartilages, nasal, ceratohyal, basibranchial and possible epibranchial cartilages, plus left and right scapulocoracoids, as well as teeth and scales. This unique specimen is assigned to Gogoselachus lynnbeazleyae n. gen. n. sp. CONCLUSIONS/SIGNIFICANCE: The Meckel's cartilages show a jaw articulation surface dominated by an expansive cotylus, and a small mandibular knob, an unusual condition for chondrichthyans. The scapulocoracoid of the new specimen shows evidence of two pectoral fin basal articulation facets, differing from the standard condition for early gnathostomes which have either one or three articulations. The tooth structure is intermediate between the 'primitive' ctenacanthiform and symmoriiform condition, and more derived forms with a euselachian-type base. Of special interest is the highly distinctive type of calcified cartilage forming the endoskeleton, comprising multiple layers of nonprismatic subpolygonal tesserae separated by a cellular matrix, interpreted as a transitional step toward the tessellated prismatic calcified cartilage that is recognized as the main diagnostic character of the chondrichthyans.

Oldest near-complete acanthodian: the first vertebrate from the Silurian Bertie Formation Konservat-Lagerstätte, Ontario.

BACKGROUND: The relationships between early jawed vertebrates have been much debated, with cladistic analyses yielding little consensus on the position (or positions) of acanthodians with respect to other groups. Whereas one recent analysis showed various acanthodians (classically known as 'spiny sharks') as stem osteichthyans (bony fishes) and others as stem chondrichthyans, another shows the acanthodians as a paraphyletic group of stem chondrichthyans, and the latest analysis shows acanthodians as the monophyletic sister group of the Chondrichthyes. METHODOLOGY/PRINCIPAL FINDINGS: A small specimen of the ischnacanthiform acanthodian Nerepisacanthus denisoni is the first vertebrate fossil collected from the Late Silurian Bertie Formation Konservat-Lagerstätte of southern Ontario, Canada, a deposit well-known for its spectacular eurypterid fossils. The fish is the only near complete acanthodian from pre-Devonian strata worldwide, and confirms that Nerepisacanthus has dentigerous jaw bones, body scales with superposed crown growth zones formed of ondontocytic mesodentine, and a patch of chondrichthyan-like scales posterior to the jaw joint. CONCLUSIONS/SIGNIFICANCE: The combination of features found in Nerepisacanthus supports the hypothesis that acanthodians could be a group, or even a clade, on the chondrichthyan stem. Cladistic analyses of early jawed vertebrates incorporating Nerepisacanthus, and updated data on other acanthodians based on publications in press, should help clarify their relationships.

X-ray microtomography of 410 million-year-old optic capsules from placoderm fishes.

The structure of two small ossified optic capsules from mid-Palaeozoic placoderm fishes has been revealed in fine detail, by the use of X-ray microtomography analysis and 3D visualisation software. These two specimens are 410 million-year-old; they were collected from an Early Devonian (Lochkovian) limestone in central New South Wales, and are the oldest known optic capsules from jawed fishes. The capsules show attachment areas for seven extrinsic eye muscles, rather than the six until recently deemed universal for gnathostomes. The analysis also revealed structures within the ossified cartilage which covered the medial surface of the eyeball, including nerve tracts, vascular canals, and possibly a choroid rete mirabile.