Morphological, Histological, And Developmental Features Of Perichondral Bone In Skates And Sharks Suggest That Modern Cartilaginous Fishes Make Bone

Bone is a mineralized (or calcified) tissue type and a defining feature of the vertebrate skeleton. Ancestral vertebrates made bone and most modern vertebrates including bony fishes and tetrapods retain bone. However, bone has never been characterized in modern chondrichthyans (sharks, skates, rays, and chimaeras), and modern chondrichthyans are hypothesized to have lost the ability to make bone during their evolution. Previous studies show that sharks have mineralized tissues with some morphological and histological features that are consistent with vertebrate perichondral bone. These mineralized tissues in sharks have been described as bone-like and occur in neural arches and a specific histological region (i.e., cap zone) of discretely mineralized tesserae. While these observations in sharks challenge the hypothesis that modern chondrichthyans lack bone, it remains debated whether other modern chondrichthyans like skates and chimaeras have bone-like tissues. Because bone-like tissues have been characterized mostly in adult sharks, it is not known whether important developmental features of perichondral bone such as cartilage maturation is demonstrated by bone-like tissues. Besides bone-like tissues, chondrichthyans also display a unique areolar mineralized tissue in the vertebral body (centrum). These chondrichthyan mineralized tissues display distinct mineralization patterns such as a classic polygonal pattern of tesserae, a compact bone-like pattern of neural arches, and a compact pattern of areolar mineralized tissue. These chondrichthyan mineralization patterns have been described in sharks and skates, but relevant data from chimaeras needed to assess whether all groups of modern chondrichthyans demonstrate these morphological features are lacking. This thesis addresses these and other knowledge gaps in the skeletal biology of modern chondrichthyans by testing the hypothesis that bone-like tissues are shared by modern chondrichthyans and are homologous to perichondral bone in other modern vertebrates. Comparative morphology and embryology were the two main approaches adopted to test this hypothesis. Specifically, mineralized tissues in two skate species (the little skate Leucoraja erinacea and the Eaton’s skate Bathyraja eatonii), a shark (the catshark Scyliorhinus canicular), and a chimaera (the spotted ratfish Hydrolagus colliei) were characterized using desktop and synchrotron micro-CT imaging, histological, histochemical, and immunofluorescence assays. Micro-CT renderings showed a bone-like mineralization pattern in neural arches of the skates and the shark, but this was absent in neural arches of the spotted ratfish. Micro-CT renderings and histological analyses of tesserae showed that the bone-like cap zone was present only in the skates, and the polygonal tesseral mineralization pattern was associated with large and laterally extensive bone-like cap zones. Another mineralization pattern described herein as trabecular tesseral was characterized in several endoskeletal regions of the skates, the catshark, and the spotted ratfish. The trabecular tesseral pattern was morphologically distinct from the polygonal tesseral pattern which is classically associated with the chondrichthyan endoskeleton. Micro-CT renderings and histological data also showed that areolar mineralized tissue, which has been described in only sharks and skates, was also present in the spotted ratfish. Perichondral bone formation in other modern vertebrates is driven by cartilage maturation. Developmental data from the little skate showed that the main histological features of cartilage maturation, such as chondrocyte hypertrophy and initiation of matrix mineralization by hypertrophic chondrocytes, were associated with the development of bone-like tissue in neural arches. In addition to limited reports of bone-like tissues in sharks, data in this thesis showed that other modern chondrichthyans like skates have bone-like tissues. Developmental features of perichondral bone demonstrated by neural arch bone-like tissue suggest that bone-like tissues and perichondral bone are homologous.

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