Natural selection, genetic drift, and trait correlation shaped hominin midfoot evolution

The foot has undergone significant morphological change throughout the hominin lineage as our extinct relatives evolved to walk upright. The midfoot displays key adaptations for terrestrial bipedal locomotion, and is therefore considered a target of natural selection. Prior work suggests that early selection for bipedalism targeted the lateral elements of the foot, but that later, among australopiths, these elements were less morphologically diverse, and less influenced by directional selection than medial elements. Here, we apply methods from quantitative genetics to test which evolutionary processes (directional vs. stabilizing selection) shaped hominin midfoot diversification under a null hypothesis of genetic drift. Results demonstrate that the lateral midfoot may have been the primary target of selection for bipedalism in Ardipithecus ramidus, but that later in the hominin lineage, there is no consistent evidence that the lateral elements were less influenced by directional selection. Instead, we find a complex interaction of evolutionary processes shaping midfoot diversification, characterized by genetic drift, directional selection, and indirect responses to selection based on correlation between different elements. In sum, we emphasize that narratives of the evolution of bipedalism should consider the role of genetic drift and correlation among skeletal elements, as both have been historically underestimated.