Adaptive landscapes challenge the “lateral-to-sagittal” paradigm for mammalian vertebral evolution

The evolution of mammals from their extinct forerunners, the non-mammalian synapsids, is one of the most iconic locomotor transitions in the vertebrate fossil record. In the limb skeleton, the synapsid-mammal transition is traditionally characterized by a shift from a sprawling limb posture, resembling that of extant reptiles and amphibians, to more adducted limbs, as seen in modern-day mammals. Based on proposed postural similarities between early synapsids and extant reptiles, this change is thought to be accompanied by a shift from ancestral reptile-like lateral bending to mammal-like sagittal bending of the vertebral column. To test this “lateral-to-sagittal” evolutionary paradigm, we used combinatorial optimization to produce functionally informed adaptive landscapes and determined the functional trade-offs associated with evolutionary changes in vertebral morphology. We show that the synapsid adaptive landscape is different from both extant reptiles and mammals, casting doubt on the reptilian model for early synapsid axial function, or indeed for the ancestral condition of amniotes more broadly. Further, the synapsid-mammal transition is characterized by not only increasing sagittal bending in the posterior column but also high stiffness and increasing axial twisting in the anterior column. Therefore, we refute the simplistic lateral-to-sagittal hypothesis and instead suggest the synapsid-mammal locomotor transition involved a more complex suite of functional changes linked to increasing regionalization of the backbone. These results highlight the importance of fossil taxa for understanding major evolutionary transitions. [Display omitted] •“Lateral-to-sagittal” paradigm is too simple to explain mammal vertebral evolution•Extant reptiles are a poor functional model for extinct non-mammalian synapsids•Non-mammalian synapsid vertebral joints are characterized by high stiffness•Mammal backbone evolution involved acquisition of multiple vertebral functions Jones et al. disprove the long-held idea that mammal backbone evolution involved a transition from reptile-like lateral bending to sagittal bending. They show that the spines of extinct mammal forerunners functioned differently to reptiles and that increasing sagittal bending, twisting, and stiffness were all hallmarks of mammal evolution.