Evolutionary Origins of Mammalian Axial Function Revealed through Digital Bending Experiments

Abstract

The origin of mammals from non‐mammalian synapsids represents an iconic locomotor transition, often described as shift from reptile‐like sprawling limbs and extensive lateral movements of the backbone to upright limbs and sagittal backbone movements that enhance mammal specific locomotor behaviors. However, recent research in comparative anatomy has called into question the lateral‐to‐sagittal functional shift, instead suggesting that vertebral morphology in basal synapsids implies a distinct functional regime not observed in extant sprawling reptiles and represents a unique ancestral condition from which mammals evolved. To investigate this idea further, we used Autobend,a novel, experimentally validated technique for estimating vertebral osteological range of motion (oROM) from skeletons using digital modeling. We applied Autobendto seven extant mammal and reptile species and 11 exceptionally preserved non‐mammalian synapsids to estimate vertebral oROM and intervertebral joint stiffness. Results revealed a clear distinction between extant mammals and reptiles in oROM, with reptiles emphasizing lateral bending and mammals sagittal bending as expected. While most extant taxa exhibited relatively similar levels of stiffness in lateral and sagittal directions, extant lizards and salamanders displayed much more compliance in lateral bending and lower stiffness overall, in keeping with their observed axial kinematics. Conversely, most non‐mammalian synapsids displayed an intermediate condition, with stiffer intervertebral joints than extant lizards, crocodiles, and therian mammals, but similar to the pattern recovered for the modern tuatara. The mammalian condition of sagittal mobility accompanied by axial twisting in the anterior column is first observed in the crownward tritylodontid cynodont Kayentatherium. Together, these results support previous morphology‐based assertions of a distinctive ancestral vertebral function for synapsids characterized by high stiffness without the specialization for lateral bending of extant lizards or the sagittal bending and twisting observed in mammals today. This indicates a more limited role for the axial skeleton in terrestrial locomotion relative to extant groups, and a greater focus on body support than propulsion during the initial stages of synapsid evolution. This stage was followed by the evolution of mammalian‐type mobility patterns in cynodonts, and a secondary reduction in axial stiffness in certain therian clades. Given the strong association between sagittal bending and asymmetric gaits in mammals, these results provide an important first step in reconstructing the evolution of synapsid locomotor patterns.