An integrative model of chimaera jaw links mechanical stress to localized cartilage mineralization

Chondrichthyans possess a tessellated cartilage which is characterized by a layer of mineralized minute plates (i.e., the tesserae) that sheathe soft cartilage. This tissue type composes most of the endoskeleton (including the fins, the branchial arches and the skull). Using the example of the adaptation of Holocephalans to durophagy, here we aim to test the capacity of the tessellated cartilage to strengthen in response to mechanical stress. Relying on an integrative approach (i.e., cranial muscle dissections, finite element models, histological cross sections and embryologic data), we strongly argue that chondrichthyans are capable of calcifying their endoskeleton in response to mechanical stress by mimicking bone microstructures (i.e., cortical thickness and formation of trabeculae). In the absence of bone cells, this mechanism relies on the calcification of Liesegang waves around the chondrocytes that might possess mechanosensing properties. This cartilage ability may have been inherited from the early jawless vertebrates before it played a critical role in the evolution of chondrichthyans who subsequently lost the bony skeleton before thriving through 400 million years and surviving four major extinction crises. Indeed, this ability to mineralize cartilage would have allowed to grow a high diversity of mechanically demanding adaptations within “bone-less” vertebrates.