The shoulder girdle of early chondrichthyans grew by skeletal remodelling

A distinct shoulder region, defined by endoskeletal and dermal girdles and associated pectoral musculature, is a major evolutionary adaptation of jawed vertebrates. In teleost model species, the large (macromeric) pectoral dermal bones can be derived from multiple embryonic tissues, identifying the shoulder of osteichthyans as a developmentally complex area at the head-trunk boundary. The absence of bone in living chondrichthyans makes Palaeozoic stem groups capable of dermal ossification key to understanding the underpinnings of skeletal growth in the shoulder of crown gnathostomes (osteichthyans and chondrichthyans). Here, using synchrotron X-ray tomography we demonstrate that individual pectoral plates in the oldest unequivocal jawed vertebrate, the Silurian (c. 439 Mya) chondrichthyan Fanjingshania renovata, develop from five separate growth centres. These centres correspond to pectoral bony spines that fuse neighbouring dermal scales into a pinnal plate and their expansion is accompanied by cyclical resorption and remodelling of bone and dentine. Our phylogenetic analyses support an interpretation of these processes as crown and stem gnathostome characters that co-occur only in the shoulder girdle of stem chondrichthyans. The systematic hard tissue remodelling in Fanjingshania reveals an unexpected growth dynamic within chondrichthyans that relates to the formation of a macromeric skeleton through integration of modular elements.