The evolution and biological correlates of hand preferences in anthropoid primates

Abstract

The evolution of human right-handedness has been intensively debated for decades. Manual lateralization patterns in non-human primates have the potential to elucidate evolutionary determinants of human handedness, but restricted species samples and inconsistent methodologies have so far limited comparative phylogenetic studies. By combining original data with published literature reports, we assembled data on hand preferences for standardized object manipulation in 1786 individuals from 38 species of anthropoid primates, including monkeys, apes, and humans. Based on that, we employ quantitative phylogenetic methods to test prevalent hypotheses on the roles of ecology, brain size, and tool use in primate handedness evolution. We confirm that human right-handedness represents an unparalleled extreme among anthropoids and found taxa displaying population-level handedness to be rare. Species-level direction of manual lateralization was largely uniform among non-human primates and did not strongly correlate with any of the selected biological predictors, nor with phylogeny. In contrast, we recovered highly variable patterns of hand preference strength, which show signatures of both ecology and phylogeny. In particular, terrestrial primates tend to display weaker hand preferences than arboreal species. These results challenge popular ideas on primate handedness evolution, including the postural origins hypothesis. Furthermore, they point to a potential adaptive benefit of disparate lateralization strength in primates, a measure of hand preference that has often been overlooked in the past. Finally, our data show that human lateralization patterns do not align with trends found among other anthropoids, suggesting that unique selective pressures gave rise to the unusual hand preferences of our species.

eLife digest

About 90% of humans are right-handed. While it is known that handedness is caused by certain brain regions that are specialized in one of the two hemispheres, it is not clear how this evolved or why right-handedness dominates. Several hypotheses have been proposed to explain this extreme preference, including the use of tools, the larger size of the human brain, and the fact that humans live primarily on the ground.

Many researchers have regarded the extreme population-wide preference for using the right hand as being uniquely human. However, handedness had not been studied in a standardized manner across a wide range of primates. To fill this gap in our knowledge and understand how handedness may have evolved in monkeys and apes, Caspar et al. used existing data and new experimental observations to create a large dataset of hand preference.

This dataset illustrates how approximately 1800 primates across 38 species retrieve mashed food from a tube (or pieces of paper in the case of humans). Similar to humans, some species of monkey only had small proportions of ambidextrous individuals. However, no species had an extreme preference for using one specific hand the way humans do. Interestingly, Caspar et al. found that the presence of tool use as well as brain size were not associated with the degree of handedness in species. However, ground-living primates tended to show weaker individual preferences for a specific hand than tree-living species, with humans being a notable exception to the trend.

These findings confirm that humans do exhibit exceptional right-handedness, being unique among primates. While the results cannot explain the cause of this behaviour, they do help to rule out some of the theories that aim to explain how this preference evolved. This will be of interest to researchers studying the origins of human behaviour as well as the emergence of asymmetries in the brain.