Lizards in chain mail: reconstructing the enigmatic past of dermal armour in squamate reptiles

Abstract Osteoderms, bone plates in the skin, occur widely but inconsistently throughout the tetrapod tree of life. Their evolutionary history remains poorly understood. Squamate reptiles (lizards and snakes) represent an ideal study system. It is often assumed that different squamate lineages acquired their osteoderms independently. However, this had yet to be tested. Covering 320 Myr of reptile evolution, we present here an ancestral character state reconstruction for the phenotypic osteoderm expression in 643 taxa of all major squamate crown-groups, including 70 extinct and outgroup representatives. Osteoderms were largely acquired in a series of events during the Late Jurassic and Early Cretaceous. Subsequent rate deceleration and absence of reversions ultimately led towards a state of evolutionary stability. As an exception, we reconstructed the loss of osteoderms in the varanid stem-lineage, and secondary re-acquisitions in Australopapuan varanids during an acquisition series in the Miocene. We discuss how lifestyle, locomotion, and biogeographical history may have driven these events. Foremost, we demonstrate that squamate osteoderm expression is the product of multiple independent acquisitions. This solidifies the foundation for future discussions on the underlying evolutionary mechanisms. Our findings also contribute towards a better understanding of the selective pressures and evolutionary trajectories that shaped present-day reptile biodiversity.