Bone-like features in skate suggest a novel elasmobranch synapomorphy and deep homology of trabecular mineralization patterns

摘要

Bone is a defining characteristic of the vertebrate skeleton, and while chondrichthyans (sharks, skates, and other cartilaginous fishes) are vertebrates, they are hypothesized to have lost the ability to make bone during their evolution. Multiple descriptions of a bone-like tissue in neural arches of vertebrae in various shark species (selachians), however, challenge this hypothesis. Here, we extend this argument by analyzing vertebrae of two members of the batoids (the little skate Leucoraja erinacea and Eaton's skate Bathyraja eatonii), the sister group to selachians within elasmobranchs. Micro-CT images showed a bone-like mineralization pattern in neural arches of each skate species, and histological analyses confirmed that this bone-like tissue surrounded a cartilage core, exactly as described in sharks. Another mineralization pattern identified in skate vertebrae was distinct from the polygonal tesseral and areolar patterns that classically are associated with the chondrichthyan endoskeleton. Many regions of the vertebrae, including the neural spine and transverse processes, showed this perichondral mineralization pattern, termed here trabecular tesseral. Other than the cartilage core of the neural arch, all mineralized tissues in skate vertebrae had flattened cells surrounded by matrix with bone-like histology. Analyses of quantitative microstructural parameters revealed that, compared to rat vertebrae, the bone-like mineralization pattern in the neural arches of skate vertebrae was more similar to compact bone than trabecular bone. In contrast, the thickness of the trabecular tesseral pattern was more similar to trabecular bone than compact bone of rat vertebrae. In conclusion, a bone-like tissue in neural arches of skate vertebrae appears to be a novel elasmobranch synapomorphy. We propose that the trabecular tesseral mineralization pattern in the skate might have deep homology to the mineralization pattern utilized in trabecular bone.