The Central Role of Small Vertical Substrates for the Origin of Grasping in Early Primates

The manual and pedal grasping abilities of primates, characterized by an opposable hallux, flat nails, and elongated digits, constitute a unique combination of features that likely promoted their characteristic use of arboreal habitats. These hand and foot specificities are central for understanding the origins and early evolution of primates and have long been associated with foraging in a fine-branch milieu. However, other arboreal mammals occupy similar niches, and it remains unclear how substrate type may have exerted a selective pressure on the acquisition of nails and a divergent pollex/hallux in primates or in what sequential order these traits evolved. Here, we video-recorded 14,564 grasps during arboreal locomotion in 11 primate species (6 strepsirrhines and 5 platyrrhines) and 11 non-primate arboreal species (1 scandentian, 3 rodents, 3 carnivorans, and 4 marsupials). We quantified our observations with 19 variables to analyze the effect of substrate orientation and diameter on hand and foot postural repertoire. We found that hand and foot postures correlate with phylogeny. Also, primates exhibited high repertoire diversity, with a strong capability for postural adjustment compared to the other studied groups. Surprisingly, nails do not confer an advantage in negotiating small substrates unless the animal is large, but the possession of a grasping pollex and hallux is crucial for climbing small vertical substrates. We propose that the divergent hallux and pollex may have resulted from a frequent use of vertical plants in early primate ecological scenarios, although nails may not have resulted from a fundamental adaptation to arboreal locomotion.