The enhanced dexterity of the human hand is unique among primates,an ability that is traditionally thought to have evolved in response totool-related behaviors and a release from the biomechanical constraints of locomotion in our bipedal hominin ancestors. However, recent fossil and archaeological evidence, as well as novel analyses, suggest that dexterity-related morphology and abilities evolved earlier than traditionally thought and that fossil hominins used their hands for locomotion until much later than presumed. Behavior evolves faster than morphology, and it is not yet clear how these different functional demands were potentially accommodated within the morphology of the hominin hand. We aim to improve our understanding of how our fossil ancestors used their hands for both locomotion and manipulation through the investigation of plastic aspects of bone morphology–internal trabecular (cancellous) bone–that can better reflect behavior during life than external morphology alone. We interpret variation in trabecular structure, focusing on metacarpals, within a comparative great ape context via pressure analyses of bonobo (Pan paniscus) arboreal locomotion and human tool-use. We then incorporate these biomechanical data into validated musculoskeletal models of the bonoboand human third digit to estimate in vivo metacarpophalangeal joint loads. Finally, using microFE-based inverse bone remodeling, we demonstrate how metacarpal trabecular structure reflects differences in joint loading across great apes, which can ultimately inform our reconstructions testing if and how different fossil hominins used their handsfor both tool use and climbing. This research is funded by the EuropeanResearch Council Starting Grant 336301, as well as the Fyssen Founda-tion (AB), British Academy (AK) and the University of Kent Vice Chancellor Fellowship (EEB, KD).