Skeletons of swiftly swimming sharks: Three-dimensional analysis of lamniform vertebral morphology and mineral architecture.

Abstract

Order Lamniformes consists of 15 extant shark species that are ecologically diverse and utilize different swimming modes and speeds. Family Lamnidae includes the shortfin mako, porbeagle, and white shark which are fast, athletic sharks that swim using oscillations confined to the caudal body and fin. Other lamniforms, like the common thresher shark (Alopiidae), sand tiger (Carchariidae), and basking shark (Cetorhinidae), swim via oscillations that begin anteriorly, impacting a greater proportion of the axial body. Swimming oscillations subject the body to repeated bending cycles, including the cartilaginous vertebral column, the main longitudinal axis of the body. Vertebrae are mineralized with the amount and arrangement varying among species. We investigated morphological variation in lamniform shark vertebrae to understand adaptations to locomotive demands among species. We examined vertebral morphology and mineral architecture of lamniform centra across three body regions (anterior, middle, and posterior) and among six species (shortfin mako, porbeagle, sand tiger, white, common thresher, and basking shark) through micro-computed tomography scans. We analyzed morphology and structure of 139 vertebrae from 24 sharks using meristics, principal component analyses, and 3D landmark-based geometric morphometrics. Through 3D quantification, we identified regional patterns in centrum size and mineral amount which also varied across shark families. In the lamnids, centra morphometrics are largest in the mid-body and decrease posteriorly simultaneous with increased counts of lamellae. Together, these trends suggest the middle body region is stabilized while allowing for rapid lateral oscillations at the precaudal pit. Cranio-caudally compressed centra with high quantities of lamellae were characteristic for common thresher shark centra, likely to support loading in multiple planes from extreme axial bending during tail-whipping behaviors. In the sand tiger and basking shark, we quantified opposing trends-large anterior centra decreased in size along the column with reduced mineralization for slow swimming. We calculated scaling relationships of mineral volume with shark size and identified a negative allometric relationship, suggesting adult sharks may adapt internal architecture rather than contributing to overall centrum size. This comprehensive analysis of calcified structure in lamniform shark centra provides a greater understanding of skeletal tissues and the adaptation of mineralized cartilage to support swimming and ecological needs.